Skip to Content
MDPIMDPI
DiagnosticsDiagnostics
PDF
  • Review
  • Open Access

7 January 2021

Pelvic Lymphadenectomy in Gynecologic Oncology—Significance of Anatomical Variations

,
,
,
,
,
and
1
Department of Gynecology, Medical University Varna “Prof. Dr. Paraskev Stoyanov”, 9002 Varna, Bulgaria
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
3
Department of Anatomy, Faculty of Medicine, Trakia University, 6000 Stara Zagora, Bulgaria
4
Department of Gynecologic Oncology, Medical University Pleven, 5800 Pleven, Bulgaria
Diagnostics2021, 11(1), 89;https://doi.org/10.3390/diagnostics11010089
This article belongs to the Special Issue Anatomical Variation and Clinical Diagnosis
Version Notes
Order Reprints
Review Reports

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 be familiar with pelvic anatomy and its variations to safely perform a pelvic lymphadenectomy. Learning the proper lymphadenectomy technique relating to anatomical landmarks and variations may decrease 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.

1. Introduction

Pelvic lymph node dissection (PLND) is a common surgical procedure in gynecologic oncology [1]. The lymphatic system is the primary dissemination pathway for gynecological malignancies. PLND is applied for cancer staging, prognosis, surgical, and postoperative 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 survival and disease-free survival [4]. Most studies examine the lymphatic spread, the prognostic, and therapeutic significance of pelvic lymph nodes. However, there are very few studies describing the possible surgical approach, dissection techniques and anatomical variations [5]. There is limited information and disagreement on lymph nodes location, groups, and overall number [6].
Moreover, a correlation between anatomical variations and PLND in the pelvic region has never been discussed in medical literature. Surgeons should be familiar with pelvic anatomy and its variations to safely perform PLND. Learning the proper lymphadenectomy technique relating to anatomical landmarks and variations may decrease morbidity 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 common anatomical variations (of nerves, vessels, ureters) and potential complications related to PLND in the pelvic region are clearly defined.

2. Pelvic Lymph Nodes and Regions

Knowledge of the anatomical localization of lymph node groups in the pelvis is essential for the effectiveness and safety of lymphadenectomy [8]. The pelvic lymph nodes and the connecting lymphatic channels communicate with the venous system; the lymphatic system embryologically develops from vascular plexuses, arising from the venous system [3]. The anatomical localization of the major groups and sub-groups of pelvic lymph nodes is summarized in Figure 1, Figure 2 and Figure 3 [2,6,8,9,10,11,12,13,14,15].
Figure 1. Common iliac lymph nodes classification (open surgery). 1. Lateral—between lateral part of CIV and medial part of psoas major muscle, 2. medial—medial to CIV and CIA, 3. middle—located in the lumbosacral fossa, 4. subaortic—below aortic bifurcation, 5. promontory—at the promontory. AA—abdominal aorta, IVC—inferior vena cava, RV—right renal vein, PMM—psoas major muscle, CIA—common iliac artery, CIV—common iliac vein, Cr—cranial, Ca—caudal, L—Left, R—right.
Figure 2. External iliac lymph nodes classification (embalmed cadaver). 1. Lateral—lateral to external iliac artery, 2. middle—medial to the EIA and lateral to the EIV, 3. medial—medial to both external iliac vessels, 4. obturator—around the obturator nerve and vessels, 5. interiliac—at the level of CIA bifurcation, between the EIA and IIA. PMM—psoas major muscle, EIA—external iliac artery, EIV—external iliac vein, IIA—internal iliac artery, Ur—ureter, U—uterus, B—bladder, SRA—superior 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. Anterior—anterior to anterior division of internal iliac artery, 2. lateral sacral—close to the paired lateral sacral arteries, 3. gluteal—between superior gluteal and internal iliac artery, 4. sacral (presacral)—along median sacral artery. CIA—common iliac artery, IIA—internal iliac artery, OA—obturator artery, UA—umbilical artery, IPA—internal pudendal artery, IGA—inferior gluteal artery, LSA—lateral sacral artery, ILA—iliolumbar artery, Pr—promontorium, S—sacrum.
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].
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 the PLND, are better described.
In medical literature and among surgeons, there are large variations and discrepancies in the nomenclature of the pelvic lymph node regions [2]. The present article and the majority of authors recognize the following pelvic lymph node regions: common iliac; external iliac; internal iliac; obturator; and sacral (or presacral) [5,7,12,13]. Some authors add parametrial, mesorectal, and interiliac regions, while others include tissue from the interiliac region to the external iliac and obturator regions and remove the tissue from the parametrial region together with the parametrium during radical hysterectomy [5,14,15].

