Pelvic Lymphadenectomy in Gynecologic Oncology—Signiﬁcance of Anatomical Variations

diagnostics

Review Pelvic Lymphadenectomy in Gynecologic Oncology—Signiﬁcance of Anatomical Variations

Stoyan Kostov 1 , Yavor Kornovski 1, Stanislav Slavchev 1 , Yonka Ivanova 1, Deyan Dzhenkov 2 , Nikolay Dimitrov 3 and Angel Yordanov 4,*

1 Department of Gynecology, Medical University Varna “Prof. Dr. Paraskev Stoyanov”, 9002 Varna, Bulgaria; [email protected] (S.K.); [email protected] (Y.K.); [email protected] (S.S.); [email protected] (Y.I.) 2 Department of General and Clinical Pathology, Forensic Medicine and Deontology, Division of General and Clinical Pathology, Faculty of Medicine, Medical University Varna “Prof. Dr. Paraskev Stoyanov”, 9002 Varna, Bulgaria; [email protected] 3 Department of Anatomy, Faculty of Medicine, Trakia University, 6000 Stara Zagora, Bulgaria; [email protected] 4 Department of Gynecologic Oncology, Medical University Pleven, 5800 Pleven, Bulgaria * Correspondence: [email protected]

Abstract: Pelvic lymphadenectomy is a common surgical procedure in gynecologic oncology. Pelvic lymph node dissection is performed for all types of gynecological malignancies to evaluate the extent of a disease and facilitate further treatment planning. Most studies examine the lymphatic spread, the prognostic, and therapeutic significance of the lymph nodes. However, there are very few studies describing the possible surgical approaches and the anatomical variations. Moreover, a correlation between anatomical variations and lymphadenectomy in the pelvic region has never been discussed in medical literature. The present article aims to expand the limited knowledge of the anatomical variations in the pelvis. Anatomical variations of the ureters, pelvic vessels, and nerves and their significance to pelvic lymphadenectomy are summarized, explained, and illustrated. Surgeons should Citation: Kostov, S.; Kornovski, Y.; be familiar with pelvic anatomy and its variations to safely perform a pelvic lymphadenectomy. Slavchev, S.; Ivanova, Y.; Dzhenkov, Learning the proper lymphadenectomy technique relating to anatomical landmarks and variations D.; Dimitrov, N.; Yordanov, A. Pelvic may decrease morbidity and mortality. Furthermore, accurate description and analysis of the majority Lymphadenectomy in Gynecologic Oncology—Significance of of pelvic anatomical variations may impact not only gynecological surgery, but also spinal surgery, Anatomical Variations. Diagnostics urology, and orthopedics. 2021, 11, 89. https://doi.org/ 10.3390/diagnostics11010089 Keywords: anatomical landmarks; anatomical variations; pelvic lymph nodes; gynecologic oncology; pelvic lymphadenectomy Received: 28 November 2020 Accepted: 5 January 2021 Published: 7 January 2021 1. Introduction Publisher’s Note: MDPI stays neu- Pelvic lymph node dissection (PLND) is a common surgical procedure in gynecologic tral with regard to jurisdictional clai- oncology [1]. The lymphatic system is the primary dissemination pathway for gynecologi- ms in published maps and institutio- cal malignancies. PLND is applied for cancer staging, prognosis, surgical, and postoper- nal affiliations. ative management [2,3]. PLND is performed for all types of gynecological malignancies to evaluate the extent of a disease and facilitate further treatment planning. Additionally, PLND is beneficial in cases where removing metastatic lymph nodes improves overall Copyright: © 2021 by the authors. Li- survival and disease-free survival [4]. Most studies examine the lymphatic spread, the censee MDPI, Basel, Switzerland. prognostic, and therapeutic significance of pelvic lymph nodes. However, there are very This article is an open access article few studies describing the possible surgical approach, dissection techniques and anatomi- distributed under the terms and con- cal variations [5]. There is limited information and disagreement on lymph nodes location, ditions of the Creative Commons At- groups, and overall number [6]. tribution (CC BY) license (https:// Moreover, a correlation between anatomical variations and PLND in the pelvic region creativecommons.org/licenses/by/ has never been discussed in medical literature. Surgeons should be familiar with pelvic 4.0/).

Diagnostics 2021, 11, 89. https://doi.org/10.3390/diagnostics11010089 https://www.mdpi.com/journal/diagnostics Diagnostics 2021, 11, x FOR PEER REVIEW 2 of 27

pelvic anatomy and its variations to safely perform PLND. Learning the proper lymphadenectomy technique relating to anatomical landmarks and variations may decrease mor- Diagnostics 2021, 11, 89 bidity and mortality [7]. The present article aims to define, detail,2 of 27 and summarize the anatomic landmarks during PLND in gynecologic oncology. Furthermore, a summary of the anatomymost common and its variations anatomical to safely perform variations PLND. Learning (of nerves, the proper vessels, lymphadenectomy ureters) and potential complica- techniquetions related relating toto anatomical PLND in landmarks the pelvic and variations region mayare decreaseclearly morbidity defined. and mortality [7]. The present article aims to deﬁne, detail, and summarize the anatomic landmarks during PLND in gynecologic oncology. Furthermore, a summary of the most common2. Pelvic anatomical Lymph variations Nodes (of and nerves, Regions vessels, ureters) and potential complications related to PLND in the pelvic region are clearly deﬁned. Knowledge of the anatomical localization of lymph node groups in the pelvis is es- 2.sential Pelvic Lymph for the Nodes effectiveness and Regions and safety of lymphadenectomy [8]. The pelvic lymph nodes Knowledge of the anatomical localization of lymph node groups in the pelvis is essentialand the for connecting the effectiveness lymphatic and safety of channels lymphadenectomy commu [8].nicate The pelvic with lymph the venous system; the lym- nodesphatic and system the connecting embryologically lymphatic channels develops communicate from with vascular the venous system;plexuses, the arising from the venous lymphatic system embryologically develops from vascular plexuses, arising from the venoussystem system [3]. [ 3].The The anatomical anatomical localization localization of the major of groupsthe major and sub-groups groups of and sub-groups of pelvic pelviclymph lymph nodes nodes is summarizedsummarized in Figures in Figures1–3[2,6,8–15 1–3]. [2,6,8–15].

FigureFigure 1. Common 1. Common iliac lymph iliac nodes lymph classiﬁcation nodes (open classification surgery). 1. Lateral—between (open surgery). lateral part1. Lateral—between lateral part ofof CIV CIV and medialand partmedial of psoas part major of muscle, psoas2. medial—medial major muscle, to CIV 2. and medial—medial CIA, 3. middle—located to CIV and CIA, 3. middle— in the lumbosacral fossa, 4. subaortic—below aortic bifurcation, 5. promontory—at the promontory. AA—abdominallocated in the aorta, lumbosacral IVC—inferior vena fossa, cava, RV—right4. subaortic—below renal vein, PMM—psoas aortic major bifurcation, muscle, 5. promontory—at the CIA—commonpromontory. iliac AA—abdominal artery, CIV—common iliac aorta, vein, Cr—cranial,IVC—inferior Ca—caudal, vena L—Left, cava, R—right. RV—right renal vein, PMM—psoas major muscle, CIA—common iliac artery, CIV—common iliac vein, Cr—cranial, Ca—caudal, L— Left, R—right.

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Figure 2. External iliac lymph nodes classification (embalmed cadaver). 1. Lateral—lateral to exter- Figure 2. External iliac lymph nodes classiﬁcation (embalmed cadaver). 1. Lateral—lateral to external iliacnal artery,iliac artery,2. middle—medial 2. middle—medial to the EIA toand the lateralEIA and to the lateral EIV, 3.tomedial—medial the EIV, 3. medial—medial to both external to both ex- Figureternal 2. iliac External vessels, iliac lymph 4. obturator—around nodes classification (embalmedthe obturator cadaver). nerve 1. Lateral—lateral and vessels, to5. exter- interiliac—at the level iliacnal iliac vessels, artery,4. 2.obturator—around middle—medial to the the EIA obturator and lateral nerve to the and EIV, vessels, 3. medial—medial5. interiliac—at to both ex- the level of CIAternalof CIA bifurcation, iliac bifurcation, vessels, between 4. obturator—around between the EIA the and EIA the IIA. and obtu PMM—psoas IIA.rator PMM—nerve and majorpsoas vessels, muscle, major 5. interiliac—at muscle, EIA—external EIA—external the level iliac artery, iliac artery, EIV—externalofEIV—external CIA bifurcation, iliac iliac between vein, vein, IIA—internal the IIA—internal EIA and IIA. iliac PMM— artery, iliacpsoas arte Ur—ureter,ry, major Ur—ureter, muscle, U—uterus, EIA—external U—uterus, B—bladder, iliac B—bladder, artery, SRA—superior SRA—supe- EIV—external iliac vein, IIA—internal iliac artery, Ur—ureter, U—uterus, B—bladder, SRA—supe- rectalrior rectal artery, artery, Pr—promontorium, Pr—promontorium, R—rectum, R—rect L—left,um, r—right, L—left, Cr—cranial, r—right, Ca—caudal.Cr—cranial, Ca—caudal. rior rectal artery, Pr—promontorium, R—rectum, L—left, r—right, Cr—cranial, Ca—caudal.

Figure 3. Internal iliac lymph nodes classification (embalmed cadaver—left hemipelvis). 1. Ante- Figure 3. Internal iliac lymph nodes classiﬁcation (embalmed cadaver—left hemipelvis). 1. Anterior— rior—anterior to anterior division of internal iliac artery, 2. lateral sacral—close to the paired lateral anteriorsacral arteries, to anterior 3. gluteal—between division of internal superior iliac gluteal artery, and2. internallateral iliac sacral—close artery, 4. sacral to the (presacral)— paired lateral sacral arteries,along median3. gluteal—between sacral artery. CIA—common superior gluteal iliac ar andtery, internal IIA—internal iliac artery,iliac artery,4. sacral OA—obturator (presacral)—along medianartery,Figure UA—umbilical sacral3. Internal artery. artery,iliac CIA—common lymph IPA—internal nodes iliac pudend classification artery,al IIA—internalartery, IGA—inferior(embalmed iliac artery, glutealcadaver—left OA—obturator artery, LSA— hemipelvis). artery, 1. Ante- lateral sacral artery, ILA—iliolumbar artery, Pr—promontorium, S—sacrum. UA—umbilicalrior—anteriorartery, to anterior IPA—internal division pudendalof internal artery, iliac artery, IGA—inferior 2. lateral gluteal sacral—close artery, LSA—lateral to the paired lateral sacral artery, ILA—iliolumbar artery, Pr—promontorium, S—sacrum. sacralSome arteries, authors 3. includegluteal—between the subaortic superior and promontory gluteal lymph and internal nodes in iliac the medial artery, com- 4. sacral (presacral)— along median sacral artery. CIA—common iliac artery, IIA—internal iliac artery, OA—obturator mon Someiliac lymph authors group; include the obturator the subaortic lymph node ands promontorymay also be considered lymph nodes as partin of the medial medialartery, external UA—umbilical lymph group. artery, Moreover, IPA—internal in some articles,pudend anterior,al artery, lateral IGA—inferior sacral, and glu-gluteal artery, LSA— common iliac lymph group; the obturator lymph nodes may also be considered as part of teallateral internal sacral lymph artery, nodes ILA—iliolumbar are defined as junctional artery, Pr—promontorium, lymph nodes. [8,10,12]. S—sacrum. the medial external lymph group. Moreover, in some articles, anterior, lateral sacral, and gluteal internal lymph nodes are deﬁned as junctional lymph nodes [8,10,12]. Some authors include the subaortic and promontory lymph nodes in the medial common iliac lymph group; the obturator lymph nodes may also be considered as part of the

medial external lymph group. Moreover, in some articles, anterior, lateral sacral, and gluteal internal lymph nodes are defined as junctional lymph nodes. [8,10,12].

