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Posterior division of the internal iliac artery: Anatomic variations and clinical applications
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Posterior division of the internal iliac artery: Anatomic variations and clinical applications April T. Bleich, MD; David D. Rahn, MD; Cecilia K. Wieslander, MD; Clifford Y. Wai, MD; Shayzreen M. Roshanravan, MD; Marlene M. Corton, MD OBJECTIVE: The objective of the study was to characterize the anatomy of the internal iliac artery (IIA) and its posterior division branches and to correlate these findings to IIA ligation. STUDY DESIGN: Dissections were performed in 54 female cadavers. RESULTS: Average length of IIA was 27.0 (range, 0-52) mm. Posterior
division arteries arose from a common trunk in 62.3% (66 of 106) of pelvic halves. In the remaining specimens, branches arose independently from the IIA, with the iliolumbar noted as the first branch in 28.3%, lateral sacral in 5.7%, and superior gluteal in 3.8%. The average width of the first branch was 5.0 (range, 2-12) mm. In all dissec-
tions, posterior division branches arose from the dorsal and lateral aspect of IIA. The internal iliac vein was lateral to the artery in 70.6% (12 of 17) of specimens on the left and 93.3% (14 of 15) on the right. CONCLUSION: Ligation of the IIA 5 cm distal from the common iliac bifurcation would spare posterior division branches in the vast majority of cases. Understanding IIA anatomy is essential to minimize intraoperative blood loss and other complications.
Key words: hypogastric artery ligation, internal iliac artery, pelvic hemorrhage, vascular anatomy
Cite this article as: 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;197:658.e1-658.e5.
H
emorrhage is the second leading cause of obstetrical mortality in the United States and the number one cause of maternal death in developing nations.1,2 It also represents a major source of morbidity in gynecologic surgery. Kelly3 was the first to describe ligation of the internal iliac artery (IIA) as a method to control hemorrhage during pelvic surgery in 1894. For many years, it was assumed that this procedure worked by ceasing blood flow to the pelvis. However, in 1968, Burchell4 shed light onto the mechanism of IIA ligation. By performing aortograms as early as 5 minutes after IIA ligation, he showed that flow
From the Division of Urogynecology and Reconstructive Surgery, Department of Obstetrics and Gynecology, University of Texas Southwestern Medical Center, Dallas, TX. Presented at the 33rd Annual Scientific Meeting of the Society of Gynecologic Surgeons, Orlando, FL, April 12-14, 2007. Received Jan. 17, 2007; revised May 17, 2007; accepted Aug. 22, 2007. Reprints not available from the authors. 0002-9378/$32.00 © 2007 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2007.08.063
658.e1
did not cease distal to the site of ligation, but rather the direction of flow was reversed using collateral pathways through the lumbar-iliolumbar, middle sacrallateral sacral, and superior and middle hemorrhoidal arteries (Figure 1). Importantly, he demonstrated that bilateral ligation decreased the pulse pressure (pulsation) in the distal artery by as much as 85%, whereas blood flow was reduced by at most 50%. He stated that reduction in pulse pressure created a “venous-like system,” which allowed blood clots to form at the sites of bleeding and that this was the factor responsible for hemostasis. The use of IIA ligation in current obstetrics and gynecology is controversial. The efficacy of this procedure in controlling obstetrical hemorrhage has been reported to range from 4275%.5-8 Similarly, studies reviewing prophylactic IIA ligation at the time of radical hysterectomy have yielded conflicting results.9,10 The 2006 American College of Obstetricians and Gynecologists Practice Bulletin regarding postpartum hemorrhage states: “Hypogastric artery ligation is performed much less frequently than in years past. Practitioners are less familiar with this technique,
American Journal of Obstetrics & Gynecology DECEMBER 2007
and the procedure has been found to be considerably less successful than previously thought.”11 Selective ligation of the uterine artery, as described by O’Leary,12 has been shown to be successful and relatively easy to perform, with few reported complications. Thus, this procedure has become one of the first surgical methods used in controlling postcesarean pelvic hemorrhage, especially when the bleeding is known to be of uterine origin. Ligation of the ovarian arteries has also been described.13 IIA ligation is still warranted in select cases, when more conservative surgical methods to control hemorrhage, including bilateral uterine and even ovarian artery ligation, have failed, especially if preservation of fertility is strongly desired in a stable patient. IIA ligation may also play a role in the setting of persistent bleeding following hysterectomy. Although embolization of the uterine vessels by interventional radiology has been shown to have higher success rates than those reported for IIA ligation,14,15 this procedure requires a stable patient and available personnel and resources. Therefore, IIA ligation may be the only alternative, and a life-saving ap-