3. Selective PLND—Anatomical Landmarks and Techniques

There are several surgical procedures related to dissection of pelvic lymph nodes: sentinel lymph node biopsy, pelvic lymph node sampling, selective lymphadenectomy and complete (systematic) PLND. The present article describes the systematic lymphadenectomy in which all pelvic lymph nodes, draining the pelvic organs, have been removed [1]. Cibula and Rustum presented detailed anatomic boundaries for five pelvic lymph node regions: external iliac, obturator, internal iliac, common iliac, and presacral region [5]. Anatomic boundaries of the common PLND are: ventral—common iliac artery bifurcations, dorsal—abdominal aorta bifurcation, lateral—psoas major muscle, medial—right-medial aspect of common iliac vessels, left-mesoureter [5]. Anatomic boundaries of the external and the internal PLND include common iliac artery bifurcation dorsally, the deep circumflex iliac vein ventrally, and the genitofemoral nerve of the psoas major muscle laterally. The medial border is the obliterated umbilical artery ventrally and the ureter dorsally (Figure 4 and Figure 5) [1,7,15].
Figure 4. Common iliac lymph nodes dissection—anatomic boundaries (open surgery, right side). Dorsal—abdominal aorta bifurcation, ventral—common iliac artery bifurcation, medial—medial aspect of common iliac vessels (on the left side is mesoureter), lateral—psoas major muscle. AAB—abdominal aorta bifurcation, PMM—psoas major muscle, CIAB—common iliac artery bifurcation, M—medial aspect of common iliac vessels on the right side (on the left side is mesoureter), IVC—inferior vena cava, CIA—common iliac artery, CIV—common iliac vein.
Figure 5. External and internal iliac lymph nodes dissection—anatomic boundaries (open surgery 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 artery, EIV—external iliac vein, OV—obturator vein. The medial border is the ureter dorsally and obliterated umbilical 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)
Peritoneal incision. After transecting (not a necessary step) the round ligament, the peritoneum is incised in a posterior (lateral and parallel to the infundibulopelvic ligament) and an anterior (ventrally and laterally to the obliterated umbilical artery) direction. The iliac vessels are exposed from the bifurcation of the aorta to the inguinal ligament.
(2)
Identification of the ureter.
(3)
Lateral paravesical and lateral (Latzko’s space) pararectal space dissection. The lateral paravesical space is dissected between the obliterated umbilical artery and the external iliac vessels. Lateral pararectal space is dissected between the internal iliac artery and the ureter.
(4)
Genitofemoral nerve identification. Lateral incision to the fascia of the psoas muscle is preferable in order to avoid genitofemoral nerve injury. The nerve is located lateral to the external iliac vessels and sometimes overlying them.
(5)
External iliac region dissection: lateral and medial external iliac vessels dissection. The dissection begins at the origin of the external iliac vessels and finishes down to the point where the deep circumflex iliac vein crosses over the external iliac artery.
(6)
Obturator region dissection. The obturator space is approached by retracting the external iliac vessels medially and the psoas muscle laterally, and by dissection of the areolar tissue that lies directly between these vessels and the lateral pelvic wall. The obturator nerve is identified. The procedure is followed by lateral retraction of the external iliac vessels to expose the obturator space. Superficial obturator lymph nodes are dissected after obturator nerve visualization (obturator nerve stripping). For locally advanced cervical cancer cases, PLND continues with dissection of the deep obturator lymph nodes and the gluteal nodes.
(7)
Internal iliac region dissection. Lymph nodes are removed medially and anteriorly to the internal iliac 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 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 [1,5,7,16,17,18,19].

7. Iliac Vessel Variations

7.1. Iliac Arteries

As 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].

7.2. Common Iliac Artery (CIA) Anatomy

The abdominal aorta bifurcates anterolaterally to the left side of the fourth lumbar vertebral body and divides into the left and right common iliac arteries. They further divide into the external and internal iliac arteries at the level of the sacroiliac joint. The right CIA (5 cm) is frequently longer than its left counterpart (4 cm) [41].

7.3. CIA Variations Related to PLNDGO

CIA variations are relatively 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, predominantly to the right, even though bilateral agenesis of CIA has also been described [42,43,44]. In one of the cases, described by Shetty et al., the abdominal aorta was directly branching into external and internal iliac arteries at the level of the 4th–5th lumbar 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 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 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 artery originated from the CIA [46].
Surgical considerations. In cases of absent CIA, surgeons should be aware of collateral, anomalous, or aberrant arteries. Collateral arteries serve as an alternative blood source, compensating the absent CIA; they might be of atypical origin from the iliac system. Iliolumbar arteries, originating from the CIA or CIA bifurcation, may be damaged during a middle common iliac lymph nodes dissection of the lumbosacral fossa.

8. External/Internal Iliac Artery Anatomy

The external iliac artery (EIA) is a direct continuation of the CIA. It runs downwards, forwards in the iliac fossa, and reaches the lacuna vasorum under the inguinal ligament. The EIA has two branches: inferior epigastric artery and deep circumflex iliac artery. After crossing the mid-inguinal point, it continues as a common femoral artery. The internal 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 Figure 7.
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.

12. Iliac Veins

12.1. Common Iliac Vein Anatomy (CIV)

Common iliac veins (CIVs) drain into the inferior vena cava. They are a direct continuation of the external iliac veins and are formed by the junction of the external and internal iliac venous system, anterior to the sacroiliac joints. The left CIV is longer than the right 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].

12.2. CIV Variations Related to the PLNDGO

Surgical considerations. All types of CIV variations are related to possible venous injuries (Figure 13) [35,69,70,71,72,73,74]. 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 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 of the right CIV, surrounding the right CIA. The other patient had a duplicated left CIV (B2 from the CIV classification), which was injured during dissection. Authors concluded that each patient’s vascular anatomy must be assessed individually to avoid injuries during scheduled operations [75].
Figure 13. Common iliac vein variations. (A) Incomplete duplication of the CIV; (B) complete duplication of the CIV; (C) lateral duplicated branch drains into the IVC, the medial drain into the CIV. (D) Absent CIV, external and internal iliac veins drain to the contralateral CIV; (E) absent CIV, the EIV drains into the IVC, the IIV drains into the contralateral CIV; (F) Absent CIV, the external and internal veins drain into IVC. Inferior vena cava (IVC), Common iliac vein (CIV), external iliac vein (EIV), internal iliac vein (IIV). (A1,B1,C1,D1,E1,F1) are related to right hemipelvises variations, whereas (A2,B2,C2,D2,E2,F2) are related to left hemipelvises variations.