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Diagnostics 2021, 11, 89 4 of 27 We present an anatomical classification of the pelvic lymph nodes rather than a clinical one. Although the anatomical classification is rather complex, it better defines the localization of the pelvic lymph nodes. Furthermore, the anatomical variations, significant for theWe PLND, present are an anatomicalbetter described. classification of the pelvic lymph nodes rather than a clinical one. Although the anatomical classification is rather complex, it better defines the In medical literature and among surgeons, there are large variations and discrepan- localization of the pelvic lymph nodes. Furthermore, the anatomical variations, significant forcies the in PLND, the nomenclature are better described. of the pelvic lymph node regions [2]. The present article and the majorityIn medical of authors literature recognize and among the surgeons, following there pelvic are largelymph variations node regions: and discrepancies common iliac; ex- internal the nomenclature iliac; internal of iliac; the pelvicobturator; lymph and node sacral regions (or presacral) [2]. The present [5,7,12,13]. article Some and authors the add majorityparametrial, of authors mesorectal, recognize and the interiliac following regions, pelvic lymph while node others regions: include common tissue iliac;from the in- externalteriliac iliac;region internal to the iliac; external obturator; iliac and sacralobturator (or presacral) regions [and5,7,12 remove,13]. Some the authors tissue from the addparametrial parametrial, region mesorectal, together and with interiliac the parametrium regions, while during others radical include hysterectomy tissue from the [5,14,15]. interiliac region to the external iliac and obturator regions and remove the tissue from the parametrial3. Selective region PLND—Anatomical together with the parametriumLandmarks duringand Techniques radical hysterectomy [5,14,15]. 3. SelectiveThere PLND—Anatomicalare several surgical Landmarks procedures and relate Techniquesd to dissection of pelvic lymph nodes: sentinelThere lymph are several node surgical biopsy, procedures pelvic lymph related node to dissection sampling, of selective pelvic lymph lymphadenectomy nodes: sentineland complete lymph node (systematic) biopsy, pelvic PLND. lymph The node present sampling, article selective describes lymphadenectomy the systematic and lymphade- completenectomy (systematic) in which all PLND. pelvic The lymph present nodes, article drai describesning the the pelvic systematic organs, lymphadenec- have been removed tomy[1]. Cibula in which and all pelvicRustum lymph presented nodes, draining detailed the anatomic pelvic organs, boundaries have been for removed five pelvic [1]. lymph Cibulanode regions: and Rustum external presented iliac, detailed obturator, anatomic internal boundaries iliac, common for five pelviciliac, and lymph presacral node region regions: external iliac, obturator, internal iliac, common iliac, and presacral region [5]. [5]. Anatomic boundaries of the common PLND are: ventral—common iliac artery bifur- Anatomic boundaries of the common PLND are: ventral—common iliac artery bifurcations, dorsal—abdominalcations, dorsal—abdominal aorta bifurcation, aorta lateral—psoas bifurcation, major lateral—psoas muscle, medial—right-medial major muscle, medial— aspectright-medial of common aspect iliac of vessels, common left-mesoureter iliac vessels, [5 ].left-mesoureter Anatomic boundaries [5]. Anatomic of the external boundaries of andthe theexternal internal and PLND the includeinternal common PLND include iliac artery common bifurcation iliac dorsally, artery bifurcation the deep circum- dorsally, the flexdeep iliac circumflex vein ventrally, iliac andvein the ventrally, genitofemoral and th nervee genitofemoral of the psoas nerve major of muscle the psoas laterally. major mus- Thecle laterally. medial border The medial is the obliterated border is the umbilical obliterated artery umbilical ventrally andartery the ventrally ureter dorsally and the ureter (Figuresdorsally4 and(Figures5)[1,7 ,415 and]. 5) [1,7,15].

FigureFigure 4. 4.Common Common iliac iliac lymph lymph nodes nodes dissection—anatomic dissection—anatomic boundaries boundaries (open surgery, (open surgery, right side). right side). Dorsal—abdominalDorsal—abdominal aorta aorta bifurcation, bifurcation, ventral—common ventral—commo iliacn iliac artery artery bifurcation, bifurcation, medial—medial medial—medial as- aspectpect of of common iliaciliac vessels vessels (on (on the the left left side side is mesoureter), is mesoureter), lateral—psoas lateral—psoas major muscle. major AAB—muscle. AAB— abdominalabdominal aorta aorta bifurcation, bifurcation, PMM—psoas PMM—psoas major major muscle, muscle, CIAB—common CIAB—common iliac artery iliac bifurcation, artery bifurcation, M—medialM—medial aspect aspect of of common common iliac iliac vessels vessels on the on right the sideright (on side the (on left the side left is mesoureter), side is mesoureter), IVC— IVC— inferiorinferior vena vena cava, cava, CIA—common CIA—common iliac iliac artery, artery, CIV—common CIV—common iliac vein. iliac vein.

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FigureFigure 5.5.External External andand internalinternal iliaciliac lymphlymph nodes nodes dissection—anatomic dissection—anatomic boundariesboundaries (open(open surgerysurgery left pelvic sidewall). CIAB—common iliac artery bifurcation, ON—obturator nerve, DCIV—deep left pelvic sidewall). CIAB—common iliac artery bifurcation, ON—obturator nerve, DCIV—deep circumflex iliac vein, GFN—genitofemoral nerve, PMM—psoas major muscle, EIA—external iliac circumflex iliac vein, GFN—genitofemoral nerve, PMM—psoas major muscle, EIA—external iliac artery, EIV—external iliac vein, OV—obturator vein. The medial border is the ureter dorsally and artery,obliterated EIV—external umbilical iliacartery vein, ventrally. OV—obturator In the figure, vein. the The ureter medial is stretched border is medially the ureter for dorsally better expo- and obliteratedsure of the umbilicalvisible structures. artery ventrally. In the figure, the ureter is stretched medially for better exposure of the visible structures. 4. Systematic Open PLND—Surgical Technique and Steps [1,5,7,16–19] 4. Systematic Open PLND—Surgical Technique and Steps (1)(1) Peritoneal incision. After transecting (not aa necessarynecessary step)step) thethe roundround ligament,ligament, thethe peritoneum is incised incised in in a aposterior posterior (lateral (lateral and and parallel parallel to tothe the infundibulopelvic infundibulopelvic lig- ligament)ament) and and an an anterior anterior (ventrally (ventrally and and laterally laterally to to the the obliterated umbilicalumbilical artery)artery) direction. TheThe iliaciliac vesselsvessels are are exposed exposed from from the the bifurcation bifurcation of of the the aorta aorta to theto the inguinal ingui- ligament.nal ligament. (2)(2) IdentificationIdentification ofof thethe ureter.ureter. (3)(3) Lateral paravesical and and lateral lateral (Latzko’s (Latzko’s space) space) pararectal pararectal space space dissection. dissection. The The lat- lateraleral paravesical paravesical space space is isdissected dissected between between the the obliterated obliterated umbilical arteryartery andand thethe external iliaciliac vessels.vessels. Lateral pararectalpararectal spacespace isis dissecteddissected betweenbetween thethe internalinternal iliaciliac artery and the ureter. (4)(4) Genitofemoral nervenerve identification.identification. LateralLateral incisionincision toto thethe fasciafascia ofof thethe psoaspsoas musclemuscle isis preferable inin orderorder toto avoidavoid genitofemoralgenitofemoral nervenerve injury.injury. The The nerve nerve is is located located lateral lateral toto thethe externalexternal iliaciliac vesselsvessels andand sometimessometimes overlyingoverlying them.them. (5)(5) External iliac regionregion dissection:dissection: lateral andand medialmedial externalexternal iliaciliac vesselsvessels dissection.dissection. The dissectiondissection beginsbegins atat thethe originorigin ofof thethe externalexternal iliaciliac vesselsvessels andand finishesfinishes downdown toto thethe pointpoint wherewhere thethe deepdeep circumflexcircumflex iliaciliac veinvein crossescrosses overover thethe externalexternal iliaciliac artery.artery. (6)(6) Obturator region dissection. dissection. The The obturator obturator space space is isapproached approached by byretracting retracting the the ex- externalternal iliac iliac vessels vessels medially medially and and the the psoas psoas muscle muscle laterally, laterally, and and by bydissection dissection of the of theareolar areolar tissue tissue that that lies liesdirectly directly between between these these vessels vessels and andthe lateral the lateral pelvic pelvic wall. wall. The Theobturator obturator nerve nerve is identified. is identified. The Theprocedure procedure is followed is followed by lateral by lateral retraction retraction of the of theexternal external iliac iliac vessels vessels to toexpose expose the the obturator obturator space. space. Superficial Superficial obturatorobturator lymphlymph nodes areare dissecteddissected afterafter obturatorobturator nervenerve visualizationvisualization (obturator(obturator nervenerve stripping).stripping). For locallylocally advancedadvanced cervicalcervical cancercancer cases,cases, PLNDPLND continuescontinues withwith dissectiondissection ofof thethe deep obturator lymphlymph nodesnodes andand thethe glutealgluteal nodes.nodes. (7)(7) InternalInternal iliaciliac regionregion dissection. dissection. Lymph Lymph nodes nodes are are removed removed medially medially and and anteriorly anteriorly to theto the internal internal iliac iliac vessels. vessels. (8) Common iliac region dissection. Lymph nodes are removed ventrally and laterally from both common iliac vessels to the aortic bifurcation. Middle common iliac lymph

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(8) Common iliac region dissection. Lymph nodes are removed ventrally and laterally from both common iliac vessels to the aortic bifurcation. Middle common iliac lymph nodes are located in the lumbosacral fossa. It is approached by medial retraction of the common iliac vessels and lateral retraction of the psoas muscle. The obturator nerve, entering the obturator fossa through the body of the psoas muscle, the iliolumbar artery/vein, and the lumbosacral plexus are exposed. (9) Sacral (presacral) region dissection. After medial mobilization of the sigma-rectum, the peritoneum and the presacral fascia are incised medially to the right common iliac artery. Sacral lymph nodes, localized below the bifurcation of the abdominal aorta and inferior vena cava, in the triangle between the left and right common iliac vessels, are dissected [1,5,7,16–19].