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FIGURE 1
Pelvic arterial anatomy
Collateral circulation after internal IIA ligation as demonstrated by Burchell. Collateral pathways include: lumbar-iliolumbar, middle sacral-lateral sacral, and superior-middle rectal (hemorrhoidal) arteries. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
proach, in the setting of severe gynecologic or obstetric pelvic hemorrhage. Despite the enormous reserve in blood supply of the pelvis, acute interruption of the IIA has been associated with buttock claudication and necrosis.16-18 Accordingly, current obstetrics and gynecology textbooks advocate ligation of the IIA distal to the posterior division branches in order to preserve collateral circulation.19,20 Because this procedure is often performed emergently and after other measures to control bleeding have failed, understanding the IIA anatomy and approximate location and anatomic relationships of the posterior division branches should reduce the risk of further intraoperative bleeding and other serious complications. Yet most studies reviewing the IIA anatomy have been performed primarily on male cadavers and have focused on branching patterns of the parietal arteries rather than the length of the IIA before its division.21-23 Thus, the objectives of this study were to examine the IIA anatomy, anatomic location, and relationships of its posterior division branches and to correlate these findings to IIA ligation.
M ATERIALS AND M ETHODS The common and internal iliac arteries were dissected out bilaterally in 37 unembalmed and 17 embalmed female cadavers. The cadavers were obtained from
the Willed Body Program at the University of Texas at Southwestern Medical Center in Dallas. This study was considered exempt by the University of Texas Southwestern Medical Center Institutional Review Board in accordance with the Code of Federal Regulations, Title 45. Age, height, and weight at the time of death, as well as cause of death, were available for the majority of donors. None of the cadavers had evidence of prior vascular surgery involving the pelvis. The abdominal cavity was opened, the rectosigmoid was tied, and the bowel proximal to this level was removed. The retroperitoneal space was entered at the level of the aortic bifurcation and the common iliacs were dissected and followed to their point of division into external and internal iliac arteries (Figure 1). The fat and loose connective tissue surrounding the internal iliac artery and vein was removed and the posterior division branches were identified. The course of each posterior division branch was traced. The iliolumbar was followed superiorly toward the false pelvis in which branches were noted to supply the iliacus, psoas major, and quadratus lumborum muscles. The superior gluteal was followed until it exited the pelvis between the lumbosacral nerves. The lateral sacrals were followed medially towards the anterior sacral foramina. The relationship between the IIA and the internal iliac vein and venous plexus was noted. The lengths of the common and internal iliac arteries were recorded. The IIA was measured from the point of bifurcation of the common iliac to the origin of the first posterior division branch (Figure 2). Branching patterns of the three posterior division branches, iliolumbar, lateral sacral, and superior gluteal were documented. The craniocaudal width of the first posterior division branch was also noted (Figure 2). The length of the IIA and the craniocaudal width of the posterior division branches were added to calculate the average length from the common iliac artery bifurcation at which posterior division branches would be spared; this was called the combined length (Figure 2). Two SDs were added
FIGURE 2
Internal iliac artery
A, Internal iliac artery length. B, Craniocaudal width of posterior division branch. C, Combined length. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
to the mean combined length to estimate the distance from the common iliac artery bifurcation in which posterior division branches would be spared in 95% of cases. Measurements were taken twice using calipers and a 10-cm plastic ruler with the pelvis in the supine position. Statistical analysis was performed using SigmaStat 2.03 statistical software (Systate Software, Inc, Inc, San Jose, CA). Continuous variables were summarized by means, medians, standard deviations (SDs), and ranges. Qualitative data were summarized by counts and percentages. P ⬍ .05 was considered statistically significant.