12.3. CIV Tributaries Variations Related to PLNDGO

Iliolumbar vein (ILV) and ascending lumbar vein (ALV) anatomy. The ILV drains the venous blood from the iliac fossa, the iliac, and psoas muscles and terminates in the CIV. It is considered the segmental equivalent of the fifth lumbar vertebra [76,77,78,79,80,81]. The ALV participates in an anastomotic venous system between the inferior vena cava and the superior vena cava. The lower end of the ALV enters the cephalic border of the CIV. Upwards, the ALV receives the lumbar veins and terminates by joining the subcostal vein to form the azygos vein on the right and the hemiazygos on the left. ILV anastomoses with ALV, deep circumflex iliac vein and lateral sacral vein [76,77,78,79,80,81].
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 [76,77,78,79,80,81]. 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 a common trunk, ILV draining into the external/internal iliac venous system. Lolis et al. reported a detailed description of the surgical anatomy and draining patterns of the ILV, based on a significantly great number of specimens [77]. They proposed and illustrated a detail classification separated into two types. In Type I (54%), ILV drainage patterns differed, whereas the ALV had the same pattern on both sides. In Type II, the ALV differed in pattern from one side to the other (46%). Authors observed high percentage of drainage variations in ILV 91% compare to ALV 34% [77]. Numerously drainage variations of ILV and ALV have been reported, but in Figure 14 are illustrated the most important during PLNDGO. The ILV and ALV drainage variations during PLND in our practice are shown in Figure 15.
Figure 14. ILV and ALV anatomy and variations. (A) ILV and ALV anatomy. HV—hemiazygos vein, LV—lumbar veins, ALV—ascending lumbar vein, ILV—iliolumbar vein, IVC—inferior vena cava, LRV—left renal vein, RRV—right renal vein, AV—azygos vein. (B) ILV variations. 1—drains into EIV, 2—drains into the confluence of the CIV, 3—drains into 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, 3—drains into the IIV. (D) Common trunks between ALV and ILV. 1—drains into the EIV, 2—drains into the confluence of CIV, 3—drains into the IIV, 4—drains into the CIV.
Figure 15. ILV or ALV drain into the EIV (open surgery right pelvic sidewall). We can only speculate if these veins are ILV, ALV, or both. (A) Two separate veins drain 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 prevent venous damage such as tears and avulsion of these veins during PLND. Injury of ILV and ALV could occur in the course of external and internal iliac lymph nodes dissection. Special attention should be paid during middle common iliac (located in the lumbosacral fossa) and lateral external iliac lymph nodes dissection. Panici et al. stated that during lateral common iliac lymph nodes dissection, the presence of iliolumbal veins could be hazardous as several iliolumbar veins could drain into the CIV. Authors concluded that the CIV should be handled very gently, and dissection must be blunt and delicate [17].

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, 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 weeks of gestation—the subcardinal, the postcardinal, and the supracardinal veins [41,42,88,89].

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 [41,101,102,103,104].

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 [41,101,102,103,104].
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 [41,102,105,106,107].

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 [101,105,106,107]. 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].
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.

Data Availability

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.

