Vol 83, No 3 (2024): Folia Morphologica
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The anatomy of the internal iliac artery: a meta-analysis

Mateusz Koziej12, Julia Toppich12, Jakub Wilk12, Dawid Plutecki3, Patryk Ostrowski12, Marta Fijałkowska4, Tomasz Bonczar12, Andrzej Dubrowski1, Małgorzata Mazur1, Jerzy Walocha12, Michał Bonczar12
Pubmed: 38512006
Folia Morphol 2024;83(3):517-530.

Abstract

Background: The internal iliac artery (IIA) originates from the common iliac artery
at the level of the sacroiliac joint and bifurcates between the L5 and S1 vertebrae.
The aim of the present meta-analysis was to demonstrate the most up-to-date
and evidence-based data regarding the general anatomy of the IIA, including
their variations, length, and diameter.
Materials and methods: Major online medical databases such as PubMed, Scopus,
Embase, Web of Science, Cochrane Library, and Google Scholar were searched
to find all studies considering the anatomy of the IIA. Eligibility assessment and
data extraction stages were performed.
Results: In the general population the pooled prevalence of Type I (The superior
gluteal artery arises independently with the inferior gluteal and internal pudendal
arteries arising from a common trunk which dividing inside [Type IA] or outside
[Type IB] pelvic cavity) was found to be 56.57% (95% CI: 53.00–60.10%). The
pooled mean length of the IIA was 39.95 mm (SE = 1.79) in the overall population.
The pooled mean diameter of the IIA was found to be 6.86 mm (SE = 0.27).
Conclusions: The IIA is responsible for supplying most of the structures located
in the pelvis. Hence, it is crucial to be aware of the possible variants of the said
vessel. The results presented in our study may be highly significant in various surgical
procedures performed in that region.

REVIEW ARTICLE

Folia Morphol.

Vol. 83, No. 3, pp. 517–530

DOI: 10.5603/fm.97800

Copyright © 2024 Via Medica

ISSN 0015–5659

eISSN 1644–3284

journals.viamedica.pl

The anatomy of the internal iliac artery: a meta-analysis

Mateusz Koziej12Julia Toppich12Jakub Wilk12Dawid Plutecki3Patryk Ostrowski12Marta Fijałkowska4Tomasz Bonczar12Andrzej Dubrowski1Małgorzata Mazur1Jerzy Walocha12Michał Bonczar12
1Department of Anatomy, Jagiellonian University Medical College Cracow, Kraków, Poland
2Youthoria, Youth Research Organization, Kraków, Poland
3Jan Kochanowski University of Kielce — Collegium Medicum, Kielce, Poland
4Department of Plastic, Reconstructive, and Aesthetic Surgery, Second Chair of Surgery Medical University of Lodz, Łódź, Poland

[Received: 20 September 2023; Accepted: 9 November 2023; Early publication date: 21 November 2023]

Address for correspondence: Michał Bonczar, Department of Anatomy, Jagiellonian University Medical College, ul. Mikołaja Kopernika 12, 33–332 Kraków, Poland; e-mail: michalbonczar01@gmail.com

This article is available in open access under Creative Common Attribution-Non-Commercial-No Derivatives 4.0 International (CC BY-NC-ND 4.0) license, allowing to download articles and share them with others as long as they credit the authors and the publisher, but without permission to change them in any way or use them commercially.

Background: The internal iliac artery (IIA) originates from the common iliac artery at the level of the sacroiliac joint and bifurcates between the L5 and S1 vertebrae. The aim of the present meta-analysis was to demonstrate the most up-to-date and evidence-based data regarding the general anatomy of the IIA, including their variations, length, and diameter.
Materials and methods: Major online medical databases such as PubMed, Scopus, Embase, Web of Science, Cochrane Library, and Google Scholar were searched to find all studies considering the anatomy of the IIA. Eligibility assessment and data extraction stages were performed.
Results: In the general population the pooled prevalence of Type I (The superior gluteal artery arises independently with the inferior gluteal and internal pudendal arteries arising from a common trunk which dividing inside [Type IA] or outside [Type IB] pelvic cavity) was found to be 56.57% (95% CI: 53.00–60.10%). The pooled mean length of the IIA was 39.95 mm (SE = 1.79) in the overall population. The pooled mean diameter of the IIA was found to be 6.86 mm (SE = 0.27).
Conclusions: The IIA is responsible for supplying most of the structures located in the pelvis. Hence, it is crucial to be aware of the possible variants of the said vessel. The results presented in our study may be highly significant in various surgical procedures performed in that region. (Folia Morphol 2024; 83, 3: 517–530)
Keywords: internal iliac artery, common iliac artery, abdominal aorta, pelvis, surgery, anatomy

INTRODUCTION

The internal iliac artery (IIA) originates from the common iliac artery at the level of the sacroiliac joint and bifurcates between the L5 and S1 vertebrae. The internal iliac vein and the lumbosacral trunk separate the said vessel from the sacroiliac joint. Subsequently, the IIA descends around the greater sciatic foramen and then divides into the anterior and posterior divisions. While descending, it accompanies the external iliac vein medially and the peritoneum laterally [37]. The anterior division later branches into superior and inferior vesical, middle rectal, vaginal, obturator, inferior gluteal, and internal pudendal arteries. The uterine and the vaginal arteries occur in women, and in men the inferior vesical artery replaces the vaginal artery, while the uterine artery is absent. The posterior division gives rise to the iliolumbar, lateral sacral, and superior gluteal arteries [37]. The IIA and its branches deliver blood to the pelvic viscera and muscles of the pelvis, the peritoneum, and the gluteal and medial thigh regions. Hence, the IIA is a major supplier of the pelvis.

The cardiovascular system begins to form in the foetus in the mid-third week [41]. The umbilical artery arises as a ventral branch of the dorsal aorta [52], and during prenatal development, the IIA derives from the umbilical artery, which is responsible for the blood and nutrient supply of the placenta. After childbirth, the umbilical cord is cut, and the distal parts of the umbilical artery occludes. Postnatally, the remaining part of the umbilical artery is the IIA [37, 48]. Additionally, the distal part of the umbilical artery obliterates into the medial umbilical ligament [49]. The process of forming the IIA and its branches varies significantly. As a result, the vascular pattern of the IIA differs in the population [33].

Over the years, researchers created numerous classification systems to distinguish variants of the IIA and its branches. In 1928, Adachi [1] formulated a classification system that became the most popular. This classification assumes that the umbilical artery is a continuation of the main stem of the IIA, while the superior gluteal, inferior gluteal, and internal pudendal arteries are the principal branches of the IIA. Thus, the variants of the ending of the IIA divide into 5 types and 8 groups.