5. Anatomical Landmarks and Anatomical Variations, Related to Systematic PLND Anatomy of the pelvic ureter. Identiﬁcation of the ureter is a necessary step during PLND for two reasons: to avoid injury and to serve as a medial landmark during PLND. The ureter is divided into abdominal, pelvic, and intramural segments [20]. According to Luschka’s law, the left ureter crosses the iliac artery 1.5 cm below the common iliac artery bifurcation, while the right ureter crosses the iliac artery 1.5 cm above the bifurcation. Therefore, the ureter enters the pelvic cavity by crossing the common iliac artery on the left side and the external iliac artery on the right [21,22]. Hence, the left ureter is located laterally to the internal iliac artery, whereas the right ureter is located medially to the right internal iliac artery. Surgeons should fully understand the anatomical relation between the ureter and iliac vessels. As the ureter enters the true pelvis, it runs caudally and medially to the ovarian vessels, reaching the bladder on the posterior leaf of the broad ligament [23].

6. Anatomical Variations of the Ureter, Related to PLND in Gynecologic Oncology (PLNDGO) There is a multitude of ureteral anomalies, but the following three groups are related to PLND in gynecologic oncology (PLNDGO): (A) Multiplication of ureter; (B) Ureteral diverticulum; (C) Unusual ureteral position—retro-iliac ureter. (A) Ureteral multiplication is a longitudinal segmentation of the ureter into two or more tubes. Multiplication may be complete, incomplete, bilateral, and unilateral (Figure6) . Ureteral duplication is the most common type of multiplication and occurs more commonly in women than in men (4–5% of the population). Incomplete duplications tend to be unilateral and more common than complete, whereas complete duplications are often bilateral [24–26]. Unilateral ureteral duplication is more common on the right ureter than on the left (Figure6)[25]. Surgical considerations. Ureteral multiplication increases the incidence of ureteral injury during PLND. Surgeons have to identify the course of the ureter as it crosses the pelvic brim and reaches the bladder. Injuries to the blood vessels of the ureters must be avoided, as duplicated ureters are usually contained within a single sheath and the associated blood supply could be interrupted [24,26]. Additionally, one of the duplicated ureters might be confused with vessel structures (artery most frequently), cut, and ligated during dissection. If intraoperatively, a suspicion of ureteral duplication arises, surgeons should observe the peristaltic activity of both ureters to differentiate this variation. (B) Ureteral diverticulum is a rare urological congenital anomaly, classiﬁed into three subgroups: (1) abortive ureteral duplications, sharing the same embryogenesis as diverticula of the disordered ureteral budding; (2) true (congenital) diverticulum, characterized by the presence of all tissue layers of the normal ureter; and (3) false (required) diverticulum, which represents a mucosal herniation [27,28]. Ureteral diverticula are mainly asymp- tomatic, although urinary tract infection and ureteral stones causing obstruction could Diagnostics 2021, 11, 89 7 of 27

appear. Papin and Eisendrath proposed and illustrated urethral diverticulum classification, which can be used clinically for PLNDGO (Figure6)[29]. Surgical considerations. Ureteral diverticulum may also be confused with vascular structures. Ampullary diverticulum could mimic retroperitoneal cysts. In cases of retroperitoneal tumors in the pelvic region during PLNDGO, the ureter must be identified. (C) Retro-iliac ureter (RIU) is a rare urological condition in which the ureter passes deep to the iliac vessels. Generally, the condition is diagnosed intraoperatively. Despite being a congenital anomaly, for the majority of patients the RIU first manifests itself as flank pain and symptoms of ureteral obstruction in their second or third decade of life. Coexisting anomalies are common: vaginal atresia, lumbosacral agenesis, or malrotation of the kidney. Surgical treatment consists of a dissection of the ureter and its anterior repositioning with a subsequent reimplantation in the bladder wall. RIU is thought to originate as a result of embryologic defects: a defect in the mesonephric ureteral migration during arterial development, persistence of the embryologic primitive ventral root of the umbilical artery, between the aorta and distal umbilical artery, traps the ureter dorsally. The third hypothesis involves abnormal development of the iliac vessels from the anterior branch of the umbilical artery instead of the dorsal [30–32]. RIU is commonly located behind the common iliac artery, but other previously reported types have been described as a retro-common iliac vein, retro-external iliac artery/vein, and retro- internal iliac artery [30–32]. A bilateral RIU is a rare but possible variation (Figure6)[30]. Surgical considerations. Although a rare anatomic variation, the RIU is of high importance. First, it is hard to be identified if the surgeon is not familiar with such a variation of the ureter. Second, it could be injured during an iliac lymph nodes dissection, especially if it is mistaken for a vascular structure. Finally, the RIU could not be the dorsomedial border of the PLND, as it has different location. In such cases, the lateral aspect of the rectum is considered as the dorsomedial border. Anatomical variations of the ureter—conclusion of surgical considerations. Ureteral injuries (UIs) occur approximately in 0.5–1% of all pelvic operations with gynecological operations accounting for 75% of these. UIs are more common during radical hysterectomy procedures combine with PLND. The incidence of UIs during PLND is 10%. It is believed that ureteral variations lead to an increased risk of UIs. There is consensus that a multiplication of the ureter is an independent risk factor for UIs during PLND. Benedetti-Panici et al. reported a prospective study, which included 309 consecutive patients with cervical, endometrial, and ovarian cancer treated with systematic aortic and PLND. Ureteral duplication was observed in four (1.6%) cases. Authors concluded that knowledge of ureteral anomalies is important in gynecological surgery, as the risk of UIs is elevated. Duplicated UIs during gynecological procedures are reported in medical literature. UIs may occur at the level of the infundibulopelvic ligament and deep in the pelvis, below the level of ischial spine, where the ureter lies lateral to the peritoneum of uterosacral ligament. Anatomical variations of the ureter are often associated with other congenital anomalies. Patients with known congenital anomalies or different types of syndromes should undergo preoperative imaging for careful surgical planning [33–39]. Postoperatively, a routine cystoscopy should be performed to rule out UIs [26]. Diagnostics 2021, 11, 89 8 of 27 Diagnostics 2021, 11, x FOR PEER REVIEW 8 of 27

FigureFigure 6. Anatomical 6. Anatomical variations variations of of the the ureter ureter related related toto pelvicpelvic lymph node node dissection dissection in in gynecologic gynecologic oncology oncology (PLNDGO). (PLNDGO). (A) Duplicated ureter. (A1) complete duplication. (A2) incomplete duplication. (B) Ureteral diverticulum (Adapted from (A) Duplicated ureter. (A1) complete duplication. (A2) incomplete duplication. (B) Ureteral diverticulum (Adapted from Papin and Eisendrath [29]). (B1) simple diverticulum, (B2) ampullary diverticulum, (B3) diverticulum ending in fibrous Papinprolongation, and Eisendrath (B4) multiple [29]). (B1 diverticulus) simple diverticulum,. (C) Retroiliac ( B2ureter.) ampullary (C1) Behind diverticulum, the common (B3 iliac) diverticulum artery, (C2) behind ending the in com- ﬁbrous prolongation,mon iliac vein, (B4) ( multipleC3) behind diverticulus. the external ( Ciliac) Retroiliac artery, (C4 ureter.) behind (C1 the) Behind external the iliac common vein, ( iliacC5) behind artery, the (C2 internal) behind iliac the artery. common iliac vein, (C3) behind the external iliac artery, (C4) behind the external iliac vein, (C5) behind the internal iliac artery. 7. Iliac Vessel Variations 7.7.1. Iliac Iliac Vessel Arteries Variations 7.1. IliacAs Arteries PLND is mainly a vascular dissection procedure, the anatomical variations of iliac vessels should be respected in order to avoid unnecessary hemorrhage or transfusion [40]. As PLND is mainly a vascular dissection procedure, the anatomical variations of iliac vessels7.2. Common should Iliac be respectedArtery (CIA) in orderAnatomy to avoid unnecessary hemorrhage or transfusion [40]. 7.2. CommonThe abdominal Iliac Artery aorta (CIA) bifurcates Anatomy anterolaterally to the left side of the fourth lumbar vertebral body and divides into the left and right common iliac arteries. They further di- The abdominal aorta bifurcates anterolaterally to the left side of the fourth lumbar vide into the external and internal iliac arteries at the level of the sacroiliac joint. The right vertebral body and divides into the left and right common iliac arteries. They further CIA (5 cm) is frequently longer than its left counterpart (4 cm) [41]. divide into the external and internal iliac arteries at the level of the sacroiliac joint. The right7.3. CIA Variations (5 cm) is frequentlyRelated to PLNDGO longer than its left counterpart (4 cm) [41]. 7.3. CIACIA Variations variations Related are relatively to PLNDGO rare. Although the true incidence of CIA variations is not known, the most frequent anomaly is an absence of the CIA. It tends to be unilateral, CIA variations are relatively rare. Although the true incidence of CIA variations predominantly to the right, even though bilateral agenesis of CIA has also been described is not known, the most frequent anomaly is an absence of the CIA. It tends to be uni- [42–44]. In one of the cases, described by Shetty et al., the abdominal aorta was directly lateral, predominantly to the right, even though bilateral agenesis of CIA has also been branching into external and internal iliac arteries at the level of the 4th–5th lumbar verte- describedbra [43]. Dabydeen [42–44]. In et one al. ofdescribed the cases, a case described of congenital by Shetty absence et al., of the the abdominal right CIA. aortaIn their was directlyarticle, branchingthe proximal into part external of the andright internal external iliac iliac arteries artery atwas the absent. level ofThe the distal 4th–5th part lumbar and vertebra [43]. Dabydeen et al. described a case of congenital absence of the right CIA. In their article, the proximal part of the right external iliac artery was absent. The distal part and the right common femoral artery was reconstituted from the right inferior epigas-

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the right common femoral artery was reconstituted from the right inferior epigastric artery, deep circumflex iliac artery, and the contralateral common femoral artery [44]. Llauger et al. presented a case of atresia of the right CIA, associated with a large aberrant and anomalous artery, connecting both hypogastric arteries within the pelvis [45]. Rusu et al. observed the anomalous origin of the iliolumbar artery, which has not Diagnostics 2021, 11, 89 9 of 27 been reported before. The authors dissected 15 human adult cadavers (30 pelvic halves). The CIA appeared trifurcated due to a higher origin of the iliolumbar artery (originating from the CIA bifurcation) in 2.5% of cadavers [46]. In 8.75% of specimens, the iliolumbar tricartery artery, originated deep circumﬂex from the iliac CIA artery, [46]. and the contralateral common femoral artery [44]. Llauger et al. presented a case of atresia of the right CIA, associated with a large aberrant Surgical considerations. In cases of absent CIA, surgeons should be aware of collat- and anomalous artery, connecting both hypogastric arteries within the pelvis [45]. eral,Rusu anomalous, et al. observed or aberrant the anomalous arteries. origin Collateral of the iliolumbar arteries artery, serve which as an has alternative not been blood reportedsource, before.compensating The authors the absent dissected CIA; 15 humanthey migh adultt be cadavers of atypical (30 pelvic origin halves). from Thethe iliac sys- CIAtem. appeared Iliolumbar trifurcated arteries, due originating to a higher originfrom the of the CIA iliolumbar or CIA arterybifurcation, (originating may from be damaged theduring CIA bifurcation)a middle common in 2.5% of iliac cadavers lymph [46 nodes]. In 8.75% dissection of specimens, of the thelumbosacral iliolumbar fossa. artery originated from the CIA [46]. 8. External/InternalSurgical considerations. Iliac InArtery cases Anatomy of absent CIA, surgeons should be aware of collateral, anomalous, or aberrant arteries. Collateral arteries serve as an alternative blood source, The external iliac artery (EIA) is a direct continuation of the CIA. It runs downwards, compensating the absent CIA; they might be of atypical origin from the iliac system. Iliolumbarforwards arteries,in the iliac originating fossa, and from reaches the CIA the or CIA lacuna bifurcation, vasorum may under be damaged the inguinal during ligament. aThe middle EIA common has two iliacbranches: lymph inferior nodes dissection epigastric of theartery lumbosacral and deep fossa. circumflex iliac artery. After crossing the mid-inguinal point, it continues as a common femoral artery. The internal 8.iliac External/Internal artery (IIA) arises Iliac Arteryfrom the Anatomy CIA anterior to the sacroiliac joint. In the majority of the cases,The the external artery iliac originates artery (EIA) at the is alevel direct of continuation the L5–S1 intervertebral of the CIA. It runs disc. downwards, The IIA descends forwardsposteriorly in the towards iliac fossa, the andsuperior reaches border the lacuna of the vasorum greater under sciatic the foramen inguinal ligament.where it divides Theinto EIA two has branches: two branches: anterior inferior and epigastric posterior artery [42,47,48]. and deep The circumﬂex anterior iliac and artery. posterior After branches crossing the mid-inguinal point, it continues as a common femoral artery. The internal of the IIA are illustrated in Figure 7. iliac artery (IIA) arises from the CIA anterior to the sacroiliac joint. In the majority of the cases, the artery originates at the level of the L5–S1 intervertebral disc. The IIA descends posteriorly towards the superior border of the greater sciatic foramen where it divides into two branches: anterior and posterior [42,47,48]. The anterior and posterior branches of the IIA are illustrated in Figure7.