References

  1. Singh, K.; Fares, R. Pelvic and Para-aortic Lymphadenectomy in Gynecologic Cancers. In Gynecologic and Obstetric Surgery: Challenges and Management Options, 1st ed.; Coomarasamy, A., Shafi, M., Davila, G.W., Chan, K.K., Eds.; John Wiley & Sons Inc.: New York, NY, USA, 2016; pp. 408–411. [Google Scholar] [CrossRef]
  2. Mangan, C.E.; Rubin, S.C.; Rabin, D.S.; Mikuta, J.J. Lymph node nomenclature in gynecologic oncology. Gynecol. Oncol. 1986, 23, 222–226. [Google Scholar] [CrossRef]
  3. Bakkum Gamez, J.N. Lymphadenectomy in the Management of Gynecologic Cancer. Clin. Obstet. Gynecol. 2019, 62, 749–755. [Google Scholar] [CrossRef]
  4. Fowler, J.; Backes, F. Pelvic and Paraaortic Lymphadenectomy in Gynecologic Cancers up to Date 2020. Available online: https://www.uptodate.com/contents/pelvic-and-paraaortic-lymphadenectomy-in-gynecologic-cancers (accessed on 8 November 2020).
  5. Cibula, D.; Abu-Rustum, N.R. Pelvic lymphadenectomy in cervical cancer—surgical anatomy and proposal for a new classification system. Gynecol. Oncol. 2010, 116, 33–37. [Google Scholar] [CrossRef]
  6. Canessa, C.E.; Miegge, L.M.; Bado, J.; Silveri, C.; Labandera, D. Anatomic Study of Lateral Pelvic Lymph Nodes: Implications in the Treatment of Rectal Cancer. Dis. Colon Rectum 2004, 47, 297–303. [Google Scholar] [CrossRef]
  7. Selçuk, İ.; Uzuner, B.; Boduç, E.; Baykuş, Y.; Akar, B.; Güngör, T. Pelvic lymphadenectomy: Step-by-step surgical education video. J. Turk. Ger. Gynecol. Assoc. 2020, 21, 66–69. [Google Scholar] [CrossRef]
  8. McMahon, C.J.; Rofsky, N.M.; Pedrosa, I. Lymphatic Metastases from Pelvic Tumors: Anatomic Classification, Characterization, and Staging. Radiology 2010, 254, 31–46. [Google Scholar] [CrossRef]
  9. Kolbenstvedt, A.; Kolstad, P. The difficulties of complete pelvic lymph node dissection in radical hysterectomy for carcinoma of the cervix. Gynecol. Oncol. 1976, 4, 244–254. [Google Scholar] [CrossRef]
  10. Ovcharov, V.; Vankov, V. Human Anatomy, 14th ed.; ARSO Publishing: Sofia, Bulgaria, 2019; pp. 632–633. [Google Scholar]
  11. Vincent, P. Lymphatic System 9 Quick Study Academic, 1st ed.; BarCharts Publishing: Boca Raton, FL, USA, 2016. [Google Scholar]
  12. Paño, B.; Sebastià, C.; Ripoll, E.; Paredes, P.; Salvador, R.; Buñesch, L.; Nicolau, C. Pathways of Lymphatic Spread in Gynecologic Malignancies. RadioGraphics 2015, 35, 916–945. [Google Scholar] [CrossRef] [PubMed]
  13. Sakuragi, N.; Satoh, C.; Takeda, N.; Hareyama, H.; Takeda, M.; Yamamoto, R.; Fujimoto, T.; Oikawa, M.; Fujino, T.; Fujimoto, S. Incidence and distribution pattern of pelvic and paraaortic lymph node metastasis in patients with stages IB, IIA, and IIB cervical carcinoma treated with radical hysterectomy. Cancer 1999, 85, 1547–1554. [Google Scholar] [CrossRef]
  14. Liu, Z.; Hu, K.; Liu, A.; Shen, J.; Hou, X.; Lian, X.; Sun, S.; Yan, J.; Zhang, F. Patterns of lymph node metastasis in locally advanced cervical cancer. Medicine 2016, 95, e4814. [Google Scholar] [CrossRef] [PubMed]
  15. Panici, P.B.; Scambia, G.I.; Baiocchi, G.A.; Matonti, G.I.; Capelli, A.R.; Mancuso, S.A. Anatomical study of para-aortic and pelvic lymph nodes in gynecologic malignancies. Obstet. Gynecol. 1992, 79, 498–502. [Google Scholar] [PubMed]
  16. Centini, G.; Fernandes, R.P.; Afors, K.; Murtada, R.; Puga, M.F.; Wattiez, A. Radical Hysterectomy and Pelvic Lymphadenectomy (French School). Hysterectomy 2017, 589–595. [Google Scholar] [CrossRef]
  17. Benedetti Panici, P.; Basile, S.; Angioli, R. Pelvic and aortic lymphadenectomy in cervical cancer: The standardization of surgical procedure and its clinical impact. Gynecol. Oncol. 2009, 113, 284–290. [Google Scholar] [CrossRef]
  18. Jones, H.W.; Rock, J.A. Te Linde’s Operative Gynecology, 10th ed.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2008. [Google Scholar]
  19. Chen, J.J.; Zhu, Z.S.; Zhu, Y.Y.; Shi, H.Q. Applied anatomy of pelvic lymph nodes and its clinical significance for prostate cancer:a single-center cadaveric study. BMC Cancer 2020, 20, 330. [Google Scholar] [CrossRef]
  20. Frober, R. Surgical anatomy of the ureter. BJU Int. 2007, 100, 949–965. [Google Scholar] [CrossRef]
  21. Razvan, R.; Geiorgescu, D.; Geavlete, P.; Bogdan, B. Retrograde Ureteroscopy: Handbook of Endourology. In Notions of Histology, Anatomy, and Physiology of the Upper Urinary Tract, 1st ed.; Geavlete, P., Ed.; Academic Press: Cambridge, MA, USA, 2016; pp. 7–19. [Google Scholar]
  22. Wedel, T. Topographical Anatomy for Hysterectomy Procedures. In Hysterectomy a Comprehensive Surgical Approach, 1st ed.; Alkatout, I., Mettler, L., Eds.; Springer: Cham, Switzerland, 2018; pp. 37–60. [Google Scholar]