The IIA is the major supplier of the pelvis, so the knowledge of its morphology is crucial from a clinical perspective. Understanding the anatomical implications of the IIA is necessary in the case of pelvic fracture treatment [25], various gynaecological procedures [60], and transplantation surgery [29]. Therefore, the main objective of the present meta-analysis was to summarise the extensive knowledge about the general anatomy of the IIA. In our article, we describe the branching variants of the IIA using the Adachi classification and the morphometric properties of the said vessel. It is hoped that our results may be a helpful tool for physicians, especially surgeons, performing procedures related to the IIA.

MATERIAL AND METHODS

Search strategy

Major online medical databases such as PubMed, Scopus, Embase, Web of Science, Cochrane Library, and Google Scholar were searched to find all studies considering the anatomy of the IIA. The systematic search was performed in 3 stages. In the first step, the following search terms were used in all databases: ((iliac artery) OR (common iliac artery) OR (external iliac artery) OR (internal iliac artery)) AND anatomy). Neither the date, language, type of article, nor text availability conditions were applied. (2) Furthermore, the mentioned databases were searched once again using another set of search phrases: (a) (internal iliac [Title/Abstract]) AND (anatomy [Title/Abstract]); (b) (internal iliac [Title/Abstract]) AND (variation [Title/Abstract]); (c) (internal iliac [Title/Abstract]) AND (morphology [Title/Abstract]); (d) (internal iliac [Title/Abstract]) AND (topography [Title/Abstract]); and (e) (internal iliac [Title/Abstract]) AND ((branch [Title/Abstract]) OR (branches [Title/Abstract])); (f) (internal iliac [Title/Abstract]) AND (type [Title/Abstract]). (3) Finally, a manual search was also performed throughout all references from the initially submitted studies. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were followed during the study. The search started in June 2023 and was completed in December 2023. It was ensured that each source was checked up to December 2023. To ensure the highest quality of findings the Critical Appraisal Tool for Anatomical Meta-Analyses (CATAM) and the Anatomical Quality Assessment (AQUA) tools were used to evaluate submitted articles [8, 16].

Eligibility assessment

Initially, a total of 4870 articles were evaluated by 2 independent reviewers (JWi and MM). Subsequently, 3181 papers were removed because they were duplicates or irrelevant. To minimise potential bias and maintain an accurate statistical methodology, articles such as case reports, case series, conference reports, reviews, letters to the editor, and studies that provided incomplete or irrelevant data were excluded. The inclusion criteria involved original studies with extractable numerical data on the anatomy, morphology, topography, and variations of the IIA. Finally, 40 studies met the inclusion criteria and were considered in the present meta-analysis [1–7, 9, 12–15, 19, 21, 22, 24, 26, 27, 30–35, 38–40, 42–47, 50, 54–59]. The flow chart that describes the study inclusion process is shown in Fig. 1.

Figure 1. Flow chart presenting the process of collecting the data included in this meta-analysis.
Characteristics of included studies

Thirty-three out of 40 studies were cadaveric dissections. The remaining 7 were radiological studies. Nineteen articles included fewer than 100 specimens, 9 articles included 101–200 specimens, 4 articles included 201–300 specimens, 3 articles included 301–400 specimens, and the remaining 5 articles included more than 400 specimens.

Most of the articles (25/40) included assessment of the IIA according to Adachi’s main classification system. The length of the IIA was studied in 9 articles. The diameter of the IIA was assessed in 6 of the included studies, whereas analysis of the location of bifurcation of the CIA into IIA and EIA was studied in 3 articles. Furthermore, the distance from the greater sciatic notch to the IIA was studied in 2 articles. The prevalence of the origin of the obturator artery from the posterior division of the IIA was assessed in 6 articles. Detailed characteristics of the submitted studies can be found in Table 1.

Table 1. Characteristics of studies included in this meta-analysis.

Abeysuriya, V. 2023

Continent, country

Asia, Sri Lanka

Methods

Cadaveric dissection

Participants

45 specimens

Outcomes

Adachi’s main classification system

Adachi 1928

Continent, country

Asia, Japan

Methods

Cadaveric dissection

Participants

121 specimens

Outcomes

Length, Adachi’s main classification system

Al-Talalwah 2014

Continent, country

Asia, Saudi Arabia

Methods

Cadaveric dissection

Participants

171 cadavers (79 females + 92 males); 342 specimens

Outcomes

Adachi’s main classification system

Notes

A modified classification system is proposed because 65 specimens of the type of internal iliac artery could not be classified