R ESULTS Study population characteristics Limited demographic data were available on all cadavers examined (Table 1). Mean age at time of death was 79.6 years (range, 45-103 yrs). Average body mass index was 23.3 kg/m2. Fifty-three cadavers were white and 1 was African American.
Common iliac artery The mean length of the common iliac artery was 57.0 (range, 30-94) mm on the left and 55.2 (range, 25-91) mm on the right. These values represent the average lengths in the 37 unembalmed specimens only because the majority of the common iliac vessels were severed dur-
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SGS Meeting Papers TABLE 1
Demographics of study population Demographic characteristic
Value
Total number cadavers, n
54
Age, mean ⫾ SD (y)
79.6 ⫾ 12.7
........................................................................................................... ...........................................................................................................
Race, n (%)
..................................................................................................
White
53 (98)
..................................................................................................
African American
1 (2)
...........................................................................................................
23.3 ⫾ 4.8
Body mass index, mean ⫾ SD (kg/m2)
...........................................................................................................
Reported cause of death, n (%)
..................................................................................................
Cardiopulmonary
23 (42.6)
Cancer
18 (33.3)
Neurologic
10 (18.5)
www.AJOG.org 54) on the right (Figure 3). In the remaining specimens, posterior division branches arose independently from the internal iliac, with the IL noted as the first branch in 28.3%, the LS in 5.7%, and the SG in 3.8% (Table 3 and Figure 4). In all cadavers, posterior division branches originated from the dorsal and lateral aspect of the artery. The SG coursed laterally and inferiorly through numerous internal iliac venous branches before exiting the pelvis through the greater sciatic foramen. The average width of the first branch of the posterior division was 4.6 (range, 2-9) mm on the left and 5.3 (range, 2-12) mm on the right.
.................................................................................................. .................................................................................................. ..................................................................................................
Other
3 (5.6)
Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
ing transection of the embalmed cadavers.
IIA The mean length of the IIA was 26.8 (range, 0-52) mm on the left and 27.0 (range, 0-49) mm on the right (Table 2).
Posterior division branches The iliolumbar (IL), lateral sacral (LS), and superior gluteal (SG) arose from a common trunk in 61.5 % (32 of 52) of cadavers on the left and in 63.0% (34 of
The mean combined length of the IIA plus posterior division branches was 28.6 (range, 2-56) mm with an SD of 11.0 mm.
Internal iliac vein and tributaries The location of the internal iliac vein relative to the IIA and posterior division branches was examined in 15 pelvic halves on the right and 17 on the left. The vein was located dorsal and lateral to the artery in 70.6% (12 of 17) of pelvic halves on the left and 93.3% (14 of 15) on the right (Figure 5). In the remaining pelvic halves, the internal iliac vein was noted medial and inferior to the artery. Multiple tributaries of the internal iliac vein
Length (mm) Mean ⴞ SD
Median
Range
P value ⬍.001
Left internal iliac
.....................................................................................................................................................................................................................................
Unembalmed
37
29.0 ⫾ 9.6
29.5
7-52
Embalmed
17
21.8 ⫾ 11.6
24.0
0-38
Total
54
26.8 ⫾ 10.7
27.0
0-52
..................................................................................................................................................................................................................................... ..................................................................................................................................................................................................................................... ..............................................................................................................................................................................................................................................
Right internal iliac
.002
.....................................................................................................................................................................................................................................
Unembalmed
37
29.0 ⫾ 10.4
29.5
0-49
Embalmed
17
22.6 ⫾ 8.1
24.5
0-31
Total
54
27.0 ⫾ 10.1
27.5
0-49
..................................................................................................................................................................................................................................... ..................................................................................................................................................................................................................................... ..............................................................................................................................................................................................................................................
P value for embalmed vs unembalmed. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
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Left pelvic half of embalmed cadaver showing the LS, SG, and IL arteries branching from a common trunk (indicated by asterisk).
were always noted on the pelvic sidewall lateral to the internal iliac artery.