  23. Selçuk, İ.; Ersak, B.; Tatar, İ.; Güngör, T.; Huri, E. Basic clinical retroperitoneal anatomy for pelvic surgeons. Turk. J. Obstet. Gynecol. 2018, 15, 259–269. [Google Scholar] [CrossRef]
  24. Amar, A.D.; Hutch, J.A. Anomalies of the Ureter. In Malformations (Handbuch der Urologie/Encyclopedia of Urology/Encyclopédie d’Urologie); Springer: Berlin, Germany, 1968. [Google Scholar] [CrossRef]
  25. Nation, E.F. Duplication of the Kidney and Ureter: A Statistical Study of 230 New Cases. J. Urol. 1944, 51, 456–465. [Google Scholar] [CrossRef]
  26. Foley, C.E.; Mansuria, S. Ureteral anomalies in gynecologic surgery. J. Minim. Invasive Gynecol. 2020, 27, 566–567. [Google Scholar] [CrossRef] [PubMed]
  27. Mayers, M.M. Diverticulum of the ureter. J. Urol. 1949, 61, 344–350. [Google Scholar] [CrossRef]
  28. McLoughlin, L.C.; Davis, N.F.; Dowling, C.; Eng, M.P.; Power, R.E. Ureteral diverticulum: A review of the current literature. Can. J. Urol. 2013, 20, 6893–6896. [Google Scholar]
  29. Papin, E.; Eisendrath, D.N. Classification of Renal and Ureteral Anomalies. Ann. Surg. 1927, 85, 735–756. [Google Scholar] [PubMed]
  30. Tawfik, A.M.; Younis, M.H. Computed Tomography Imaging Appearance of a Unique Variant of Retroiliac Ureter. Urology 2016, 88, e7–e9. [Google Scholar] [CrossRef]
  31. Prasad, H.L.; Karthikeyan, V.S.; Shivalingaiah, M.; Ratkal, C.S. Retroiliac ureter presenting as right upper ureteric obstruction—Report of a rare case. Int. J. Res. Med. Sci. 2015, 3, 2143–2144. [Google Scholar] [CrossRef]
  32. Ebiloglu, T.; Kaya, E.; Zorba, O.; Kibar, Y.; Gok, F. Retro-Iliac Ureters: Review of Literature and Two Cases with Two Different Techniques. Turk. Klin. J. Case Rep. 2016, 24, 66–69. [Google Scholar] [CrossRef]
  33. Parashar, M.; Sharma, R.K.; Kumar, S. Ureteric injury in gynaecological surgery: A rare but serious event. Int. J. Health Sci. Res. 2019, 9, 397–401. [Google Scholar]
  34. Mylonas, I.; Briese, V.; Vogt-Weber, B.; Friese, K. Complete bilateral crossed ureteral duplication observed during a radical hysterectomy with pelvic lymphadenectomy for ovarian cancer. A case report. Arch. Gynecol. Obstet. 2003, 267, 250–251. [Google Scholar] [CrossRef]
  35. Ostrzenski, A.; Radolinski, B.; Ostrzenska, K.M. A review of laparoscopic ureteral injury in pelvic surgery. Obstet. Gynecol. Surv. 2003, 58, 794–799. [Google Scholar] [CrossRef]
  36. Davis, A.A. Transection of Duplex Ureter During Vaginal Hysterectomy. Cureus 2020, 12, e6597. [Google Scholar] [CrossRef]
  37. Benedetti-Panici, P.; Maneschi, F.; Scambia, G.; Greggi, S.; Mancuso, S. Anatomic abnormalities of the retroperitoneum encountered during aortic and pelvic lymphadenectomy. Am. J. Obstet. Gynecol. 1994, 170 Pt 1, 111–116. [Google Scholar] [CrossRef]
  38. Dalzell, A.P.B.; Robinson, R.G.; Crooke, K.M. Duplex ureter damaged during laparoscopic hysterectomy. Pelviperineology 2010, 29, 88. [Google Scholar]
  39. Subbiah, S.; Rajaraman, N.N. Congenital anomalies in surgical oncology practice. Edorium J. Surg. 2015, 2, 29–36. [Google Scholar] [CrossRef]
  40. Li, J.; Wang, Z.; Chen, C.; Liu, P.; Duan, H.; Chen, L.; Wang, J.; Tan, H.; Li, P.; Zhao, C.; et al. Distribution of iliac veins posterior to the common iliac artery bifurcation related to pelvic lymphadenectomy: A digital in vivo anatomical study of 442 Chinese females. Gynecol. Oncol. 2016, 141, 538–542. [Google Scholar] [CrossRef]
  41. Gray, H.; Standring, S.; Hrold Ellis, H.; Berkovitz, B. Gray’s Anatomy: The Anatomical Basis of Clinical Practice, 39th ed.; Elsevier Churchill Livingstone Edinburgh: New York, NY, USA, 2005; pp. 2171–2175. [Google Scholar]
  42. Tubbs, R.S.; Shoja, M.M.; Loukas, M. Bergman’s Comprehensive Encyclopedia of Human Anatomic Variation; John Wiley & Sons: Hoboken, NJ, USA, 2016; pp. 669–673, 884–889. [Google Scholar]
  43. Shetty, S.; Kantha, L.; Sheshgiri, C. Bilateral absence of common iliac artery—A cadaveric observation. Int. J. Anat. Var. 2013, 6, 7–8. [Google Scholar]
  44. Dabydeen, D.A.; Shabashov, A.; Shaffer, K. Congenital Absence of the Right Common Iliac Artery. Radiol. Case Rep. 2015, 3, 47. [Google Scholar] [CrossRef]
  45. Llauger, J.; Sabaté, J.M.; Guardia, E.; Escudero, J. Congenital absence of the right common iliac artery: CT and angiographic demonstration. Eur. J. Radiol. 1995, 21, 128–130. [Google Scholar] [CrossRef]
  46. Rusu, M.C.; Cergan, R.; Dermengiu, D.; Curcă, G.C.; Folescu, R.; Motoc, A.G.M.; Jianu, A.M. The iliolumbar artery—Anatomic considerations and details on the common iliac artery trifurcation. Clin. Anat. 2009, 23, 93–100. [Google Scholar] [CrossRef]
  47. Lierse, W. Applied Anatomy of the Pelvis, 1st ed.; Springer: Berlin/Heidelberg, Germany, 1987; pp. 47–58. [Google Scholar] [CrossRef]