Arai 1936

Continent, country

Asia, Japan

Methods

Cadaveric dissection

Participants

500 specimens

Outcomes

Adachi’s main classification system

Ashley 1941

Continent, country

North America, USA

Methods

Cadaveric dissection

Participants

247 specimens

Outcomes

Adachi’s main classification system

Bilhim, T. 2010

Continent, country

Europe, Portugal

Methods

Radiological study — angio MR, angio CT, digital angiography

Participants

42 specimens (21 male patients) Age: 73.2 (range 58–83) years

Outcomes

Yamaki classification system

Bleich 2007

Continent, country

North America, USA

Methods

Cadaveric dissection

Participants

54 cadavers (54 females + 0 male); 108 specimens

Outcomes

Length

Boonruangsri 2015

Continent, country

Asia, Thailand

Methods

Cadaveric dissection

Participants

41 specimens

Outcomes

Length

Braithwaite 1952

Continent, country

Europe, United Kingdom

Methods

Cadaveric dissection

Participants

169 specimens

Outcomes

Adachi’s main classification system

Fatu 2006

Continent, country

Europe, Romania

Methods

Cadaveric dissection

Participants

50 cadavers (20 females + 30 males), 100 specimens

Outcomes

Length, diameter, Adachi’s main classification system

Notes

One of cases could not be included in

Adachi’s classification, 109 specimens in Adachi classification

Fisher 1959

Continent, country

Europe, Germany

Methods

Radiological study

Participants

50 specimens

Outcomes

Adachi’s main classification system

Francis 2018

Continent, country

Asia, India

Methods

Cadaveric dissection

Participants

80 cadavers, 160 specimens

Outcomes

Length

Gabryszuk, K. 2023

Continent, country

Europe, Poland

Methods

Computed tomography angiography analysis

Participants

145 arteries

Outcomes

IIA Diameter

Havaldar 2014

Continent, country

Asia, India

Methods

Cadaveric dissection

Participants

50 specimens

Outcomes

Origin of IIA from different levels, distance from greater sciatic notch

Hoshai 1938

Continent, country

Asia, Japan

Methods

Adachi’s main classification system

Participants

379 specimens

Outcomes

Adachi’s main classification system

Iwasaki 1987

Continent, country

Asia, Japan

Methods

Cadaveric dissection

Participants

251 specimens

Outcomes

Adachi’s main classification system

Jastschinski 1891

Continent, country

Europe, Germany

Methods

Cadaveric dissection

Participants

396 specimens

Outcomes

Adachi’s main classification system

Jusoh 2010

Continent, country

Asia, Malaysia

Methods

Cadaveric dissection

Participants

17 cadavers, 34 specimens

Outcomes

Prevalence of obturator artery deriving from posterior division of IIA

Katara, P. 2023

Continent, country

Asia, India

Methods

Cadaveric dissection

Participants

30 cadavers, 60 specimens

Outcomes

Mean length of the IIA

Khan 2021

Continent, country

Africa, South Africa

Methods

Cadaveric dissection

Participants

20 cadavers, 40 specimens

Outcomes

Prevalence of obturator artery deriving from posterior division of IIA

Li, L. 2019

Continent, country

Asia, China

Methods

Radiological study — computed tomography angiography, digital subtraction angiography

Participants

86 specimens (43 patients with pelvic tumours) Age: 52.7 (range 24–91) years

Outcomes

Yamaki classification system

Lipshutz 1916

Continent, country

North America, USA

Methods

Cadaveric dissection

Participants

181 specimens

Outcomes

Adachi’s main classification system

Lorbeer, R. 2018

Continent, country

Europe, Germany

Methods

Gadolinium-enhanced magnetic resonance angiography

Participants

756 male participants (median age = 52 years, range = 21–82 years)

Outcomes

Diameter of the IIA

Mamatha 2012

Continent, country

Asia, India

Methods

Cadaveric dissection

Participants

50 specimens

Outcomes

Distance from greater sciatic notch, Origin of the IIA from different levels, Prevalence of obturator artery deriving from posterior division of IIA

Miyaji 1935

Continent, country

Asia, Japan

Methods

Cadaveric dissection

Participants

179 specimens

Outcomes

Adachi’s main classification system

Morita, S. 1974

Continent, country

Asia, Japan

Methods

Cadaveric dissection

Participants

267 specimens

Outcomes

Adachi’s main classification system

Naveen, N. 2011

Continent, country

Asia, India

Methods

Cadaveric dissection

Participants

60 specimens

Outcomes

Adachi’s main classification system

Nguyen, B. 2022

Continent, country

Asia, Vietnam

Methods

Cadaveric dissection

Participants

18 cadavers, 36 specimens

Outcomes

Origin of the IIA from different levels, Mean diameter and length of the IIA

Ongidi, I. 2021

Continent, country

Africa, Kenya

Methods

Cadaveric dissection

Participants

57 specimens (48 males + 9 females)

Outcomes

Adachi’s main classification system, origin of the iia from different levels, location of the IIA in relation to the sacroiliac joint, mean diameter and length of the IIA

Pereira, J.A. 2013

Continent, country

Europe, Portugal

Methods

Radiological study — computerised tomography angiography and digital subtraction angiography

Participants

42 specimens (21 male patients with arteriogenic erectile dysfunction), age: 67.2 (range 57–78) years

Outcomes

Yamaki classification system

Pradhan, A. 2022

Continent, country

Asia, Nepal

Methods

Cadaveric dissection

Participants

15 cadavers, 30 specimens

Outcomes

Prevalence of obturator artery deriving from posterior division of IIA, mean diameter and length of the IIA, Adachi’s main classification system

Quain, J. 1908

Continent, Country

Europe, United Kingdom

Methods

Cadaveric dissection

Participants

297

Outcomes

Length

Ramakrishnan, P. K. 2012

Continent, country

Asia, India

Methods

Cadaveric dissection

Participants

50 specimens

Outcomes

Adachi’s main classification system

Roberts, W. 1967

Continent, country

North America, USA

Methods

Cadaveric dissection

Participants

167 specimens

Outcomes

Adachi’s main classification system, prevalence of obturator artery deriving from posterior division of IIA

Sakthivelavan, S. 2014

Continent, country

Asia, India

Methods

Cadaveric dissection

Participants

116 specimens (34R + 34L males, 24R + 24L females)

Outcomes

Adachi’s main classification system, prevalence of obturator artery deriving from posterior division of IIA

Suzuki, H. 1951

Continent, country

Asia, Japan

Methods

Cadaveric dissection

Participants

490 specimens

Outcomes

Adachi’s main classification system

Takenaka, Y. 2023

Continent, country

Asia, Japan

Methods

Radiological study — three-phase multidetector row computed tomography

Participants

60 specimens (30 patients with colorectal cancers) Age: 67 (range: 47–78) years

Outcomes

Adachi’s main classification system

Tsukamoto, N. 1929

Continent, country

Asia, Japan

Methods

Cadaveric dissection

Participants

287 specimens

Outcomes

Adachi’s main classification system

Yamaki, J. 1998

Continent, country

Asia, Japan

Methods

Cadaveric dissection

Participants

645 specimens

Outcomes

Adachi’s main classification system

Notes

A modified classification system is proposed — 5 types and 19 groups

Yasukawa, S. 1954

Continent, country

Asia, Japan

Methods

Cadaveric dissection

Participants

544 specimens

Outcomes

Adachi’s main classification system

Data extraction

Data from studies that met the inclusion criteria were extracted by 2 independent researchers (DP and JWi). Qualitative data, such as data collection methodology, year of publication, and country of origin, were assembled. Quantitative data about the IIA, such as prevalence of each anatomical variation, with respect to patients’ sex and origin, morphological data regarding length, diameter, and other extractable numerical data were gathered. Any discrepancies between the studies identified by the 2 reviewers were resolved by contacting the authors of the original studies wherever possible or by consensus with a third reviewer.

Statistical analysis

To perform the meta-analyses, STATISTICA version 13.1 software (StatSoft Inc., Tulsa, OK, USA), MetaXL version 5.3 software (EpiGear International Pty Ltd., Wilston, Queensland, Australia), and Comprehensive Meta-analysis version 4.0 software (Biostat, Inc., Englewood, NJ, USA) were used. A random effects model was used in all analyses. The chi-square test and the I-squared statistic were used to assess the heterogeneity among the studies [17, 18]. A p-value and confidence intervals were used to determine statistical significance between studies. A p-value lower than 0.05 was considered statistically significant. In the event of overlapping confidence intervals, differences were considered statistically insignificant. I-squared statistics were interpreted as follows: values of 0–40% were considered as “might not be important”, values of 30–60% were considered as “might indicate moderate heterogeneity”, values of 50–90% were considered as “may indicate substantial heterogeneity”, and values of 75–100% were considered as “may indicate substantial heterogeneity”.