Figure 7. The internal iliac artery (IIA) branches. OA—obturator artery, UA—obliterated umbilical artery, SVA—superior vesical artery, UA—uterine artery, VA—vaginal artery, MRA—middle rectal artery, IPA—internal pudendal artery, IGA—inferior gluteal artery, LSA—lateral sacral artery, SGA— superior gluteal artery, ILA—iliolumbar artery. 9.Figure EIA Variations 7. The internal Related iliac to artery PLNDGO (IIA) branches. OA—obturator artery, UA—obliterated umbilical artery,Variations SVA—superior of the EIA vesical are grouped artery, UA—uterine into four categories artery, VA—vagin [48,49]: al artery, MRA—middle rectal artery, IPA—internal pudendal artery, IGA—inferior gluteal artery, LSA—lateral sacral artery, (A) Hypoplasia, agenesis of the EIA; SGA—superior gluteal artery, ILA—iliolumbar artery. (B) Anomalous origin and position of the EIA; (C) Morphological variations (variations in the shape of the EIA); (D) Variations in the branching pattern of the EIA.

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(A) Kawashima et al. reported a rare case of hypoplastic right EIA, which continued into the normal femoral artery by anastomoses formed with the enlarged obturator and deep circumflex iliac arteries [50]. Okamoto et al. reported a case of the CIA entering into the pelvic cavity without branching to the EIA. The artery passed behind the first sacral nerve and gave rise to each branch of the IIA in the pelvis [51]. In cases of EIA hypoplasia, an ipsilateral persistent sciatic artery may also be observed [49]. Surgical considerations. Cases of EIA hypoplasia and agenesis are of clinical significance due to the possible presence of a collateral pathway. PLND should be meticulous in order to preserve collateral and anomalous vessels. (B) The EIA may directly originate from the abdominal aorta. The origin of the EIA could be posterior in the internal iliac fossa. The position of the EIA may differ to the external iliac vein (EIV) position. The EIA might be located superficially or medially to the EIV [48,49]. Surgical considerations. During an external iliac lymph nodes dissection, surgeons should be familiar with the EIA position differences to prevent iliac vessel injury. Safi et al. reported a case of EIA laparoscopic injury due to an anomalous position of the artery. The EIA was elongated and located posterior and medial to the EIV. They repaired the artery using a two-needle single-knot technique and continued the lymphadenectomy. Authors concluded that during PLND, both external iliac vessels should be exposed and visible to the surgeon, as the anatomical variations of the EIA increased the risk of injury [52]. (C) Morphological variations of the EIA are grossly classified in five groups: looped, tortuous, curved, twisted, and S-shaped EIA. Nayak et al. presented a cadaveric study of 48 hemipelvises. They observed morphological variations in nine (19%) of the hemipelvises [48].

Diagnostics 2021, 11, x FOR PEER REVIEWLooped and tortuous EIA have been reported in other case studies [53,54]. We11 also of 27 observed morphological variations of EIA (Figure8).

Figure 8. Morphological variations of the external iliac artery (EIA). (A) The EIA with an inward Figure 8. Morphological variations of the external iliac artery (EIA). (A) The EIA with an inward loop loop in the left hemipelvis. (B) The EIA with a gentle inward loop in the left hemipelvis. (C) ’S’ inshaped the left EIA hemipelvis. in the right hemipelvis. (B) The EIA EIA—external with a gentle iliac inward artery, loopEIV—external in the left iliac hemipelvis. vein, IIA—inter- (C) ’S’ shaped EIAnal iliac in the artery, right PMM—psoas hemipelvis. major EIA—external muscle. iliac artery, EIV—external iliac vein, IIA—internal iliac artery, PMM—psoas major muscle.

Surgical considerations. Knowledge of the EIA morphological variations is essential during an external iliac lymph nodes dissection. Particular attention should be paid during dissection of the lateral, middle, and medial external iliac lymph nodes. The risk of iatrogenic EIA lesions may increase as a result of existing morphological differences.

Figure 9. An aberrant obturator artery arising as a common trunk with the inferior epigastric artery (open surgery). EIA—external iliac artery, EIV—external iliac vein, AOA- aberrant obturator artery, ACOV- accessory obturator vein, ON—obturator nerve, OV- obturator vein, IEA—inferior epigastric artery, UMA—umbilical artery, FR—the deep femoral ring, OF—obturator foramen. Ca—caudal, Cr –cranial, R—right, L—left.

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(D) Variability in the origin of the obturator artery (OA) from the EIA has also been reported in medical literature [55,56]. If the OA originates from the external iliac system, it crosses the superior pubic ramus and the external iliac vein vertically [55]. The OA can also arise as a common trunk with the inferior epigastric artery and the deep circumﬂex

iliac artery (Figure9)[ 55,56]. Nayak et al. reported duplication of the deep circumﬂex iliac arteryFigure and 8. Morphological an additional variations large muscular of the external branch, iliac arising artery and (EIA). descending (A) The EIA laterally with froman inward the EIAloop [ 48in]. the The left medial hemipelvis. circumﬂex (B) The femoral EIA with artery a gentle and theinward profunda loop in femoral the left arteryhemipelvis. could (C) also ’S’ shaped EIA in the right hemipelvis. EIA—external iliac artery, EIV—external iliac vein, IIA—inter- arise from the EIA [42]. nal iliac artery, PMM—psoas major muscle.

FigureFigure 9.9. AnAn aberrant aberrant obturator obturator artery artery arising arising as asa co ammon common trunk trunk with with the inferior the inferior epigastric epigastric artery (open surgery). EIA—external iliac artery, EIV—external iliac vein, AOA- aberrant obturator artery, artery (open surgery). EIA—external iliac artery, EIV—external iliac vein, AOA—aberrant obturator ACOV- accessory obturator vein, ON—obturator nerve, OV- obturator vein, IEA—inferior epigas- artery, ACOV—accessory obturator vein, ON—obturator nerve, OV—obturator vein, IEA—inferior tric artery, UMA—umbilical artery, FR—the deep femoral ring, OF—obturator foramen. Ca—cau- epigastricdal, Cr –cranial, artery, UMA—umbilicalR—right, L—left. artery, FR—the deep femoral ring, OF—obturator foramen. Ca— caudal, Cr—cranial, R—right, L—left.

Surgical considerations. An OA, arising from the EIA, is not a rare variation. The majority of OA origin variations are located at the distal part of the EIA. 10. IIA Variations, Related to PLNDGO Most of the IIA variations are related to its branching pattern. Different authors have suggested various concepts for classification of the ending branches of the IIA. Most researchers and clinicians refer to the Adachi classification, which has been the standard for many years. Adachi classified the branching of the IIA using its four large parietal branches: the umbilical, superior gluteal, inferior gluteal, and the internal pudendal arteries (Figure 10)[42,57–59]. Diagnostics 2021, 11, x FOR PEER REVIEW 12 of 27

10. IIA Variations, Related to PLNDGO Most of the IIA variations are related to its branching pattern. Different authors have suggested various concepts for classification of the ending branches of the IIA. Most researchers and clinicians refer to the Adachi classification, which has been the standard for many years. Adachi classified the branching of the IIA using its four large parietal Diagnostics 2021, 11, 89 branches: the umbilical, superior gluteal, inferior gluteal, and the internal pudendal arter-12 of 27 ies (Figure 10) [42,57–59].

FigureFigure 10 10.. ClassificationClassification of of IIA IIA variations. variations. Ad Adoptedopted from from Adachi Adachi [58]. [58]. Type Type I—The I—The su superiorperior gluteal gluteal artery artery (SGA) (SGA) arises arises separatelyseparately from from internal internal iliac iliac artery, artery, while while the the inferior inferior glut glutealeal (IGA) (IGA) and and internal internal pudendal pudendal vessel vessel (IPA) (IPA) share share a a common common trunk. Type Ia—the bifurcation of IGA and IPA occurs within the pelvis. Type Ib—the bifurcation occurs below the pelvis. trunk. Type Ia—the bifurcation of IGA and IPA occurs within the pelvis. Type Ib—the bifurcation occurs below the pelvis. Type II—The internal pudendal artery arises separately from the IIA, while the superior gluteal artery shares a trunk with theType inferior II—The gluteal internal artery. pudendal Type IIa—the artery arises bifurcation separately of SGA from and the IGA IIA, whileoccurs the within superior the pelvis. gluteal Type artery IIb—the shares abifurcation trunk with occursthe inferior below gluteal the pelvis. artery. Type Type III—SGA, IIa—the bifurcationIGA, and IPA of SGA arise and separately IGA occurs from within the internal the pelvis. iliac Type artery, IIb—the and the bifurcation internal pudendaloccurs below artery the is pelvis.the last Typebranch. III—SGA, Type IV—SGA, IGA, and IGA, IPA and arise IPA separately share a common from the trunk. internal Type iliac IVA—the artery, andSGA the is the internal first vesselpudendal from artery the common is the last trunk, branch. before Type bifurcating IV—SGA, into IGA, the and other IPA two share branches—SGA a common trunk. and IG TypeA. Type IVA—the IVB—the SGA IPA is the is firstthe firstvessel from from the the common common trunk, trunk, which before then bifurcating divides into into SGA the an otherd IGA. two Type branches—SGA V—The IGA andhas a IGA. separate Type origin IVB—the from IPA the is IIA, the whilefirst from the SGA the commonand IGA trunk,share a which common then trunk. divides into SGA and IGA. Type V—The IGA has a separate origin from the IIA, while the SGA and IGA share a common trunk. Surgical consideration. As shown in Figure 10, the SGA is a variable artery. Surgeons shouldSurgical be aware consideration. of the SGA variations As shown to in safely Figure perform 10, the gluteal SGA islymph a variable node artery.group dis- Sur- section.geons should be aware of the SGA variations to safely perform gluteal lymph node group dissection. 11. Uterine and Obturator Artery Variations Related to PLNDGO 11. Uterine and Obturator Artery Variations Related to PLNDGO Uterine artery. In the majority of cases, the uterine artery (UA) arises from the anterior branchUterine of artery.the IIA. In Different the majority origins of cases, of the the UA uterine have arterybeen reported: (UA) arises from from the the umbilical anterior arterybranch as of a theseparate IIA. Different branch and origins via ofa common the UA have trunk been (Figure reported: 11); from from the the inferior umbilical gluteal artery as a separate branch and via a common trunk (Figure 11); from the inferior gluteal artery as a separate branch; as a bifurcation from the inferior gluteal; and as a trifurcation with the superior and the inferior gluteal arteries [60].