  48. Badagabettu Nayak, S.; Padur Aithal, A.; Kumar, N.; Regunathan, D.; Shetty, P.; Alathady Maloor, P. A cadaveric study of variations of external iliac artery and its implication in trauma and radiology. Morphologie 2019, 103, 24–31. [Google Scholar] [CrossRef]
  49. Tamisier, D.; Melki, J.-P.; Cormier, J.-M. Congenital Anomalies of the External Iliac Artery: Case Report and Review of the Literature. Ann. Vasc. Surg. 1990, 4, 510–514. [Google Scholar] [CrossRef]
  50. Kawashima, T.; Sato, K.; Sasaki, H. A human case of hypoplastic external iliac artery and its collateral pathways. Folia Morphol. 2006, 65, 157–160. [Google Scholar]
  51. Okamoto, K.; Wakebe, T.; Saiki, K.; Nagashima, S. Consideration of the potential courses of the common iliac artery. Anat. Sci. Int. 2005, 80, 116–119. [Google Scholar] [CrossRef]
  52. Safi, K.C.; Teber, D.; Moazen, M.; Anghel, G.; Maldonado, R.V.; Rassweiler, J.J. Laparoscopic repair of external iliac-artery transection during laparoscopic radical prostatectomy. J. Endourol. 2006, 20, 237–239. [Google Scholar] [CrossRef] [PubMed]
  53. Boonruangsri, P.; Suwannapong, I.; Rattanasuwan, S.; Iamsaard, S. Aneurysm, tortuosity, and kinking of abdominal aorta and iliac arteries in Thai cadavers. Int. J. Morphol. 2015, 33, 73–76. [Google Scholar] [CrossRef]
  54. Moul, J.W.; Wind, G.G.; Wright, C.R. Tortuous and aberrant external iliac artery precluding radical retropubic prostatectomy for prostate cancer. Urology 1993, 42, 450–452. [Google Scholar] [CrossRef]
  55. Kostov, S.; Slavchev, S.; Dzhenkov, D.; Stoyanov, G.; Dimitrov, N.; Yordanov, A. Corona mortis, aberrant obturator vessels, accessory obturator vessels: Clinical applications in gynecology. Folia Morphol. 2020. [Google Scholar] [CrossRef]
  56. Sañudo, J.R.; Roig, M.; Rodriguez, A.; Ferreira, B.; Domenech, J.M. Rare origin of the obturator, inferior epigastric and medial circumflex femoral arteries from a common trunk. J. Anat. 1993, 183, 161–163. [Google Scholar]
  57. Fătu, C.; Puişoru, M.; Fătu, I.C. Morphometry of the internal iliac artery in different ethnic groups. Ann. Anat. 2006, 188, 541–546. [Google Scholar] [CrossRef]
  58. Adachi, B. Das Arteriensystem der Japaner, Bd. II; Kyoto. Supp. to Acta Scholae Medicinalis Universitatis Imperalis in Kioto: Tokyo, Japan, 1928; Volume 9, pp. 1926–1927. [Google Scholar]
  59. Yamaki, K.; Saga, T.; Doi, Y.; Aida, K.; Yoshizuka, M. A statistical study of the branching of the human internal iliac artery. Kurume Med. J. 1998, 45, 333–340. [Google Scholar] [CrossRef]
  60. Liapis, K.; Tasis, N.; Tsouknidas, I.; Tsakotos, G.; Skandalakis, P.; Vlasis, K.; Filippou, D. Anatomic variations of the Uterine Artery. Review of the literature and their clinical significance. Turk. J. Obstet. Gynecol. 2020, 17, 58–62. [Google Scholar] [CrossRef]
  61. Kumari, S.; Trinesh Gowda, M.S. A study of variations of origin of obturator artery: Review in south Indian population. J. Anat. Soc. India 2016, 65, S1–S4. [Google Scholar] [CrossRef]
  62. Granite, G.; Meshida, K.; Wind, G. Frequency and Clinical Review of the Aberrant Obturator Artery: A Cadaveric Study. Diagnostics 2020, 10, 546. [Google Scholar] [CrossRef]
  63. Sañudo, J.R.; Mirapeix, R.; Rodriguez-Niedenführ, M.; Maranillo, E.; Parkin, I.G.; Vázquez, T. Obturator artery revisited. Int. Urogynecol. J. 2011, 22, 1313–1318. [Google Scholar] [CrossRef]
  64. Bae, J.W.; Lee, J.H.; Choi, J.S.; Son, C.E.; Jeon, S.W.; Hong, J.H.; Eom, J.M.; Joo, K.J. Laparoscopic lymphadenectomy for gynecologic malignancies: Evaluation of the surgical approach and outcomes over a seven-year experience. Arch Gynecol. Obstet. 2012, 285, 823–829. [Google Scholar] [CrossRef]
  65. Ricciardi, E.; di Martino, G.; Maniglio, P.; Schimberni, M.; Frega, A.; Jakimovska, M.; Kobal, B.; Moscarini, M. Life-threatening bleeding after pelvic lymphadenectomy for cervical cancer: Endovascular management of ruptured false aneurysm of the external iliac artery. World J. Surg. Onc. 2012, 10, 149. [Google Scholar] [CrossRef]
  66. Ishikawa, M.; Nakayama, K.; Razia, S.; Yamashita, H.; Ishibashi, T.; Sato, S.; Sasamori, H.; Sawada, K.; Kurose, S.; Ishikawa, N.; et al. External Iliac Artery Injury and Thrombosis during Laparoscopic Gynecologic Surgery. Case Rep. Obstet. Gynecol. 2020. [Google Scholar] [CrossRef]
  67. Gyimadu, A.; Salman, M.C.; Karcaaltincaba, M.; Yuce, K. Retroperitoneal vascular aberrations increase the risk of vascular injury during lymphadenectomy in gynecologic cancers. Arch Gynecol. Obstet. 2012, 286, 449–455. [Google Scholar] [CrossRef] [PubMed]