RESULTS

The anatomical types of the IIA and their prevalence were evaluated according to the classification presented by Adachi et al. in 1928 (Fig. 2) [1]:

  1. Type I: The superior gluteal artery arises independently with the inferior gluteal and internal pudendal arteries arising from a common trunk, which divides inside (Type IA) or outside (Type IB) the pelvic cavity [1, 56].
  2. Type II: The superior and inferior gluteal arteries arise from a common trunk, which divides inside (Type IIA) or outside (Type IIB) the pelvic cavity, with the internal pudendal artery arising independently [1, 56].
  3. Type III: The superior and inferior gluteal and internal pudendal arteries all arise from the internal iliac artery independently [1, 56].
  4. Type IV: The superior and inferior gluteal and internal pudendal arteries arise from a common trunk [1, 56].
  5. Type V: The internal pudendal and superior gluteal arteries arise from a common trunk with the inferior gluteal having a separate origin [1, 56].
Figure 2. Scheme, presenting the types of the internal iliac artery (IIA) according to Adachi’s classification: Type I: The superior gluteal artery arises independently with the inferior gluteal and internal pudendal arteries arising from a common trunk, dividing inside (Type IA) or outside (Type IB) the pelvic cavity [1, 56]. Type II: The superior and inferior gluteal arteries arise from a common trunk, which divides inside (Type IIA) or outside (Type IIB) the pelvic cavity, with the internal pudendal artery arising independently [1, 56]. Type III: The superior and inferior gluteal and internal pudendal arteries all arise from the internal iliac artery independently [1, 56]. Type IV: The superior and inferior gluteal and internal pudendal arteries arise from a common trunk [1, 56]. Type V: The internal pudendal and superior gluteal arteries arise from a common trunk with the inferior gluteal having a separate origin [1, 56]. IIA — internal iliac artery; SA — superior gluteal artery; IGA — inferior gluteal artery; PA — internal pudendal artery; UA — umbilical artery.

In the general population the pooled prevalence of Type I was found to be 56.57% (95% CI: 53.00–60.10%). The pooled prevalence of Type II was established at 16.46% (95% CI: 14.03–19.05%). The pooled prevalence of Type III was found to be 20.28% (95% CI: 17.31–23.43%). The pooled prevalence of Type IV was found to be 4.84% (95% CI: 3.64–6.20%). The pooled prevalence of Type V was found to be 0.27% (95% CI: 0.05–0.62%). All the results mentioned above and more detailed ones can be found in Table 2.

Table 2. Statistical results of this meta-analysis regarding the pooled prevalence of each type of internal iliac artery (IIA) according to Adachi’s classification.

Category

Number of articles

Number of studied arteries

Pooled prevalence

LCI

HCI

Q

I2

Main types

Type I

22

5695

56.57%

53.00%

60.10%

141.87

85.20

Type II

16.46%

14.03%

19.05%

125.68

83.29

Type III

20.28%

17.31%

23.43%

160.63

86.93

Type IV

4.84%

3.64%

6.20%

96.48

78.23

Type V

0.27%

0.05%

0.62%

73.28

71.34

Furthermore, subgroup analyses were performed according to the patients’ sex and origin. The pooled prevalence of Type I in females was found to be 57.75% (95% CI: 42.17–72.61%), whereas in males it was established at 63.41% (95% CI: 57.39–69.23%). The pooled prevalence of Type II in females was found to be 17.69% (95% CI: 12.38–23.69%), whereas in males it was established at 12.84% (95% CI: 10.48–15.40%). Type V was found to occur statistically significantly (p = 0.0002) more often in females than in males. All the results mentioned above and more detailed ones regarding the pooled prevalence with respect to the patients’ sex can be found in Table 3. The pooled prevalence of Type I in the Asian population was found to be 58.44% (95% CI: 46.36–70.04%), whereas in the European population it was found to be 57.14% (95% CI: 51.29–62.98%). All the results mentioned above and more detailed ones regarding the pooled prevalence with respect to the patients’ origin can be found in Table 4.

Table 3. Statistical results of this meta-analysis regarding the pooled prevalence of each type of internal iliac artery (IIA) according to Adachi’s classification, with respect to patients’ sex.

Category

Sex

Number of articles

Number of studied arteries

Pooled prevalence

LCI

HCI

Q

I2

P-value

Type I

Females

5

386

57.75%

42.17%

72.61%

27.13

85.25

0.58

Males

709

63.41%

57.39%

69.23%

7.92

49.50

Type II

Females

386

17.69%

12.38%

23.69%

6.55

38.90

0.13

Males

709

12.84%

10.48%

15.40%

2.25

0.00

Type III

Females

386

17.50%

13.22%

22.24%

4.77

16.18

0.49

Males

709

20.51%

14.33%

27.47%

13.65

70.70

Type IV

Females

386

2.60%

0.06%

7.55%

13.67

70.73

0.95

Males

709

2.94%

1.48%

4.84%

5.44

26.45

Type V

Females

386

4.21%

0.00%

15.46%

57.41

93.03

0.0002

Males

709

0.14%

0.00%

0.49%

0.89

0.00

Table 4. Statistical results of this meta-analysis regarding the pooled prevalence of each type of internal iliac artery (IIA) according to Adachi’s classification, with respect to the geographical region.

Category

Number of articles

Number of studied arteries

Pooled prevalence

LCI

HCI

Q

I2

Asia

Type I

6

1561

58.44%

46.36%

70.04%

97.30

94.86

Type II

14.06%

9.23%

19.70%

36.39

86.26

Type III

22.62%

16.19%

29.77%

42.89

88.34

Type IV

3.62%

1.10%

7.35%

42.57

88.25

Type V

0.16%

0.01%

0.43%

3.94

0.00

Europe

Type I

2

278

57.14%

51.29%

62.89%

0.37

0.00

Type II

16.79%

12.62%

21.40%

1.23

0.00

Type III

15.94%

6.19%

28.76%

9.59

58.28

Type IV

2.61%

0.97%

4.95%

4.06

1.41

Type V

9.71%

0.00%

35.74%

41.39

90.34

The pooled mean length of the IIA was set to be 39.95 mm (SE = 1.79) in the overall population. In females, it was found to be 34.88 mm (SE = 5.08), whereas in males it was 45.43 mm (SE = 8.62). The pooled mean diameter of the IIA was found to be 6.86 mm (SE = 0.27). All the results mentioned above and more detailed ones regarding the IIA morphology can be found in Table 5.

Table 5. Statistical results of this meta-analysis regarding the morphometric parameters and location of the internal iliac artery (IIA).