C OMMENT
Lengths of internal iliac arteries n
Left pelvic half of embalmed cadaver
Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
Combined length of IIA plus posterior division branches
TABLE 2
Artery
FIGURE 3
American Journal of Obstetrics & Gynecology DECEMBER 2007
When performing an IIA ligation, the surgeon should not only achieve hemostasis but also must be cognizant of avoiding iatrogenic injury to nearby vital structures. The ureter courses just medial to the IIA near the origin of the posterior division branches and must be identified and displaced medially. The bifurcation of the common iliac artery into external and internal iliacs must be unequivocally identified and the IIA traced distally to prevent unintentional ligation of the external iliac artery. Ideally, one would ligate the IIA distal to the posterior division branches because buttock claudication and necrosis have been associated with ligation proximal to these branches.16-18 In this study, posterior division branches arose from a common trunk in the majority of cases, on average 2.7 cm from the common iliac artery bifurcation. When the craniocaudal width of this first branch is taken into consideration, the mean combined distance from the common iliac artery bifurcation where posterior division branches would be spared was 3.2 cm. However, to avoid these branches in 95% of cases, the addition of 2 SDs to the mean combined distance is necessary. This yields an average
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TABLE 3
Frequency distribution of first posterior division branch Posterior division Left, branch n (%)
Right, n (%)
Common trunk
32 (61.5) 34 (63.0)
Iliolumbar
14 (26.9) 16 (29.6)
........................................................................................................... ...........................................................................................................
Lateral sacral
3 (5.8)
3 (5.6)
Superior gluteal
3 (5.8)
1 (1.8)
...........................................................................................................
Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
distance of 5 cm from the common iliac artery bifurcation. In a study of the IIA in 22 fresh female cadavers, Terek et al24 reported an average length of 38.4 mm on the left and 40.2 mm on the right. The 39th edition of Gray’s Anatomy25 also reports the length of each IIA to be approximately 4 cm. These values differ significantly from ours. The references cited in Gray’s Anatomy do not comment on whether these measurements were obtained in embalmed or unembalmed cadavers, and neither of these sources provide detailed descriptions regarding the methodology used to obtain measurements. In our study, we found a significant difference in the average length of the IIA between embalmed (22.2 mm) and unembalmed (29.0 mm) cadavers (Table 2). It is unclear whether this difference FIGURE 4
Right pelvic half of embalmed cadaver
Right pelvic half of embalmed cadaver with IL artery arising as the first branch, separately from the SG and LS. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
was related to the effects of the embalming process on the arteries or to increased pliability of unembalmed tissue leading to measurement overestimates. In the study by Terek et al,24 mean cadaver age was not reported, but the age range was 13-76 years. The average age in our study was 80 years (range, 45-103). Although unlikely to account for more than 1 cm difference in average length, it is possible that changes associated with aging and/or atherosclerosis can affect the length of the vessels. Additionally, in our study, the iliolumbar artery was noted to be the first posterior division branch in 28% of cadavers, arising independently from the superior gluteal and lateral sacrals. The location of this branch from the common iliac artery bifurcation was highly variable and was even noted to arise from the proximal portion of the IIA just at the point of bifurcation of the common iliac. Because this vessel coursed superiorly toward the false pelvis and behind or posterior to the common iliac vessels and