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artery as a separate branch; as a bifurcation from the inferior gluteal; and as a trifurcation with the superior and the inferior gluteal arteries [60]. Diagnostics 2021, 11, 89 Surgical considerations. The risk of iatrogenic injury to the UA is increased when13 of the 27 artery arises from the umbilical artery, as the UA crosses the operative field. If the PLND is performed before hysterectomy, surgeons should first identify the UA origin.

Figure 11. Uterine artery and umbilical artery, arising in a common trunk. VA arising from the uter- Figure 11. Uterine artery and umbilical artery, arising in a common trunk. VA arising from the ine artery. OA—obturator artery, OV—obturator vein, ON—obturator nerve, UMA—obliterated uterine artery. OA—obturator artery, OV—obturator vein, ON—obturator nerve, UMA—obliterated umbilical artery, IIA—internal iliac artery, IGA—inferior gluteal artery, UR—ureter, VA—vaginal umbilicalartery. artery, IIA—internal iliac artery, IGA—inferior gluteal artery, UR—ureter, VA—vaginal artery. Obturator artery. The OA, branching from the EIA, has been discussed above. Surgical considerations. The risk of iatrogenic injury to the UA is increased when the Herein, most of the OA anomalies will be analyzed. artery arises from the umbilical artery, as the UA crosses the operative field. If the PLND is In most cases, the OA originates from the anterior trunk of the IIA [55]. The OA runs performed before hysterectomy, surgeons should first identify the UA origin. anteroinferiorly and lies longitudinally to the obturator foramen on the medial part of the Obturator artery. The OA, branching from the EIA, has been discussed above. Herein, obturator internal muscle. It gives several branches within the pelvis, before entering the most of the OA anomalies will be analyzed. obturatorIn most foramen. cases, the They OA are originates classified from as ilia thec, anterior vesical, trunk and pubic of the branches. IIA [55]. TheThe OAOA runsis lo- anteroinferiorlycated medially to and the lies ureter, longitudinally cranially to tothe the obturator obturator vein, foramen and caudally on the medialto the obturator part of thenerve obturator [55,61]. internal The OA muscle. has the It greatest gives several variation branches frequency within among the pelvis, the IIA before branches entering [62]. theFurthermore, obturator foramen.the OA may They arise are from classified the EIA, as the iliac, femoral vesical, artery, and the pubic deep branches. circumflex The iliac OAartery, is located the posterior medially branch to the of ureter, IIA, or cranially from the to theinferior obturator epigastric vein, artery and caudally (Figure to12) the[42,55,63]. obturator In nerve20% to [55 34%,61]. of The the OA cases, has the the pu greatestbic branch variation of the frequency inferior epigastric among the artery IIA branchesreplaces [the62]. OA. Furthermore, In such cases, the OA the may OA arise passes from posterior the EIA, to the the femoral lacunar artery, ligament the deep and circumflexcourses into iliac the artery, superior the pubic posterior ramus branch vertically of IIA, to or enter from the the obturator inferior epigastricforamen [55]. artery An (FigureOA arising 12)[ 42from,55, 63the]. EIA In 20% or its to 34%branches of the is cases, classified the pubic as an branch aberrant of theobturator inferior artery. epigastric Two arteryobturator replaces arteries the OA.could In be such observed cases, theduring OA dissection. passes posterior An additional to the lacunar OA with ligament a different and coursesorigin or into path the through superior the pubic obturator ramus fossa vertically is classified to enter as thean accessory obturator obturator foramen [artery.55]. An OA arisingSurgical from consideration. the EIA or its Surgeons branches should is classified be aware as an of aberrant the possible obturator presence artery. of acces- Two obturatorsory or aberrant arteries obturator could be observed arteries during during external dissection. and An internal additional iliac OAlymph with node a different groups origindissection. or path The through presence the of obturator normal OA fossa does is classifiednot exclude as anthe accessory existence obturatorof an accessory artery. OA. The inferior epigastric artery is located below the deep circumflex iliac vein. Any injury

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of the OA arising from the inferior epigastric artery should be avoided, as the deep circumflex iliac vein is the ventral border of the dissection. Anatomical variations of iliac arteries—conclusion of surgical considerations. Arterial injuries during PLNDGO are less common than venous ones. There are very few studies describing arterial damage during PLNDGO. Bae et al. presented a retrospec- tive review study. Authors observed four (1.3%) cases of major vascular injuries during 225 laparoscopic lymph node dissections. One of the injuries was to the EIA. Ricciardi et al. and Ishikawa et al. also reported damage to the EIA in a course of PLND. These studies showed that the EIA is more likely to be injured during PLND than the other iliac arteries. Gyimadu et al. concluded that the occurrence of vascular injuries during the course of PLNDGO may be due to variations in the anatomy of great retroperitoneal vessels. In Diagnostics 2021, 11, 89 medical literature the frequency of such abnormalities varies between14 of 27 5.6 and 23.0% [64– 68].

FigureFigure 12. 12.Obturator Obturator artery artery arising fromarising the posteriorfrom the branch posterior of the IIA.branch U—uterus, of the EIA—external IIA. U—uterus, EIA—external iliaciliac artery, artery, EIV—external EIV—external iliac vein, iliac IIA—internal vein, IIA—internal iliac artery, SGA—superior iliac artery, glutealSGA—superior artery, LSA— gluteal artery, LSA— laterallateral sacral sacral artery, artery, IPA—internal IPA—internal pudendal pudendal artery, OA—obturator artery, OA—obturator artery, ON—obturator artery, nerve, ON—obturator nerve, SUA—severedSUA—severed uterine uterine artery. artery. Surgical consideration. Surgeons should be aware of the possible presence of acces- sory12. orIliac aberrant Veins obturator arteries during external and internal iliac lymph node groups dissection.12.1. Common The presence Iliac Vein of normal Anatomy OA does (CIV) not exclude the existence of an accessory OA. The inferior epigastric artery is located below the deep circumflex iliac vein. Any injury of the OACommon arising from iliac the inferior veins epigastric (CIVs) arterydrain should into the be avoided, inferior as thevena deep cava. circumflex They are a direct con- iliactinuation vein is the of ventral the external border of iliac the dissection. veins and are formed by the junction of the external and Anatomical variations of iliac arteries—conclusion of surgical considerations. internalArterial iliac injuries venous during system, PLNDGO anterior are less to common the sacroiliac than venous joints. ones. The There left are CIV is longer than verythe right few studies one. The describing left CIV arterial is located damage first during medi PLNDGO.ally, then Bae posteriorly et al. presented to the a left EIA, whereas retrospectivethe right CIV review is posterior study. Authors and observed then lateral four (1.3%) to the cases right of major EIA. vascular The iliolumbar, injuries the ascending duringlumbar 225 vein, laparoscopic and the lymph lateral node sacral dissections. vein drain One into of the the injuries CIV. In was most to the cases, EIA. the median sacral Ricciardi et al. and Ishikawa et al. also reported damage to the EIA in a course of PLND. Thesevein studiesdrains showed into the that left the EIACIV is [41,42,47]. more likely to be injured during PLND than the other iliac arteries. Gyimadu et al. concluded that the occurrence of vascular injuries during the12.2. course CIV of Variations PLNDGO may Related be due to tothe variations PLNDGO in the anatomy of great retroperitoneal vessels. In medical literature the frequency of such abnormalities varies between 5.6 and 23.0% [Surgical64–68]. considerations. All types of CIV variations are related to possible venous injuries (Figure 13) [35,69–74]. Iatrogenic damage could occur during dissection of all five 12.types Iliac of Veins common iliac lymph node groups. Kose et al. reported a study of 229 patients 12.1. Common Iliac Vein Anatomy (CIV) who underwent paraaortic and PLND. Authors observed major retroperitoneal vessel Common iliac veins (CIVs) drain into the inferior vena cava. They are a direct contin- uationvariations of the external in thirty iliac nine veins (17%) and are patients. formed by Great the junction vessel of the injury external was and present internal in nineteen (8.3%) iliacpatients. venous CIV system, variations anterior to were the sacroiliac found joints. in two The leftpatients. CIV is longerOne thanof the the patients right had a venous one. The left CIV is located first medially, then posteriorly to the left EIA, whereas the right CIV is posterior and then lateral to the right EIA. The iliolumbar, the ascending lumbar vein, and the lateral sacral vein drain into the CIV. In most cases, the median sacral vein drains into the left CIV [41,42,47].

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12.2. CIV Variations Related to the PLNDGO Surgical considerations. All types of CIV variations are related to possible venous injuries (Figure 13)[35,69–74]. Iatrogenic damage could occur during dissection of all ﬁve types of common iliac lymph node groups. Kose et al. reported a study of 229 patients who Diagnostics 2021, 11, x FOR PEER REVIEW 15 of 27 underwent paraaortic and PLND. Authors observed major retroperitoneal vessel variations in thirty nine (17%) patients. Great vessel injury was present in nineteen (8.3%) patients. CIV variations were found in two patients. One of the patients had a venous annulus ofannulus the right of the CIV, right surrounding CIV, surrounding the right the CIA. right The CIA. other The patient other had patient a duplicated had a duplicated left CIV (B2left fromCIV (B2 the CIVfrom classiﬁcation), the CIV classification), which was which injured was during injured dissection. during dissection. Authors concluded Authors thatconcluded each patient’s that each vascular patient’s anatomy vascular must anat beomy assessed must individually be assessed to individually avoid injuries to during avoid scheduledinjuries during operations scheduled [75]. operations [75].

Figure 13. Common iliac vein variations. (A) Incomplete duplication of the CIV; (B) complete duplication of the CIV; Figure 13. Common iliac vein variations. (А) Incomplete duplication of the CIV; (B) complete duplication of the CIV; (C) (C) lateral duplicated branch drains into the IVC, the medial drain into the CIV. (D) Absent CIV, external and internal lateral duplicated branch drains into the IVC, the medial drain into the CIV. (D) Absent CIV, external and internal iliac iliac veins drain to the contralateral CIV; (E) absent CIV, the EIV drains into the IVC, the IIV drains into the contralateral veins drain to the contralateral CIV; (E) absent CIV, the EIV drains into the IVC, the IIV drains into the contralateral CIV; CIV;(F) Absent (F) Absent CIV, the CIV, external the external and internal and internal veins drain veins into drain IVC. into Inferior IVC. Inferior vena cava vena (IVC), cava Common (IVC), Common iliac vein iliac (CIV), vein external (CIV), externaliliac vein iliac (EIV), vein internal (EIV), internal iliac vein iliac vein(IIV). (IIV). (A1, (B1A1,C1,B1,D1,C1,,E1D1,F1,E1) ,F1are) arerelated related to toright right hemipelvises hemipelvises variations, variations, whereaswhereas ((A2A2,,B2B2,,C2C2,,D2D2,,E2E2,,F2F2)) areare relatedrelated toto leftleft hemipelviseshemipelvises variations. variations.