Category

Mean

Standard error

Variance

Lower limit

Upper limit

Z-value

P-value

Length

Overall [mm]

39.95

1.79

3.21

36.14

43.16

22.12

0.00

Studies from Asia only [mm]

43.82

2.38

5.65

39.16

48.48

18.44

0.00

Females [mm]

34.88

5.08

25.83

24.92

44.84

6.86

0.00

Males [mm]

45.43

8.62

74.30

28.54

62.33

5.27

0.00

Right IIA [mm]

41.33

4.71

22.15

32.10

50.55

8.78

0.00

Left IIA [mm]

39.79

3.63

13.19

32.67

46.91

10.96

0.00

Diameter

Overall [mm]

7.43

0.19

0.03

7.06

7.80

39.72

0.00

Distance from the mid-sagittal line

Overall [mm]

32.25

0.25

0.06

31.76

32.74

128.99

0.00

Furthermore, an analysis of the anatomical types of the IIA according to the classification by Yamaki et al. (1998) [58] was performed: Group A: The internal iliac artery divides into 2 branches, the superior gluteal artery and the common trunk of the inferior gluteal and internal pudendal arteries. Group B: The internal iliac artery divides into 2 branches, the internal pudendal artery and the common trunk of the superior gluteal and inferior gluteal arteries. Group C: The internal iliac artery simultaneously divides into 3 major branches. Group D: The internal iliac artery divides into the common trunk for the superior gluteal and internal pudendal arteries and the inferior gluteal artery [58]. The pooled prevalence of Type A was found to be 71.16% (95% CI: 62.72–78.92%). Detailed results regarding this classification can be found in Table 6.

Table 6. Statistical results of this meta-analysis regarding the pooled prevalence of each type of internal iliac artery (IIA) according to Yamaki classification.

Category

Number of articles

Number of studied arteries

Pooled prevalence

LCI

HCI

Q

I2

Main types

Type A

4

901

71.16%

62.72%

78.92%

16.08

75.12

Type B

15.29%

9.79%

21.73%

13.66

70.72

Type C

12.60%

5.55%

21.80%

29.84

86.60

Type D

0.21%

0.00%

0.65%

0.26

0.00

DISCUSSION

In 1928 Adachi et al. [1] formulated a classification system concerning the branching pattern of the IIA. They stated that the superior gluteal, the inferior gluteal, and the internal pudendal arteries are the principal branches of the IIA [Fig. 3]. According to Adachi’s classification system, we distinguished 6 main types of the branching pattern of the IIA (Tab. 2). The classification system consisted of the following types: Type I — the superior gluteal artery originates from the main stem, while the inferior gluteal and internal pudendal arteries occur as a common trunk. If these arteries are located within the pelvis, this branching pattern is classified as Ia. However, in cases where the embranchment is present outside the pelvis, it is presented as Type Ib. Type II — the superior and inferior gluteal arteries arise together from the IIA, and the internal pudendal originates from the stem of the IIA as a second branch. Similarly to Type I, when the embranchment exists within the pelvis, it is classified as Type IIa, and when it occurs outside the pelvis, it is classified as Type IIb. Type III – the superior gluteal, inferior gluteal, and internal pudendal arteries arise independently from the IIA. When these vessels form a common trunk and the superior gluteal artery (IVa) or the internal pudendal artery (IVb) branches out first, this variant is classified as Type IV. Type V — the superior gluteal and the internal pudendal arteries arise as a common trunk, and the inferior gluteal as a separate branch [1].

Figure 3. Photo of a cadaveric dissection of internal iliac artery (IIA) and its close anatomical area. SP — sacral promontory; PTIIA — posterior trunk of internal iliac artery; ATIIA — anterior trunk of internal iliac artery.

The results presented in our meta-analysis demonstrate that Type I is the most common branching pattern (56.57%) in the general population. Type III is the second most observed branching type (20.28%), while Type II is the third (16.46%). Types IV and V were found to be relatively rare (less than 5%). These results do not differ much from the observations of other researchers. Yamaki et al. [58] examined 645 pelvic halves to determine which branching pattern of the IIA is the most common. They noted that 58% of patients had the Type I branching pattern. Similarly, Sakthivelavan et al. [50] dissected 116 Indian specimens to analyse the variability of the IIA branching. They demonstrated similar conclusions: Type I was observed in 63.2% of cases. Both teams of researchers proved that the second most commonly observed is Type III: 22.8% and 21%, respectively.

However, original research done by Adachi et al. [1] revealed that the second most common branching pattern corresponds with Type II. Roberts et al. [47] examined 167 Caucasian specimens to compare Adachi’s results (Japanese population) with the ones analysed in their own study. Their conclusions were similar to those of Adachi: Type II was found in 26.8%, while Type III occurred in 14.4% of patients. Furthermore, Type V is rare in the general population — Yamaki et al. [58] observed it in only one out of 645 specimens (0.2%). Our studies revealed that the pool prevalence of type V amounts to 0.27%. Many researchers did not find this type of branching in their studies [42, 47, 50]. However, when Type V was found, it occurred only in single cases. Yevstifeieva et al. [60] reviewed the literature to determine the prevalence of the branching patterns of the IIA. They found that the fifth type of branching is present in 0.5% of cases. Similarly, Yamaki et al. [58] found it only in 0.2% of cases.

The pooled prevalence of each type of the IIA concerning the patient’s sex were also analysed. Type I was the most common in both sexes. However, it was found in 63.41% of men, while in the case of women, it was present only in 57.75% of cases. The second most common branching was Type III, present in 20.51% of men. In women, the prevalence of Type II was higher (17.69%) than that of Type III (17.50%). Type V was absent in men, but in women, it occurred in 4.21% of cases. Braithwaite et al. [7] proved that Type II is present in 10.1% of men and 24.5% of women. This conclusion corresponds with our findings.

Most research concerning the Adachi classification of the IIA originated from Asia. The most common branching pattern was found to be Type I in both Asian and European populations (58.44% and 57.14%, respectively). However, Type III is the second most frequent type in the Asian population (24.58%), but in the case of the European population, it is replaced by Type II (16.79%). Furthermore, the Type V is rare in Asians (0.16%), while 9.71% of European patients presented this type of branching. Adachi examined Japanese patients [1] and revealed that Type I was present in 51.2% of cases. Furthermore, Fatu et al. [12] examined Romanian individuals and found that in 60% of patients, the branching pattern is Type I. Moreover, the Polish population was analysed by Kosinski et al. [28]. In that study, Type I occurred in 79% of patients. These results demonstrate a different distribution of branching patterns in the discussed groups. However, regardless of the geographical region, Type I is the most common branching pattern.