lumbosacral nerve trunk, identification required more detailed dissection. We do not know whether this vessel was taken into consideration when measuring the IIA length in the aforementioned studies. Because we considered this branch as one of the points of reference to measure the length of the IIA, our data could potentially be skewed to reflect a shorter IIA length. Based on our data, the posterior division branches should be encountered, on average, 3.2 cm from the common iliac artery bifurcation. To spare the posterior division branches in 95% of cases, or 2 SDs from the mean, a ligation distance of 5 cm from the common iliac artery bifurcation is a safe recommendation. It should be stressed, however, that blind ligation of the IIA artery, at any location, is never advocated. Even in the setting of acute hemorrhage, a surgeon must maintain control and obtain adequate exposure to avoid causing further iatrogenic injury. Posterior division branches were always noted to arise from the dorsal and lateral aspect of the IIA. Although the IL and LS branches coursed superiorly and medially within the pelvis, respectively, the SG coursed laterally and inferiorly through the
FIGURE 5
Right pelvic half of unembalmed cadaver
Right pelvic half of unembalmed cadaver showing the most common location of the internal iliac vein, lateral to the artery. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
internal iliac venous tributaries prior to exiting the pelvis through the greater sciatic foramen. Therefore, when passing a clamp around the IIA to retrieve a ligating suture, the surgeon should be aware of the lateral location of these veins relative to the arteries. Accordingly, lateral to medial placement of the clamp is advisable to avoid vein laceration and difficult-to-control venous bleeding. Although performed less frequently than in years past, IIA ligation continues to be a surgical alternative in select cases of pelvic hemorrhage, in both obstetric and gynecologic settings. In the event of acute hemorrhage, a detailed dissection of the IIA is not always feasible. Thus, understanding the approximate location, orientation, and anatomic relationships of the IIA and its posterior division branches should aid in preventing further blood loss and other potentially severe complications such as ureteral injury, vein laceration, and ligation of the external iliac artery. The relationship of the IIA to the ureter, internal iliac vein, and pelvic sidewall veins warrants that IIA ligation be performed only by surgeons with sufficient surgical skill and a thorough understanding of pelvic anatomy. f REFERENCES 1. Obstetrical hemorrhage. In: Cunningham FG, Leveno KJ, Bloom SL, Hauth JC, Gilstrap LC 3rd,
DECEMBER 2007 American Journal of Obstetrics & Gynecology
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SGS Meeting Papers Wenstrom KD, eds. Williams obstetrics. 22nd ed. New York: McGraw-Hill; 2005. p. 828-9. 2. Obstetrics in broad perspective. In: Cunningham FG, Leveno KJ, Bloom SL, Hauth JC, Gilstrap LC 3rd, Wenstrom KD, eds. Williams obstetrics. 22nd ed. New York: McGraw-Hill; 2005. p. 7-8. 3. Kelly HA. Ligation of both internal arteries for hemorrhage in hysterectomy for carcinoma uteri. Bull Johns Hopkins Hosp 1894;5:53-4. 4. Burchell RC. Physiology of internal iliac artery ligation. J Obstet Gynaec Br Commonw 1968;75:642-51. 5. Evans S, McShane P. The efficacy of internal iliac artery ligation in obstetric hemorrhage. Surg Gynecol Obstet 1985;160:250-3. 6. Clark SL, Phelan JP, Yeh SY, Bruce SR, Paul RH. Hypogastric artery ligation for obstetric hemorrhage. Obstet Gynecol 1985;66:353-6. 7. Das BN, Biswas AK. Ligation of internal iliac arteries in pelvic haemorrhage. J Obstet Gynaecol Res 1998;24:251-4. 8. Papp Z, Tóth-Pál E, Papp C, Sziller I, et al. Hypogastric artery ligation for intractable pelvic hemorrhage. Int J Gynaecol Obstet 2005; 92:27-31. 9. Arango HA, Hoffman MS, Roberts WS, et al. Does ligation of the hypogastric artery at the time of radical hysterectomy and lymphadenectomy decreased blood loss: results of a prospective randomized trial. Int J Gynecol Cancer 1999; 9:137-40.