12.3. CIV Tributaries Variations Related to PLNDGO 12.3. CIV Tributaries Variations Related to PLNDGO Iliolumbar vein (ILV) and ascending lumbar vein (ALV) anatomy. The ILV drains the Iliolumbar vein (ILV) and ascending lumbar vein (ALV) anatomy. The ILV drains venous blood from the iliac fossa, the iliac, and psoas muscles and terminates in the CIV. the venous blood from the iliac fossa, the iliac, and psoas muscles and terminates in the It is considered the segmental equivalent of the fifth lumbar vertebra [76–81]. The ALV CIV. It is considered the segmental equivalent of the ﬁfth lumbar vertebra [76–81]. The participates in an anastomotic venous system between the inferior vena cava and the su- ALV participates in an anastomotic venous system between the inferior vena cava and perior vena cava. The lower end of the ALV enters the cephalic border of the CIV. Up- the superior vena cava. The lower end of the ALV enters the cephalic border of the CIV. wards, the ALV receives the lumbar veins and terminates by joining the subcostal vein to Upwards, the ALV receives the lumbar veins and terminates by joining the subcostal vein toform form the the azygos azygos vein vein on on the the right right and and the the hemiazygos hemiazygos on on the the left. left. ILV ILV anastomoses withwith ALV,ALV, deepdeep circumﬂexcircumflex iliac iliac vein vein and and lateral lateral sacral sacral vein vein [ 76[76–81].–81]. ILV and ALV variations related to PLNDGO. Particular attention should be given to the ILV and AVL as high percentage of drainage variations is documented. Furthermore, our literature survey revealed that the clinical significance of these veins is rarely mentioned in gynecologic oncology practice. In PLNDGO, we observed a high percentage of drainage variations of the ILV and ALV. In medical literature, there is a controversy as to the anatomy and the nomenclature of the ILV and ALV. Terms such as “lateral lumbosacral veins”, “inferior lumbar”, and “superior iliac” veins have been used to define ILV and ALV [76–81]. Moreover, different drainage patterns of ILV and ALV have been reported for both veins—ILV/ALV draining separately into CIV; ILV/ALV draining into the CIV as

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ILV and ALV variations related to PLNDGO. Particular attention should be given to the ILV and AVL as high percentage of drainage variations is documented. Furthermore, our literature survey revealed that the clinical significance of these veins is rarely mentioned in gynecologic oncology practice. In PLNDGO, we observed a high percentage of drainage variations of the ILV and ALV. In medical literature, there is a controversy as to the anatomy Diagnostics 2021, 11, x FOR PEER REVIEW 16 of 27 and the nomenclature of the ILV and ALV. Terms such as “lateral lumbosacral veins”, “inferior lumbar”, and “superior iliac” veins have been used to define ILV and ALV [76–81]. Moreover, different drainage patterns of ILV and ALV have been reported for both veins— ILV/ALVa common draining trunk, ILV separately draining intointo CIV;the external ILV/ALV/internal draining iliac into venous the CIVsystem. as a Lolis common et al. trunk,reported ILV a drainingdetailed description into the external/internal of the surgical iliacanatomy venous and system. draining Lolis patterns et al. reportedof the ILV, a detailedbased on description a significantly of thegreat surgical number anatomy of specimens and draining [77]. They patterns proposed of the and ILV, illustrated based on a adetail significantly classification great separated number ofinto specimens two types. [77 In]. Type They I proposed (54%), ILV and drainage illustrated patterns a detail dif- classificationfered, whereas separated the ALV intohad twothe same types. pattern In Type on Iboth (54%), sides. ILV In drainage Type II, patternsthe ALVdiffered, differed whereasin pattern the from ALV one had side the to same the patternother (46%). on both Authors sides. observed In Type II, high the ALVpercentage differed of in drainage pattern fromvariations one side in ILV to the 91% other compare (46%). to Authors ALV 34% observed [77]. Numerously high percentage drainage of drainage variations variations of ILV inand ILV ALV 91% have compare been reported, to ALV 34% but [ 77in ].Figure Numerously 14 are illustrated drainage variationsthe most important of ILV and during ALV havePLNDGO. been reported,The ILV and but ALV in Figure drainage 14 are variations illustrated during the most PLND important in our practice during PLNDGO.are shown Thein Figure ILV and 15. ALV drainage variations during PLND in our practice are shown in Figure 15.

FigureFigure 14.14. ILVILV andand ALVALV anatomyanatomy andand variations.variations. (A) ILV andand ALVALV anatomy.anatomy. HV—hemiazygosHV—hemiazygos vein, LV—lumbar veins,veins, ALV—ascendingALV—ascending lumbar lumbar vein, vein, ILV—iliolumbar ILV—iliolumbar vein, vein, IVC—inferior IVC—inferior vena vena cava, cava, LRV—left LRV—left renal renal vein, vein, RRV—right RRV—right renal renal vein, AV—azygosvein, AV—azygos vein. (vein.B) ILV (B variations.) ILV variations. 1—drains 1—drains into EIV, into 2—drainsEIV, 2—drains into theinto confluence the confluence of the of CIV, the CIV, 3—drains 3—drains into into the IIV,the IIV, 4—two ILVs drains into the CIV. (C) ALV variations. 1—drains into the EIV, 2—drains into the confluence of the CIV, 4—two ILVs drains into the CIV. (C) ALV variations. 1—drains into the EIV, 2—drains into the confluence of the CIV, 3—drains into the IIV. (D) Common trunks between ALV and ILV. 1—drains into the EIV, 2—drains into the confluence 3—drains into the IIV. (D) Common trunks between ALV and ILV. 1—drains into the EIV, 2—drains into the confluence of of CIV, 3—drains into the IIV, 4—drains into the CIV. CIV, 3—drains into the IIV, 4—drains into the CIV.

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Figure 15. ILV or ALV drain into the EIV (open surgery right pelvic sidewall). We can only specu- Figure 15. ILV or ALV drain into the EIV (open surgery right pelvic sidewall). We can only speculate late if these veins are ILV, ALV, or both. (A) Two separate veins drain into the EIV. The EIA is ifretracted these veins medially. are ILV, (B) Two ALV, veins or both. drain ( Ainto) Two the EIV separate via common veins draintrunk. into the EIV. The EIA is retracted medially. (B) Two veins drain into the EIV via common trunk. Surgical considerations. Knowledge of the surgical anatomy of ILV and ALV may preventSurgical venous considerations. damage such as tears Knowledge and avulsion of the of surgicalthese veins anatomy during PLND. of ILV Injury and ALVof may preventILV and venousALV could damage occur suchin the ascourse tears of and exte avulsionrnal and internal of these iliac veins lymph during nodes PLND. dissec- Injury of ILVtion. and Special ALV attention could occur should in thebe paid course during of external middle and common internal iliac iliac (located lymph in nodesthe lum- dissection. Specialbosacral attention fossa) and should lateral beexternal paid duringiliac lymph middle nodes common dissection. iliac Panici (located et al. in stated the lumbosacralthat fossa)during and lateral lateral common external iliac iliaclymph lymph nodes nodes dissection, dissection. the presence Panici of et iliolumbal al. stated veins that during lateralcould be common hazardous iliac as lymphseveral nodesiliolumbar dissection, veins could the drain presence into ofthe iliolumbal CIV. Authors veins con- could be hazardouscluded that as the several CIV should iliolumbar be handled veins couldvery gently, drain intoand thedissection CIV. Authors must be concluded blunt and that the delicate [17]. CIV should be handled very gently, and dissection must be blunt and delicate [17]. 13. Median Sacral Vein (MSV) and Lateral Sacral Veins (LSVs) Anatomy and Varia- 13. Median Sacral Vein (MSV) and Lateral Sacral Veins (LSVs) Anatomy and Variationstions Related Related to PLNDGO to PLNDGO The median sacral vein (MSV) runs anterior and in the midline of the sacrum and the The median sacral vein (MSV) runs anterior and in the midline of the sacrum and the coccyx. It commonly drains into the left CIV. The lateral sacral veins lie on the periosteum coccyx.of the sacrum It commonly and typically drains connect into the the left epidural CIV. Theplexus lateral with sacralthe internal veins iliac lie on veins. the The periosteum ofMSV the might sacrum drain and into typically the left internal connect iliac the vein epidural or the plexuscommon with iliac the junction. internal Anastomo- iliac veins. The MSVses between might drainthe lateral into and the leftmedian internal sacral iliac veins vein form or the the presacral common venous iliac junction. plexus. Cardi- Anastomoses betweennot et al. reported the lateral a case and of median both internal sacral iliac veins veins, form which the formed presacral a common venous trunk plexus. with Cardinot eta short al. reported and an average a case ofcourse, both receiving internal iliacthe middle veins, sacral which vein’s formed drainage a common and flowing trunk with a shortinto the and left an external average iliac course, vein. receivingThe lateral the sacral middle veins sacral (LSVs) vein’s might drainage drain into and the ﬂowingCIV into theand left external external iliac iliacvein [41,47,72,82]. vein. The lateral sacral veins (LSVs) might drain into the CIV and externalSurgical iliac considerations. vein [41,47,72, 82The]. MSV and the LSVs have to be preserved in cases of presacralSurgical and lateral considerations. sacral lymph The node MSV grou andp dissection. the LSVs Surgeons have to should be preserved be aware in of cases of presacraldifferent drainage and lateral patterns sacral and lymph venous node plexus group existence dissection. between Surgeonsthe two veins. should be aware of External iliac vein (EIV) anatomy. The EIV is the continuation of the femoral vein. different drainage patterns and venous plexus existence between the two veins. The inferior epigastric vein, the deep circumflex iliac vein, and the pubic branch drain into the EIV.External The vein iliac is vein located (EIV) medially anatomy. to the The ipsilateral EIV is thehomonymous continuation artery. of the femoral vein. The inferior epigastric vein, the deep circumﬂex iliac vein, and the pubic branch drain into the EIV. The vein is located medially to the ipsilateral homonymous artery.