Although the Adachi classification has become the primary system for distinguishing branching types of the IIA, it is burdened with limitations. This classification correlates with embryological processes. Thus, some researchers state that it is not clinically useful. Hence, various improvements have been implemented. Yamaki et al. [58] excluded the umbilical artery from their classification because it is not clinically significant after birth. Ashley and Anson [3] proposed a new approach: the obturator artery constitutes the base for further divisions. However, this classification was compatible with the Adachi classification in 95% of cases. Al Talalwah et al. [56] accentuated the need to include the coexistence of the sciatic artery in the overall classification. He noted that type IIA, according to Adachi’s classification, may be misinterpreted by radiologists, resulting in surgical complications.

The IIA is one of the terminal branches of the common iliac artery. It originates anteromedially from the sacroiliac joint. According to Ongidi et al. [42], the origin lies medially from the sacroiliac joint. However, Mohammadbaigi et al. [36] noted that the origin is located anteriorly to it. Generally, the common iliac artery gives rise to the IIA at the level of the L5/S1 intervertebral disc [10]. This has been confirmed in several articles in the past [33, 42]. However, according to Naveen et al. [39], the origin of the IIA is located at the level of the S1 vertebra (58.3% of cases). Moreover, our study revealed that the distance of the IIA from the midsagittal plane amounts to 32.25 mm. Other researchers came up with similar results. Ongidi et al. [42] noted that the mean distance was 31.47 mm. Furthermore, Fatu et al. [12] measured the distance between the IIA and the midsagittal plane on the right and left side (right: 29–36 mm, left: 40–50 mm). In our article, we summarised the information about the IIA origin to create a helpful tool in preoperative planning. Pelvic surgery may be burdened with potential threats, such as acute haemorrhage. Thus, radiologists and surgeons should be aware of different variants of the anatomy of the IIA. A well-planned surgical procedure may prevent injury to major pelvic vessels, including the common iliac artery.

The results in the present meta-analysis demonstrate that the mean length of the IIA was 39.95 mm. The right IIA was found to be longer (41.33 mm) than the left (39.79 mm). Furthermore, men were found to have significantly longer IIA (45.43 mm) than women (34.88 mm). The measurements by other researchers revealed that the mean length of the IIA is 37.00 mm [42, 50]. The difference in the length of the IIA between our and previous studies is minor and may result from the larger sample in our study compared to others. According to Francis et al. [34], the overall length of the right IIA equals 39.43 mm, and the left: is 36.10 mm. Furthermore, our research revealed that the overall diameter of the IIA is 6.86 mm. Fatu et al. [12] presented similar results: the diameter of the IIA was stated to be 6.83 mm.

The origin and length of the IIA can determine the possible outcome of endovascular procedures. These aspects of the said vessel should be included in the preoperative planning of pelvic surgery, which could be accompanied by potential complications, such as severe bleeding. Performing a selective anterior division ligation or embolisation of the IIA branches requires a thoughtful operation and should be well-planned [5, 51]. The IIA and its branches are a major supplier of the pelvis. Thus, it plays a significant role in various areas of medicine. Kachlik et al. [25] analysed possible fractures of the pelvis with vascular damage. In the study, they distinguished different types of pelvic injuries — 3 of them referred to the IIA. The most probable cause of the injury was dislocation. Dzupa [11], Zhang [61], and Hussami [20] presented similar conclusions. Because the IIA plays a significant role in the blood supply of the pelvis, it is crucial to be aware of the possible damage that may result from the injury of the pelvis. Additionally, the ligation of the said artery is used in case of pelvic fracture [23]. Hence, the surgeons must be aware of the possible variations in the anatomy of the IIA to avoid intra- and postoperative complications. The anatomy of the IIA is also highly significant for gynaecologists and obstetricians. Yevstifeieva et al. [60] proved that the IIA has great clinical value in gynaecological surgery. Surgeons ligate the IIA in cases of bleeding resulting from a hysterectomy, known as the Wertheim operation [25, 53]. The ligation procedure serves in the prevention and treatment of postpartum haemorrhage [25]. According to the data published by the World Health Organisation, postpartum haemorrhage causes 35% of maternal deaths. Hence, having adequate knowledge of the morphological properties of the internal iliac arteries is crucial to provide safer and more effective surgical treatments. A recent study showed that the IIA plays a significant role in the transplantation of the uterus because it is required to form anastomoses and supply the organ with blood [29].

The presented meta-analysis includes extensive knowledge about the internal iliac arteries and their principal branches. However, this study is not without limitations. Since meta-analyses refer to research by other authors, they are burdened with potential bias. Our study is no exception. Furthermore, most of the studies we refer to are from Asia. Hence, our result may reflect mostly the Asian rather than the global population. Nevertheless, we hope this research will be an effective and helpful tool for surgeons and clinicians. We believe that knowledge of the anatomy and variants of the IIA will contribute to safer and more accurate treatment.

CONCLUSIONS

Our study describes the prevalence of the IIA branching patterns according to the Adachi classification. Type I was the most common in the general population. There is no difference regarding the patient’s sex and ethnicity. Furthermore, the length of the IIA was found to be 39.95 mm, and the arterial diameter was 6.86 mm. The IIA is responsible for supplying most of the structures located in the pelvis. Hence, it is crucial to be aware of the possible variants of the vessel. The results presented in our study may be highly significant in various surgical procedures performed in that region.

ARTICLE INFORMATION AND DECLARATIONS

Author contributions

Mateusz Koziej — writing, statistical analysis.

Julia Toppich — writing, literature.

Jakub Wilk — literature search, data extraction.

Dawid Plutecki — literature search, data extraction.

Patryk Ostrowski — writing, literature, tables, figures.

Marta Fijałkowska — writing.

Tomasz Bonczar — writing, statistical analysis.

Andrzej Dubrowski — figures, writing.

Małgorzata Mazur — writing.

Jerzy Walocha — writing, figures.