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www.AJOG.org 10. Gharoro EP. Surgical management of early stages of cervical cancer: the value of internal iliac artery ligation. J Obstet Gynaecol 2003;23:44-7. 11. American College of Obstetricians and Gynecologists. Postpartum hemorrhage. Practice bulletin no. 76, October 2006. Washington, DC: American College of Obstetricians and Gynecologists. 12. O’Leary JA. Uterine artery ligation in the control of postcesarean hemorrhage. J Reprod Med 1995;40:189-93. 13. Cruikshank SH, Stoelk EM. Surgical control of pelvic hemorrhage: bilateral hypogastric artery ligation and method of ovarian ligation. South Med J 1985;78:539-43. 14. Badawy SZ, Etman A, Singh M, Murphy K, Mayelli T, Philadelphia M. Uterine artery embolization: the role in obstetrics and gynecology. Clin Imaging 2001;25:288-95. 15. Hansch E, Chitkara U, McAlpine J, Yasser E, Dake MD, Razavi MK. Pelvic arterial embolization for control of obstetrical hemorrhage: a five year experience. Am J Obstet Gynecol 1999;180:1454-60. 16. Iliopoulos JI, Howanitz PE, Pierce GE, Kueshkerian SM, Thomas JH, Hermreck AS. The critical hypogastric circulation. Am J Surg 1987;154:671-5. 17. Picone AL, Green RM, Ricotta JR, May AG, DeWeese JA. Spinal cord ischemia following operations on the abdominal aorta. J Vasc Surg 1986;3:94-103.
American Journal of Obstetrics & Gynecology DECEMBER 2007
18. Seagraves A, Rutherford RB. Isolated hypogastric artery revascularization after previous bypass for aortoiliac occlusive disease. J Vasc Surg 1987;5:472-4. 19. Management of postpartum hemorrhage. In: Gilstrap LC 3rd, Cunningham FG, VanDorsten JP, eds. Operative obstetrics. 2nd ed. New York: McGraw-Hill; 2002. p. 410-1. 20. Jones HW 3rd, Rock WA Jr. Control of pelvic hemorrhage. In: Rock JA, Jones HW 3rd, eds. TeLinde’s operative gynecology. 9th ed. Philadelphia: Lippincott Williams & Wilkins; 2003. p. 437-41. 21. Ashley FL, Anson BJ. The hypogastric artery in American whites and negroes. Am J Phys Anthropol 1941;28:381-95. 22. Braithwaite JL. Variations in origin of the parietal branches of the internal iliac artery. J Anat 1953;86:423-30. 23. Roberts WH, Krishingner GL. Comparative study of human internal iliac artery based on Adachi classifications. Anat Rec 1967; 158:191-6. 24. Terek MC, Saylam C, Orhan M, Yilmaz A, Oztekin K. Surgical anatomy of the posterior division of the internal iliac artery: the important point for internal iliac artery ligation to control pelvic haemorrhage. Aust N Z J Obstet Gynaecol 2004;44:374. 25. Healy JC, Borley NR, Mundy A. True pelvis, pelvic floor and perineum. In: Standring S, ed. Gray’s anatomy. 39th ed. Edinburgh: Elsevier; 2005. p. 1360-1.
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Posterior division of the internal iliac artery: Anatomic variations and clinical applications April T. Bleich, MD; David D. Rahn, MD; Cecilia K. Wieslander, MD; Clifford Y. Wai, MD; Shayzreen M. Roshanravan, MD; Marlene M. Corton, MD OBJECTIVE: The objective of the study was to characterize the anatomy of the internal iliac artery (IIA) and its posterior division branches and to correlate these findings to IIA ligation. STUDY DESIGN: Dissections were performed in 54 female cadavers. RESULTS: Average length of IIA was 27.0 (range, 0-52) mm. Posterior
division arteries arose from a common trunk in 62.3% (66 of 106) of pelvic halves. In the remaining specimens, branches arose independently from the IIA, with the iliolumbar noted as the first branch in 28.3%, lateral sacral in 5.7%, and superior gluteal in 3.8%. The average width of the first branch was 5.0 (range, 2-12) mm. In all dissec-
tions, posterior division branches arose from the dorsal and lateral aspect of IIA. The internal iliac vein was lateral to the artery in 70.6% (12 of 17) of specimens on the left and 93.3% (14 of 15) on the right. CONCLUSION: Ligation of the IIA 5 cm distal from the common iliac bifurcation would spare posterior division branches in the vast majority of cases. Understanding IIA anatomy is essential to minimize intraoperative blood loss and other complications.
Key words: hypogastric artery ligation, internal iliac artery, pelvic hemorrhage, vascular anatomy
Cite this article as: 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;197:658.e1-658.e5.