14. EIV Variations Related to PLNDGO Anatomical variations of the EIV are less common than the CIV and internal iliac vein. The EIV might double, be absent, or be located lateral to the homonymous artery [82–84]. Diagnostics 2021, 11, x FOR PEER REVIEW 18 of 27

Diagnostics 2021, 11, 89 14. EIV Variations Related to PLNDGO 18 of 27 Anatomical variations of the EIV are less common than the CIV and internal iliac vein. The EIV might double, be absent, or be located lateral to the homonymous artery Hayashi[82–84]. etHayashi al. reported et al. reported a case of a an case additional of an additional right EIV, right which EIV, originated which originated 45 mm inferior 45 mm toinferior the iliocaval to the iliocaval junction andjunction ran ventrallyand ran ventrally to the EIA to to the surround EIA to surround it with a rightit with EIV. a right The rightEIV. CIVThe right was absentCIV was [84 absent]. Djedovic [84]. andDjedovic Putz observedand Putz observed a case of aa venouscase of a annulus venous ofannu- the leftlus externalof the left iliac external vein. The iliac medial vein. andThe the medial lateral and branch the lateral of the leftbranch EIV surroundedof the left EIV the leftsur- EIA.rounded Moreover, the left a communicationEIA. Moreover, branch,a communic betweenation the branch, lateral between and the medialthe lateral branches and the of themedial EIV, branches was identiﬁed. of the ItEIV, was was located identified below. It the was left located EIA [83 below]. the left EIA [83]. SurgicalSurgical considerations.considerations. Lateral,Lateral, additional,additional, doubledouble EIV,EIV, or or venous venous annulus annulus might might be be injuredinjured duringduring aa dissectiondissection ofof external external iliac iliac lymph lymph nodes. nodes. Lateral,Lateral, middle,middle, andand median median externalexternal iliaciliac lymphlymph nodesnodes areare atat greatgreat risk risk of of iatrogenic iatrogenic damage. damage. EIVEIV injuriesinjuries duringduring PLNDGOPLNDGO havehave beenbeen reportedreported in in medical medical literature literature [ 85[85,86].,86]. Roda Roda et et al. al. reportedreported two two cases cases ofof EIVEIV injuryinjury amongamong 327327 pelvicpelvic lymphadenectomieslymphadenectomies forfor gynecologicalgynecological malignanciesmalignancies [[86].86]. KoseKose etet al.al. reportedreported aa casecase wherewhere damagedamage toto thethe EIAEIA waswas duedue toto supernumerary supernumerary renalrenal arteryartery andand vein,vein, whichwhich distorteddistorted thethe normalnormal anatomy anatomy [ 75[75].].

15.15. EIVEIV TributariesTributaries Variations Variations Related Related to to PLNDOG PLNDOG DeepDeep circumflexcircumflex iliaciliac veinvein (DCIV)(DCIV) anatomyanatomy andand variationsvariations relatedrelated toto PLNDG.PLNDG. TheThe deepdeep circumflexcircumflex iliaciliac veinvein (DCIV)(DCIV) runsruns overover thetheEIA EIAand and above above the the inguinal inguinal ligament, ligament,it it drainsdrains inin thethe EIV.EIV. It It is is known known that that the the draining draining pattern pattern of of the the DCIV DCIV is is variable. variable. Ghassemi Ghassemi etet al.al. observedobserved thatthat thethe DCIVDCIV ranran overover (82.5%)(82.5%) andand underunder (17.5%)(17.5%) thethe EIA.EIA. TheirTheir studystudy includedincluded 216 216 hemipelvises—78 hemipelvises—78 cadavers cadavers and and 60 60 clinical clinical cases cases [ 87[87].]. SurgicalSurgical considerations.considerations. TheThe DCIVDCIV underunder thethe EIAEIA isis lessless likelylikely to to be be identified. identified. Such Such anan instanceinstance maymay leadlead toto anan expandedexpanded pelvicpelvic lymphlymph nodenode dissectiondissection (PLND).(PLND). As As mentionedmentioned above,above, thethe DCIVDCIV isis thethe ventralventral borderborder ofof PLND.PLND. TheThe DCIVDCIV underunder thethe EIAEIA isis visualized visualized betweenbetween thethe EIAEIA andand EIVEIV oror byby medialmedial traction traction of of the the EIV EIV (Figure (Figure 16 16).).

FigureFigure 16. 16.The The deep deep circumﬂex circumflex iliac iliac vein vein (DCIV) (DCIV) normal normal anatomy anatomy (A )(A and) and variation variation (B) ( (openB) (open surgery, sur- leftgery, pelvic left pelvic sidewall). sidewall). (A) The (A DCIV) The DCIV runs over runs the over EIA the and EIA drains and drains into the into EIV. the (B EIV.) The (B DCIV) The passesDCIV passes under the EIA and drains into the EIV. under the EIA and drains into the EIV.

16.Internal Iliac Vein (IIV) Anatomy IIV follows its named arterial counterpart and ascends posteromedial to the IIA. IIV drains towards the ipsilateral EIV. The IIV tributaries are the superior/inferior gluteal, obturator, internal pudendal, lateral sacral, middle rectal, superior/inferior vesical, uterine,

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16. Internal Iliac Vein (IIV) Anatomy IIV follows its named arterial counterpart and ascends posteromedial to the IIA. IIV Diagnostics 2021, 11, 89 drains towards the ipsilateral EIV. The IIV tributaries are the superior/inferior gluteal,19 of 27 obturator, internal pudendal, lateral sacral, middle rectal, superior/inferior vesical, uterine, and vaginal veins. The retroperitoneal venous system is derived from the modification of three parallel primary venous networks in the embryo between the sixth and tenth and vaginal veins. The retroperitoneal venous system is derived from the modiﬁcation of weeks of gestation—the subcardinal, the postcardinal, and the supracardinal veins three parallel primary venous networks in the embryo between the sixth and tenth weeks [41,42,88,89]. of gestation—the subcardinal, the postcardinal, and the supracardinal veins [41,42,88,89].

17.17. IIV IIV Variations Variations Related to PLNDGO TheThe multiple multiple anomalies anomalies in in the the hypogastric hypogastric venous venous drainage drainage system system represent represent poste- pos- riorterior cardinal cardinal vein vein maldevelopment, maldevelopment, as asthe the posterior posterior cardinal cardinal veins veins form form the the iliac iliac bifurca- bifur- tioncation and and iliac iliac veins veins [75]. [75 IIV]. variations IIV variations have havenot been not beenstudied studied as thoroughly as thoroughly as IIA asvaria- IIA tions.variations [79,89–92]. [79,89– Despite92]. Despite the various the various classifi classificationscations describing describing the thediverse diverse variations variations of theof the IIV, IIV, there there is isno no established established standard standard classification classification [79,89–94]. [79,89–94]. Shin Shin et et al. al. have have created created anan impressive, comprehensive,comprehensive, and and generally generally reliable reliable classification classification of iliacof iliac vessel vessel variations varia- tionsbased based on 2488 on patients2488 patients using using multidetector multidetector computed computed tomography tomography [90]. However,[90]. However, other othertypes types of IIV of variations IIV variations exist, whichexist, which have nothave been not mentionedbeen mentioned in Shin’s in Shin’s classification. classification. There- Therefore,fore, to clarify to clarify most ofmost IIV of variations, IIV variations, a modification a modification of Shin’s of classificationShin’s classification was developed was de- velopedbased on based previous on previous findings findings (Figures (Figures17 and 18 17)[ and42,73 18),79 [42,73,79,89–94].,89–94].

Figure 17 17.. IIVIIV variations. variations. ( (A1A1)) high high joining joining of of the the IIV IIV to to the the ipsilateral ipsilateral EIV. EIV. ( (B1B1)) Joining Joining of of the the IIV IIV to to the the contralateral contralateral CIV CIV.. (C1) Separated trunk of the IIV IIV drains drains into into the the ipsilateral ipsilateral CIV. CIV. ( D1) separated trunk of the IIV drains into the contralateral contralateral CIV. (E1) Duplication of the IIV. (F1) Duplication of the IIV with a venous connection between them. Variations 1 are CIV. (E1) Duplication of the IIV. (F1) Duplication of the IIV with a venous connection between them. Variations 1 are related related to right pelvic sidewall, whereas variations 2 are related to the left pelvic sidewall. to right pelvic sidewall, whereas variations 2 are related to the left pelvic sidewall.

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Figure 18. IIA variations. (G1) Communication vein between the IIV and the EIV. (H1) Separated trunk of bilateral internal iliacFigure veins 18. connecting IIA variations. with ( eachG1) Communication other before draining vein between into the the left IIV CIV. and (H2 the) The EIV. internal (H1) Separated iliac veins trunk form of a bilateral common internal trunk, thatiliac drains veins intoconnecting the inferior with venaeach other cava. before (H3) The draining internal into iliac the veins left CIV. form (H2 a common) The internal trunk, iliac which veins drains form a into common the inferior trunk, venathat cava,drains communication into the inferior vein vena between cava. (H3 the) IIVsThe internal and ipsilateral iliac veins EIV. form (H4) a Both common IIVs aretrunk, joined which by adrains connecting into the vein inferior that drainsvena cava, into thecommunication IVC. (L) Communication vein between veins. the IIVs (L1 ,andL2) Communicationipsilateral EIV. (H4 vein) Both between IIVs are the joined IIV and by ipsilateral a connecting CIV. vein (L3, L4that) communicationdrains into the veinIVC. between (L) Communication the IIV and contralateral veins. (L1,L2 CIV.) Communication (L5,L6) Both internal vein between iliac veins the are IIV joined and withipsilateral a communication CIV. (L3,L4) vein,communication which drains vein into between the inferior the venaIIV and cava. contralateral (L7,L8) Communicating CIV. (L5,L6) Both vein betweeninternal iliac both veins IIVs. Variationsare joined (withG1,L1 a ,L3communi-,L5,L7) arecation related vein, to rightwhich pelvic drains sidewall, into the whereas inferior variations vena cava. (G2, L2(L7,L4,L8,L6) ,CommunicatingL8) are related to vein left pelvic between sidewall. both IIVs. Variations (G1,L1,L3,L5,L7) are related to right pelvic sidewall, whereas variations (G2,L2,L4,L6,L8) are related to left pelvic sidewall. Surgical considerations. As shown in Figures 17 and 18, the prevalence of IIV variations isSurgical high. These considerations. variation veins As shown may cause in Figures problems 17 and of unexpected 18, the prevalence hemorrhage of IIV during varia- dissectiontions is high. of all These lymph variation node groups. veins may Therefore, cause problems it is crucial of unexpected to recognize hemorrhage the presence dur- of theseing dissection variations, of which all lymph are oftennode encounteredgroups. Therefor intraoperatively.e, it is crucial Gyimaduto recognize et al.the reported presence threeof these (8.1%) variations, cases of which left duplicated are often encountered IIV injuries intraoperatively. (E2 from the IIV Gyimadu classiﬁcation) et al. reported among 37three patients (8.1%) with cases anatomical of left duplicated vessel variations. IIV injuries All (E2 of from the patients the IIV classification) underwent PLND among and 37 paraaorticpatients with lymphadenectomy anatomical vessel for gynecologicalvariations. All malignancies.of the patients Authors underwent concluded PLND thatand anatomicalparaaortic lymphadenectomy vessel variations are for notgynecological uncommon malignancies. and may increase Authors the concluded risk of vascular that an- complicationsatomical vessel during variations PLND are [67 not]. Paniciuncommon et al. describedand may increase the frequency the risk of of retroperitoneal vascular com- variationsplications amongduring 309PLND consecutive [67]. Panici patients et al. described with cervical, the frequency endometrial, of retroperitoneal and ovarian cancer vari- treatedations withamong systematic 309 consecutive aortic and patients PLND. with Authors cervical, observed endometrial, three (1.3%) and ovarian cases of cancer right IIVtreated draining with systematic into the left aortic CIV and (B2 PLND. from the Authors IIV classiﬁcation). observed three There (1.3%) were cases no of casesright IIV of intraoperativedraining into the injury left toCIV these (B2 veinsfrom the [37 ].IIV classification). There were no cases of intraoper- ativeAnatomical injury to these variations veins [37]. of iliac veins—conclusion of surgical considerations. IliacAnatomical vein variations variations and of injuriesiliac veins—conclusion are more common of surgical than arterial considerations. ones. The three- dimensionalIliac vein (3D) variations models are and reconstructed injuries are onmore the common basis ofmulti-detector than arterial ones. computed The three-di- tomog- raphy.mensional The surgeons (3D) models observe are reconstructed the reconstructed on the 3D modelsbasis of andmulti-detector identify all computed of the anatomical tomog- structuresraphy. The before surgeons surgery. observe The the 3D reconstructed models of the 3D pelvic models vessels and mayidentify help all avoid of the injury anatom- to ical structures before surgery. The 3D models of the pelvic vessels may help avoid injury