  68. Fotopoulou, C.; Neumann, U.; Kraetschell, R.; Lichtenegger, W.; Sehouli, J. External iliac artery ligation due to late postoperative rupture after radical lymphadenectomy for advanced ovarian cancer—Two case reports. Eur. J. Gynaecol. Oncol. 2010, 31, 198–200. [Google Scholar] [PubMed]
  69. Mehta, K.; Iwanaga, J.; Tubbs, R.S. Absence of the Right Common Iliac Vein with the Right Internal Iliac Vein Arising from the Left Common Iliac Vein: Case Report. Cureus 2019, 11, e4575. [Google Scholar] [CrossRef]
  70. Morris, H. Human Anatomy: A Complete Systematic Treatise by English and American Authors, 5th ed.; P. Blakiston, Son & Co.: Philadelphia, PA, USA, 1893. [Google Scholar] [CrossRef]
  71. Cardinot, T.M.; Aragão, A.H.; Babinski, M.A.; Favorito, L.A. Rare variation in course and affluence of internal iliac vein due to its anatomical and surgical significance. Surg. Radiol. Anat. 2006, 28, 422–425. [Google Scholar] [CrossRef]
  72. Yahyayev, A.; Bulakci, M.; Yilmaz, E.; Ucar, A.; Sayin, O.A.; Yekeler, E. Absence of the right iliac vein and an unusual connection between both common femoral veins. Phlebology 2013, 28, 162–164. [Google Scholar] [CrossRef]
  73. Panchal, P.; Chaturvedi, H. Agenesis of common iliac vein encroaching development of inferior vena cava. IJAV 2014, 7, 21–23. [Google Scholar]
  74. Nusrath, S.; Pawar, S.; Goel, V.; Raju, K. Common Internal Iliac Vein Joining Inferior Vena Cava—A Rare Anatomical Variation: Anatomic and Surgical Relevance. Indian J. Surg. 2020, 82, 701–703. [Google Scholar] [CrossRef]
  75. Kose, M.F.; Turan, T.; Karasu, Y.; Gundogdu, B.; Boran, N.; Tulunay, G. Anomalies of Major Retroperitoneal Vascular Structure. Int. J. Gynecol. Cancer 2011, 21, 1312–1319. [Google Scholar] [CrossRef] [PubMed]
  76. Jasani, V.; Jaffray, D. The anatomy of the iliolumbar vein: A cadaver study. J. Bone Joint Surg. Br. 2002, 84, 1046–1049. [Google Scholar] [CrossRef]
  77. Lolis, E.; Panagouli, E.; Venieratos, D. Study of the ascending lumbar and iliolumbar veins: Surgical anatomy, clinical implications and review of the literature. Ann. Anat. 2011, 193, 516–529. [Google Scholar] [CrossRef]
  78. Unruh, K.P.; Camp, C.L.; Zietlow, S.P.; Huddleston, P.M. Anatomical variations of the iliolumbar vein with application to the anterior retroperitoneal approach to the lumbar spine: A cadaver study. Clin. Anat. 2008, 21, 666–673. [Google Scholar] [CrossRef]
  79. Venieratos, D.; Panagouli, E.; Lolis, E. Variations of the iliac and pelvic venous systems with special attention to the drainage patterns of the ascending lumbar and iliolumbar veins. Ann. Anat. 2012, 194, 396–403. [Google Scholar] [CrossRef]
  80. Hamid, M.; Toussaint, P.J.; Delmas, V.; Gillot, C.; Coutaux, A.; Plaisant, O. Anatomical and radiological evidence for the iliolumbar vein as an inferior lumbar venous system. Clin. Anat. 2007, 20, 545–552. [Google Scholar] [CrossRef]
  81. Sivakumar, G.; Paluzzi, A.; Freeman, B. Avulsion of ascending lumbar and iliolumbar veins in anterior spinal surgery: An anatomical study. Clin. Anat. 2007, 20, 553–555. [Google Scholar] [CrossRef]
  82. Lotz, P.R.; Seeger, J. Normal variation in iliac venous anatomy. AJR 1982, 138, 735–738. [Google Scholar] [CrossRef] [PubMed]
  83. Djedovic, G.; Putz, D. Case report: Description of a venous annulus of the external iliac vein. Ann. Anat. 2006, 188, 451–453. [Google Scholar] [CrossRef] [PubMed]
  84. Hayashi, S.; Naito, M.; Yakura, T.; Kumazaki, T.; Itoh, M.; Nakano, T. A case of an additional right external iliac vein surrounding the right external iliac artery and lacking the right common iliac vein. Anat. Sci. Int. 2015, 91, 106–109. [Google Scholar] [CrossRef] [PubMed]
  85. Nezhat, C.; Childers, J.; Nezhat, F.; Nezhat, C.H.; Seidman, D.S. Major retroperitoneal vascular injury during laparoscopic surgery. Hum. Reprod. 1997, 12, 480–483. [Google Scholar] [CrossRef] [PubMed]
  86. Herraiz Roda, J.L.; Llueca, A.; Maazouzi, Y.; Piquer Simó, D.; Guijarro Colomer, M.; Sentís Masllorens, J. Complications of laparoscopic lymphadenectomy for gynecologic malignancies. Experience of 372 patients. Res. Rep. Gynaecol. Obstet. 2017, 1, 12–16. [Google Scholar]
  87. Ghassemi, A.; Furkert, R.; Prescher, A.; Riediger, D.; Knobe, M.; O’dey, D.; Gerressen, M. Variants of the supplying vessels of the vascularized iliac bone graft and their relationship to important surgical landmarks. Clin. Anat. 2013, 26, 509–521. [Google Scholar] [CrossRef]
  88. Elsy, B.; Alghamdi, A.; Osman, L. Bilateral branching variants of internal and external iliac arteries—Cadaveric study Case Report. Eur. J. Anat. 2020, 24, 63–68. [Google Scholar]
  89. Vidal, V.; Monnet, O.; Jacquier, A.; Bartoli, J.-M.; Tropiano, P. Accessory Iliac Vein. J. Spinal Disord Tech. 2010, 23, 398–403. [Google Scholar] [CrossRef]