Michał Bonczar — writing, statistical analysis, figures, tables.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Conflict of interest

The authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

REFERENCES

  1. Adachi B. Das Arteriensystem der Japaner. Kenkyusha Press, Tokyo 1928.
  2. Arai S. The distribution pattern of the hypogastric artery in Japanese. Acta Anat Nippon. 1936; 9: 81–88.
  3. Ashley FL, Anson B. The hypogastric artery in American Whites and Negroes. Am J Phys Anthropol. 2005; 28(4): 381–395, doi: 10.1002/ajpa.1330280404.
  4. Bilhim T, Casal D, Furtado A, et al. Branching patterns of the male internal iliac artery: imaging findings. Surg Radiol Anat. 2011; 33(2): 151–159, doi: 10.1007/s00276-010-0716-3, indexed in Pubmed: 20798937.
  5. Bleich AT, Rahn DD, Wieslander CK, et al. Posterior division of the internal iliac artery: anatomic variations and clinical applications. Am J Obstet Gynecol. 2007; 197(6): 658.e1–658.e5, doi: 10.1016/j.ajog.2007.08.063, indexed in Pubmed: 18060970.
  6. Boonruangsri P, Suwannarong B, Chaisiwamongkol K, et al. Morphometric analysis of the iliac arterial lengths in normal and abnormal aortoiliac arteries (tortuosity, kinking and aneurysm) conditions. Srinagarind Medical Journal. 2015; 30(4): 352–357.
  7. Braiwaite JL. Variations in origin of the parietal branches of the internal iliac artery. J Anat. 1952; 86(4): 423–430, indexed in Pubmed: 12999644.
  8. D’Antoni AV, Tubbs RS, Patti AC, et al. The critical appraisal tool for anatomical meta-analysis: a framework for critically appraising anatomical meta-analyses. Clin Anat. 2022; 35(3): 323–331, doi: 10.1002/ca.23833, indexed in Pubmed: 35015336.
  9. Dodampahala SH, Chandrasena L, Abeysuriya V. Usefulness of knowledge in anatomy of the internal iliac artery in its ligation during life-threatening pelvic haemorrhages. Sri Lanka J Obstet Gyn. 2023; 45(2): 84–88, doi: 10.4038/sljog.v45i2.8079.
  10. Drake L, Vogl W, Mitchell AWM. Gray’s Anatomy for Students. Elsevier/Churchill Livingstone, Philadelphia 2005.
  11. Dzupa V, Chmelová J, Pavelka T, et al. Multicentric study of patients with pelvic injury: basic analysis of the study group. Acta Chir Orthop Traumatol Cech. 2009; 76(5): 404–409, indexed in Pubmed: 19912705.
  12. Fătu C, Puişoru M, Fătu IC. Morphometry of the internal iliac artery in different ethnic groups. Ann Anat. 2006; 188(6): 541–546, doi: 10.1016/j.aanat.2006.05.016, indexed in Pubmed: 17140147.
  13. Fisher W. Anatomisch-rontgenologische Untersuchungen uber die Verteilung and Anastomosenbildung der viszeralen and parietalen weiblichen Beckenarterien. Geburtsh Gynaek. 1959; 154: 321–340.
  14. Gabryszuk K, Gliwa J, Dziedzic M, et al. The superior gluteal artery and the posterior division of the internal iliac artery: an analysis of their complete anatomy. Folia Morphol. 2023 [Epub ahead of print], doi: 10.5603/fm.96695, indexed in Pubmed: 37957934.
  15. Havaldar P, Taz S, Angadi A, et al. Study of posterior division of internal iliac artery. IJAR. 2014; 2(2): 375–379.
  16. Henry BM, Tomaszewski KA, Ramakrishnan PK, et al. Development of the anatomical quality assessment (AQUA) tool for the quality assessment of anatomical studies included in meta-analyses and systematic reviews. Clin Anat. 2017; 30(1): 6–13, doi: 10.1002/ca.22799, indexed in Pubmed: 27718281.
  17. Henry BM, Tomaszewski KA, Walocha JA. Methods of Evidence-Based Anatomy: a guide to conducting systematic reviews and meta-analysis of anatomical studies. Ann Anat. 2016; 205: 16–21, doi: 10.1016/j.aanat.2015.12.002, indexed in Pubmed: 26844627.
  18. Higgins JPT, Thomas J, Chandler J. Cochrane handbook for systematic reviews of interventions. John Wiley & sons, Hoboken 2019.
  19. Hoshiai H. Anatomical study on the pelvic arteries in Japanese fetus. Acta Mat Nippon. 1938; 11: 61–72.
  20. Hussami M, Grabherr S, Meuli RA, et al. Severe pelvic injury: vascular lesions detected by ante- and post-mortem contrast medium-enhanced CT and associations with pelvic fractures. Int J Legal Med. 2017; 131(3): 731–738, doi: 10.1007/s00414-016-1503-4, indexed in Pubmed: 27891547.
  21. Iwasaki Y, Shoumura S, Ishizaki N, et al. The anatomical study on the branches of the internal iliac artery — comparison of the findings with Adachi’s classification. Kaibogaku Zasshi. 1987; 62(6): 640–645.
  22. Jastchinski S. Die tyischen verzweigsform der arteria hypogastrica. Internationale Monatsschrift für Anatomie und Physiologie. 1891; 8: 111–127.
  23. Joshi VM, Otiv SR, Majumder R, et al. Internal iliac artery ligation for arresting postpartum haemorrhage. BJOG. 2007; 114(3): 356–361, doi: 10.1111/j.1471-0528.2006.01235.x, indexed in Pubmed: 17261120.
  24. Jusoh AR, Abd Rahman N, Abd Latiff A, et al. The anomalous origin and branches of the obturator artery with its clinical implications. Rom J Morphol Embryol. 2010; 51(1): 163–166, indexed in Pubmed: 20191138.
  25. Kachlik D, Vobornik T, Dzupa V, et al. Where and what arteries are most likely injured with pelvic fractures? Clin Anat. 2019; 32(5): 682–688, doi: 10.1002/ca.23372.
  26. Katara P, Sharma RK, Bansal NA. Morphometric study of common iliac artery, internal iliac artery and external iliac artery at SMS medical college, Jaipur. Int J Life Sci Biotechnol Pharma Res. 2023; 12(4): 667–670.
  27. Khan R, Naidoo N, Lazarus L. Unique vascular patterns of the internal iliac artery and its clinical import in pelvic surgery. Transl Res Anat. 2021; 25: 100151, doi: 10.1016/j.tria.2021.100151.
  28. Kosinski C. Quelques notions sur la ramification des artères iliaques. CR Ass Anat. 1929; 1: 46–48.
  29. Kristek J, Johannesson L, Novotny R, et al. Human uterine vasculature with respect to uterus transplantation: A comprehensive review. J Obstet Gynaecol Res. 2020; 46(11): 2199–2220, doi: 10.1111/jog.14428, indexed in Pubmed: 32840043.