Diagnostics 2021, 11, x FOR PEER REVIEW 21 of 27

Diagnostics 2021, 11, 89 21 of 27 to anatomical vessel variations during PLNDGO by providing information on individual anatomical features before gynecological procedures [95]. anatomical vessel variations during PLNDGO by providing information on individual anatomical18. Corona featuresMortis, beforeAberrant gynecological and Accessory procedures Obturator [95]. Veins Related to PLNDGO Corona mortis (CMOR) is defined as any vessel anastomoses between the external 18.iliac Corona and obturator Mortis, Aberrant vessels, andexcluding Accessory aberrant Obturator and accessory Veins Related obturator to PLNDGO vessels. These originateCorona from mortis the external (CMOR) iliac is deﬁned or the inferi as anyor vesselepigastric anastomoses vessels and between pierce the obturator external iliacmembrane, and obturator not participating vessels, excluding in anastomoses aberrant [55,96]. and accessoryThe CMOR obturator could be vessels.arterial, venous These originateanastomoses, from or the both. external The iliac frequency or the inferiorof venous epigastric CMOR vessels is higher and than pierce the the arterial. obturator The membrane,CMOR is located not participating behind the in su anastomosesperior pubic [ 55ramus,96]. Theand CMORon the posterior could be arterial,aspect of venous the la- anastomoses,cunar ligament or [55,96–98]. both. The frequency of venous CMOR is higher than the arterial. The CMORAberrant is located and behind accessory the obturator superior pubicveins could ramus arise and from on the the posterior EIV and aspectits tributaries. of the lacunarThe definition ligament of [an55 ,aberrant96–98]. obturator vein is a vein that drains into the EIV system. There is noAberrant other obturator and accessory vein (Figure obturator 19). veins could arise from the EIV and its tributaries. The deﬁnitionAn accessory of an obturator aberrant obturator vein is an vein extra is obturator a vein that vein, drains draining into the into EIV the system. EIV system, There isin no addition other obturator to the normal vein (Figurecounterpart 19). [47,96–98].

Figure 19. An aberrant obturator vein (left pelvic sidewall). EIA—external iliac artery, EIV—exter- Figure 19. An aberrant obturator vein (left pelvic sidewall). EIA—external iliac artery, EIV—external nal iliac vein, PMM—psoas major muscle, AOV—aberrant obturator vein, ON—obturator nerve, iliac vein, PMM—psoas major muscle, AOV—aberrant obturator vein, ON—obturator nerve, OA— OA—obturator artery, DCIV—deep circumflex iliac vein. obturator artery, DCIV—deep circumﬂex iliac vein. Surgical consideration. Damaging the CMOR, aberrant and accessory obturator ves- An accessory obturator vein is an extra obturator vein, draining into the EIV system, insels addition could occur to the throughout normal counterpart medial external [47,96–98 iliac]. and obturator lymph node group dissection.Surgical Aberrant consideration. or accessory Damaging obturator veins the CMOR, have vertical aberrant direction and accessory through the obturator obtura- vesselstor canal. could Injuring occur of throughout these vessels medial is more external troublesome iliac and than obturator CMOR lymphinjury, nodeas obturator group dissection.nerve and artery Aberrant are orlocated accessory nearby obturator and should veins be have preserved. vertical Lee direction et al. reported through thetwo obturator(10.5%) cases canal. of aberrant Injuring obturator of these vesselsveins injury is more during troublesome 19 PLND for than gynecological CMOR injury, malig- as obturatornancies [99]. nerve Selcuk and arteryet al. reported are located four nearby (4.1%) and cases should of CMOR be preserved. injuries among Lee et al.209 reported patients twowho (10.5%) underwent cases PLNDGO of aberrant [100]. obturator veins injury during 19 PLND for gynecological malignancies [99]. Selcuk et al. reported four (4.1%) cases of CMOR injuries among 209 patients who underwent PLNDGO [100].

Diagnostics 2021, 11, 89 22 of 27

19. Nerves Anatomy 19.1. Obturator Nerve (ON) Anatomy The obturator nerve (ON) arises from the ventral roots of the second, third, and fourth lumbar nerves. It descends through the ﬁbers of the psoas major muscle and emerges from its medial border. The ON crosses the sacroiliac joint behind the CIA, lateral to the internal iliac vessels travels along the lateral wall of the lesser pelvis and enters the obturator foramen. The ON is located cranial to the OA and OV [41,101–104].

19.2. ON Variations Related to PLNDGO An accessory obturator nerve (AON) could arise from the anterior divisions of L2–L3, L3 only, L3–L4, from the ON, and from the femoral nerve. The AON is located medially to the femoral nerve and laterally to the ON. The nerve lies on the medial border of the psoas major muscle, but instead of piercing the obturator foramen, it passes over the superior pubic ramus. It runs behind pectineus and divides into three branches, which are also variable. The incidence of AON in the human population varies from 10% to 30%. Studies did not ﬁnd differences of AON presence between genders [41,101–104]. Surgical considerations. Compression and subsequent neuropathy may occur as a result of damage to the AON [103]. Such an injury is possible during a dissection of the lateral external iliac, obturator, lateral, and middle common iliac lymph nodes.

19.3. Genitofemoral Nerve (GFN) Anatomy The origin of the genitofemoral nerve (GFN) is from the ventral rami of L1 and L2 of lumbar plexus. It penetrates the psoas major muscle and runs cranially along the anterior aspect of the muscle, beneath the transversalis fascia and the peritoneum. In most cases, the GFN bifurcates into its both branches midway along the anterior surface of the psoas major. The genital branch follows the inguinal ligament and ends in the skin of mons pubis and labium majus. The femoral branch leaves the pelvis by passing through the femoral sheath lateral to the femoral artery and supplies the skin of the proximal anterior thigh [41,102,105–107].

19.4. The GFN Variations Related to PLNDGO The GFN exhibits a large number of origin variations—T12-L1, L2-L3, L1, L2, and L3. Unilateral absence of the GFN has been reported. In such cases, the ilioinguinal nerve replaces the genital branch and the anterior femoral nerve or lateral cutaneous replaces the femoral branch. The genital or femoral branches of the nerve may arise separately [101,105–107]. Paul and Shastri observed the GFN in 60 hemipelvises. They reported for early division of the nerve into genital and femoral branches at its formation in 13.3% of hemipelvises or in the middle of its course, after emerging from psoas major in 3.3% of specimens [106]. Another study, reported that the most common variation of the GFN was splitting of the nerve into genital and femoral branches within the substance of the psoas muscle [102]. Injury to the GFN may cause entrapment neuropathy [106]. Surgical considerations. As the GFN is the lateral border of PLND, it should be identified on the psoas major muscle prior to PLND. Early division of the GFN into genital and femoral branches means that two nerve fibers would be identified on the psoas major muscle—genital and femoral. If the two nerve fibers are recognized on the psoas major muscle, they should be preserved to prevent neuropathy. Anatomical variations of the GFN and the ON—conclusion of surgical considerations. Cardosi reported a study of 1210 patients, who underwent major pelvic surgeries for gynecological malignancies. Twenty-three patients had postoperative neuropathies. The incidence of obturator nerve injury (39% of all neuropathies) was higher than for other nerve lesions. Genitofemoral neuropathy was identified in four (17.3% of all neuropathies) women who underwent PLND. The frequency of injury of variant ON and GFN during PLNDGO is uncertain, but it is believed to be higher than those with normal anatomy [108]. Diagnostics 2021, 11, 89 23 of 27

There are several strengths of the present article. First, such a comprehensive review of the topic has never been made. Second, despite the multitude of articles describing PLNDGO, authors did not mention differences in morphology of the EIA. Very few anatomical articles reported morphological differences of the EIA [48,53,54]. Third, the different drainage patterns of ILV and ALV have never been discussed in gynecologic oncology. An article presented by Cibula and Rustum illustrated the ILV draining into the EIV and the CIV [5]. Panici et al. discussed the importance of ILV draining into the CIV during PLNDGO [17]. In both articles, it is not mentioned that the ALV could also drain into the CIV, EIV, or IIV. These articles described the ILV as the only vein draining into the EIV or the CIV. Moreover, the ILV and the ALV may drain into the iliac venous system by sharing a common trunk. A potential limitation of the present article is that some of the anatomical variations are rare and there is limited data about the actual incidence of complications during PLNDGO. A possible explanation about the limited data could be that injuries to variant anatomical structures are managed during surgery. Furthermore, injuries with fatal outcome are less likely to be reported. We encourage surgeons to share their experience with injuries to variant anatomical structures during PLNDGO in order to estimate the actual incidence of complications.

20. Conclusions A wide variety of anatomical variations among pelvic structures (ureters, vessels, and nerves) could cause severe and potentially lethal complications during surgery. The majority of the anatomical variations are discovered intraoperatively. Therefore, a detailed knowledge of the anatomy and anatomical variations is essential in order to prevent serious damage to vital structures during pelvic operations. The present article aims to expand the limited knowledge about anatomical variations in the pelvis. An association between variations of the most important pelvic structures and PLND is conducted for the ﬁrst time. We hope that the detailed review of the anatomical variations will decrease patient morbidity and mortality. Furthermore, accurate description and analysis of the majority of pelvic anatomical variations may impact not only gynecological surgery, but also spinal surgery, urology, and orthopedics.

Author Contributions: Conceptualization, S.K. and Y.K.; methodology, S.K., A.Y., and Y.I.; formal analysis, S.S., Y.I., and S.K.; investigation, S.K. and D.D.; resources, D.D., Y.I., and S.K.; data curation, S.S.; writing—original and draft preparation, S.K.; writing—review and editing, S.S., N.D., and Y.I.; visualization, D.D. and N.D.; supervision, A.Y. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Informed Consent Statement: Informed consents were signed antemortem by those participating in the study, stating that they knowingly and willingly donate their bodies to medical education and scientific work. Data Availability Statement: Authors declare that all related data are available concerning researchers by the corresponding author’s email. Acknowledgments: The authors sincerely thank those who donated their bodies to science so that anatomical research could be performed. Results from such research can potentially increase mankind’s overall knowledge that can then improve patient care. Therefore, these donors and their families deserve our highest gratitude [25]. The authors wish to thank Niko Valnarov, Marina Klissourova, Assia Konsulova, and Georgi Kostov for their technical support. The authors wish to thank Miglena Nevyanova Drincheva for her beautiful artwork. Conflicts of Interest: The authors declare no conflict of interest. Diagnostics 2021, 11, 89 24 of 27

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