  90. Shin, M.; Lee, J.B.; Park, S.B.; Park, H.J.; Kim, Y.S. Multidetector computed tomography of iliac vein variation: Prevalence and classification. Surg. Radiol. Anat. 2014, 37, 303–309. [Google Scholar] [CrossRef]
  91. Morita, S.; Saito, N.; Mitsuhashi, N. Variations in internal iliac veins detected using multidetector computed tomography. Acta Radiol. 2007, 48, 1082–1085. [Google Scholar] [CrossRef]
  92. Chong, G.O.; Lee, Y.H.; Hong, D.G.; Cho, Y.L.; Lee, Y.S. Anatomical variations of the internal iliac veins in the presacral area: Clinical implications during sacral colpopepxy or extended pelvic lymphadenectomy. Clin. Anat. 2014, 28, 661–664. [Google Scholar] [CrossRef]
  93. Nayak, S.B. Dangerous twisted communications between external and internal iliac veins which might rupture during catheterization. Anat. Cell. Biol. 2018, 51, 309–311. [Google Scholar] [CrossRef]
  94. Kanjanasilp, P.; Ng, J.L.; Kajohnwongsatit, K.; Thiptanakit, C.; Limvorapitak, T.; Sahakitrungruang, C. Anatomical Variations of Iliac Vein Tributaries and Their Clinical Implications During Complex Pelvic Surgeries. Dis. Colon Rectum. 2019, 62, 809–814. [Google Scholar] [CrossRef] [PubMed]
  95. Duan, H.; Liu, P.; Chen, C.; Chen, L.; Li, P.; Li, W.; Gong, S.; Xv, Y.; Chen, R.; Tang, L. Reconstruction of three-dimensional vascular models for lymphadenectomy before surgery. Minim. Invasive Ther. Allied Technol. 2020, 29, 42–48. [Google Scholar] [CrossRef] [PubMed]
  96. Sanna, B.; Henry, B.M.; Vikse, J.; Skinningsrud, B.; Pękala, J.R.; Walocha, J.A.; Cirocchi, R.; Tomaszewski, K.A. The prevalence and morphology of the corona mortis (Crown of death): A meta-analysis with implications in abdominal wall and pelvic surgery. Injury 2018, 49, 302–308. [Google Scholar] [CrossRef] [PubMed]
  97. Darmanis, S.; Lewis, A.; Mansoor, A.; Bircher, M. Corona mortis: An anatomical study with clinical implications in approaches to the pelvis and acetabulum. Clin. Anat. 2007, 20, 433–439. [Google Scholar] [CrossRef] [PubMed]
  98. Berberoĝlu, M.; Uz, A.; Özmen, M.M.; Bozkurt, C.; Erkuran, C.; Taner, S.; Tekin, A.; Tekdemir, I. Corona mortis: An anatomic study in seven cadavers and an endoscopic study in 28 patients. Surg. Endosc. 2001, 15, 72–75. [Google Scholar] [CrossRef] [PubMed]
  99. Lee, Y.S. Early experience with laparoscopic pelvic lymphadenectomy in women with gynecologic malignancy. J. Am. Assoc. Gynecol. Laparosc. 1999, 6, 59–63. [Google Scholar] [CrossRef]
  100. Selçuk, İ.; Tatar, İ.; Fırat, A.; Huri, E.; Güngör, T. Is corona mortis a historical myth? A perspective from a gynecologic oncologist. J. Turk. Ger. Gynecol. Assoc. 2018, 19, 171–172. [Google Scholar] [CrossRef]
  101. Anagnostopoulou, S.; Kostopanagiotou, G.; Paraskeuopoulos, T.; Chantzi, C.; Lolis, E.; Saranteas, T. Anatomic Variations of the Obturator Nerve in the Inguinal Region. Reg. Anesth. Pain Med. 2009, 34, 33–39. [Google Scholar] [CrossRef]
  102. Anloague, P.A.; Huijbregts, P. Anatomical Variations of the Lumbar Plexus: A Descriptive Anatomy Study with Proposed Clinical Implications. J. Man Manip. Ther. 2009, 17, 107E–114E. [Google Scholar] [CrossRef]
  103. Turgut, M.; Protas, M.; Gardner, B.; Oskouian, R.; Loukas, M.; Tubbs, R. The accessory obturator nerve: An anatomical study with literature analysis. Anatomy 2017, 11, 121–127. [Google Scholar] [CrossRef]
  104. Archana, B.J.; Nagaraj, D.N.; Pradeep, P.; Subhash, L. Anatomical Variations of Accessory Obturator Nerve: Cadaveric Study with Proposed Clinical Implications. Int. J. Anat. Res. 2016, 4, 2158–2161. [Google Scholar] [CrossRef]
  105. Gindha, G.S.; Arora, D.; Kaushal, S.; Chhabra, U. Variations in origin of the genitofemoral nerve from the lumbar plexuses in north Indian population (a cadaveric study). MOJ Anat. Physiol. 2015, 1, 72–76. [Google Scholar] [CrossRef]
  106. Paul, L.; Shastri, D. Anatomical variations in formation and branching pattern of the border nerves of lumbar Region. Natl. J. Clin. Anat. 2019, 8, 57–61. [Google Scholar] [CrossRef]
  107. Deepti, A.; Shyam, S.T.; Subhash, K.; Usha, C. Morphology of Lumbar Plexus and Its Clinicalsignificance. Int. J. Anat. Res. 2016, 4, 2007–2014. [Google Scholar] [CrossRef]
  108. Cardosi, R.; Cox, C.; Hoffman, M. Postoperative neuropathies after major pelvic surgery. Obstet. Gynecol. 2002, 100, 240–244. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Article Metrics

Citations

Article Access Statistics

Journal Statistics
Multiple requests from the same IP address are counted as one view.
Systemic Mastocytosis Associated with “Smoldering” Multiple Myeloma
Previous
Altered Expression of Circadian Clock Genes in Patients with Atrial Fibrillation Is Associated with Atrial High-Rate Episodes and Left Atrial Remodeling
Next