  30. Li L, Wu K, Liu Y, et al. Angiographic evaluation of the internal iliac artery branch in pelvic tumour patients: diagnostic performance of multislice computed tomography angiography. Oncol Lett. 2019; 17(5): 4305–4312, doi: 10.3892/ol.2019.10084, indexed in Pubmed: 30944625.
  31. Lipshutz B. A composite study of the hypogastric artery and its branches. Ann Surg. 1918; 67(5): 584–608, doi: 10.1097/00000658-191805000-00012, indexed in Pubmed: 17863918.
  32. Lorbeer R, Grotz A, Dörr M, et al. Reference values of vessel diameters, stenosis prevalence, and arterial variations of the lower limb arteries in a male population sample using contrast-enhanced MR angiography. PLoS One. 2018; 13(6): e0197559, doi: 10.1371/journal.pone.0197559, indexed in Pubmed: 29924802.
  33. Mamatha H, Hemalatha B, Vinodini P, et al. Anatomical study on the variations in the branching pattern of internal iliac artery. Indian J Surg. 2015; 77(Suppl 2): 248–252, doi: 10.1007/s12262-012-0785-0, indexed in Pubmed: 26730003.
  34. Francis YM, Balaji T, Rajendran H, et al. Study on variations in the origin and branching pattern of internal iliac artery in cadavers. Biomed Pharmacol J. 2018; 11(4): 2201–2207, doi: 10.13005/bpj/1602.
  35. Miyaji K, Miyaji K. Sie AU hypogastrica. Arbeit Mat Institut Kanazawa. 1935; 20: 85–93.
  36. Mohammadbaigi H, Darvishi M, Moayeri A. Variations of anterior and posterior division of internal iliac artery: a systematic review and clinical implications. Biomed Res Ther. 2019; 6(5): 3189–3206, doi: 10.15419/bmrat.v6i5.546.
  37. Moore KL, Dalley AF, Agur A. Clinically oriented anatomy (8th ed). Lippincott Williams and Wilkins, Philadelphia 2017.
  38. Morita K, Kono M. Changes in the nitrogen localized in the lamellae systems and stroma of rice chloroplast accompanying the stages of growth. Soil Sci Plant Nutr. 1974; 20(1): 79–86, doi: 10.1080/00380768.1974.10433230.
  39. Naveen N, Murlimanju B, Kumar V, et al. Morphological analysis of the human internal iliac artery in South Indian population. Online J Health Allied Sci. 2011; 10(1): 1–4.
  40. Vo T, Nguyen T, Pham H, et al. Insight into Vietnamese women’s internal iliac artery anatomy. Eur J Anat. 2022; 26(6): 721–729, doi: 10.52083/flot6898.
  41. Noden DM, Reiss KZ, Noden DM, et al. Embryonic origins and assembly of blood vessels. Am Rev Respir Dis. 1989; 140(4): 1097–1103, doi: 10.1164/ajrccm/140.4.1097, indexed in Pubmed: 2478056.
  42. Ongidi I, Amuti TM, Abdulsalaam FY, et al. Variability in morphology and branching of the internal iliac artery: Implications for pelvic surgery. Transl Res Anat. 2021; 22: 100097, doi: 10.1016/j.tria.2020.100097.
  43. Pereira JA, Bilhim T, Rio Tinto H, et al. Radiologic anatomy of arteriogenic erectile dysfunction: a systematized approach. Acta Med Port. 2013; 26(3): 219–225, indexed in Pubmed: 23815835.
  44. PK R, CD S, MA E. A descriptive anatomical study of the branching pattern of internal iliac artery in humans. Natl. J Clin Anat. 2020; 01(01): 7–13, doi: 10.1055/s-0039-3401659.
  45. Pradhan A, Pradhan M, Kharbuja R, et al. Variations in origin and branching pattern of anterior division of internal iliac artery: a cadaveric study. J Coll Med Sci Nepal. 2022; 18(2): 153–161, doi: 10.3126/jcmsn.v18i2.44309.
  46. Quain J. Quain, J., 1908. In: W. Sharpey (Ed.), Quain’s Elements of Anatomy, 7th ed., vol. I. London 1908.
  47. Roberts WH, Krishingner GL. Comparative study of human internal iliac artery based on Adachi classification. Anat Rec. 1967; 158(2): 191–196, doi: 10.1002/ar.1091580208, indexed in Pubmed: 6034641.
  48. Sadler TW. Langman’s Medical Embryology, 6th ed. Williams & Wilkins Co, London 1990.
  49. Sadler TW, Langman J. Langman’s Medical Embryology, 12th ed. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia 2012.
  50. Sakthivelavan S, Aristotle S, Sivanandan A, et al. Variability in the branching pattern of the internal iliac artery in Indian population and its clinical importance. Anat Res Int. 2014; 2014: 597103, doi: 10.1155/2014/597103, indexed in Pubmed: 25580296.
  51. Selçuk İ, Uzuner B, Boduç E, et al. Step-by-step ligation of the internal iliac artery. J Turk Ger Gynecol Assoc. 2019; 20(2): 123–128, doi: 10.4274/jtgga.galenos.2018.2018.0124, indexed in Pubmed: 30499283.
  52. Senior HD. The development of the arteries of the human lower extremity. Am J Anat. 2005; 25(1): 54–95, doi: 10.1002/aja.1000250105.
  53. Sirca A. The arterial supply of the pelvic ureter in the female. Acta Anat. 1958; 33: 252.
  54. Suzuki H. The mode of branching of the internal iliac artery in Japanese. Jikeikai Ikadaigaku kaibougaku Kyoshitsu Gyosekishu. 1951; 5: 1–49.
  55. Takenaka Y, Beppu N, Otani M, et al. Anatomical validation of internal iliac vessels assessed by three-dimensional angiographic analysis. J Anus Rectum Colon. 2023; 7(3): 186–196, doi: 10.23922/jarc.2022-066, indexed in Pubmed: 37496569.
  56. Talalwah WAl. Internal Iliac Artery Classification and Its Clinical Significanc. Rev Arg de Anat Clin. 2014; 6(2): 63–71, doi: 10.31051/1852.8023.v6.n2.14126.
  57. Tsukamoto N. Studies on the arterial system in pelvic cavity of Japanese. Acta Mat Nippon. 1929; 2: 830–852.
  58. Yamaki K, Saga T, Doi Y, et al. A statistical study of the branching of the human internal iliac artery. Kurume Med J. 1998; 45(4): 333–340, doi: 10.2739/kurumemedj.45.333, indexed in Pubmed: 9914720.
  59. Yasukawa S. An Anatomical study on the hypogastric artery in Japanese. Jikeikai Ikadaigaku kaibougaku Kyoshitsu Gyosekishu. 1954; 12: 1–43.
  60. Yevstifeieva A, Krzeszowiak J, Lastovetskyi I, et al. Variations in branching patterns of internal iliac artery according to Adachi’s classification — literature review and presentation of a case. Transl Res Anat. 2021; 24: 100119, doi: 10.1016/j.tria.2021.100119.
  61. Zhang Qi, Chen W, Smith WR, et al. Superior gluteal artery injury presenting as delayed onset shock. Arch Orthop Trauma Surg. 2010; 130(2): 251–256, doi: 10.1007/s00402-009-0916-7, indexed in Pubmed: 19533156.