H
emorrhage is the second leading cause of obstetrical mortality in the United States and the number one cause of maternal death in developing nations.1,2 It also represents a major source of morbidity in gynecologic surgery. Kelly3 was the first to describe ligation of the internal iliac artery (IIA) as a method to control hemorrhage during pelvic surgery in 1894. For many years, it was assumed that this procedure worked by ceasing blood flow to the pelvis. However, in 1968, Burchell4 shed light onto the mechanism of IIA ligation. By performing aortograms as early as 5 minutes after IIA ligation, he showed that flow
From the Division of Urogynecology and Reconstructive Surgery, Department of Obstetrics and Gynecology, University of Texas Southwestern Medical Center, Dallas, TX. Presented at the 33rd Annual Scientific Meeting of the Society of Gynecologic Surgeons, Orlando, FL, April 12-14, 2007. Received Jan. 17, 2007; revised May 17, 2007; accepted Aug. 22, 2007. Reprints not available from the authors. 0002-9378/$32.00 © 2007 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2007.08.063
658.e1
did not cease distal to the site of ligation, but rather the direction of flow was reversed using collateral pathways through the lumbar-iliolumbar, middle sacrallateral sacral, and superior and middle hemorrhoidal arteries (Figure 1). Importantly, he demonstrated that bilateral ligation decreased the pulse pressure (pulsation) in the distal artery by as much as 85%, whereas blood flow was reduced by at most 50%. He stated that reduction in pulse pressure created a “venous-like system,” which allowed blood clots to form at the sites of bleeding and that this was the factor responsible for hemostasis. The use of IIA ligation in current obstetrics and gynecology is controversial. The efficacy of this procedure in controlling obstetrical hemorrhage has been reported to range from 4275%.5-8 Similarly, studies reviewing prophylactic IIA ligation at the time of radical hysterectomy have yielded conflicting results.9,10 The 2006 American College of Obstetricians and Gynecologists Practice Bulletin regarding postpartum hemorrhage states: “Hypogastric artery ligation is performed much less frequently than in years past. Practitioners are less familiar with this technique,
American Journal of Obstetrics & Gynecology DECEMBER 2007
and the procedure has been found to be considerably less successful than previously thought.”11 Selective ligation of the uterine artery, as described by O’Leary,12 has been shown to be successful and relatively easy to perform, with few reported complications. Thus, this procedure has become one of the first surgical methods used in controlling postcesarean pelvic hemorrhage, especially when the bleeding is known to be of uterine origin. Ligation of the ovarian arteries has also been described.13 IIA ligation is still warranted in select cases, when more conservative surgical methods to control hemorrhage, including bilateral uterine and even ovarian artery ligation, have failed, especially if preservation of fertility is strongly desired in a stable patient. IIA ligation may also play a role in the setting of persistent bleeding following hysterectomy. Although embolization of the uterine vessels by interventional radiology has been shown to have higher success rates than those reported for IIA ligation,14,15 this procedure requires a stable patient and available personnel and resources. Therefore, IIA ligation may be the only alternative, and a life-saving ap-
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FIGURE 1
Pelvic arterial anatomy
Collateral circulation after internal IIA ligation as demonstrated by Burchell. Collateral pathways include: lumbar-iliolumbar, middle sacral-lateral sacral, and superior-middle rectal (hemorrhoidal) arteries. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
proach, in the setting of severe gynecologic or obstetric pelvic hemorrhage. Despite the enormous reserve in blood supply of the pelvis, acute interruption of the IIA has been associated with buttock claudication and necrosis.16-18 Accordingly, current obstetrics and gynecology textbooks advocate ligation of the IIA distal to the posterior division branches in order to preserve collateral circulation.19,20 Because this procedure is often performed emergently and after other measures to control bleeding have failed, understanding the IIA anatomy and approximate location and anatomic relationships of the posterior division branches should reduce the risk of further intraoperative bleeding and other serious complications. Yet most studies reviewing the IIA anatomy have been performed primarily on male cadavers and have focused on branching patterns of the parietal arteries rather than the length of the IIA before its division.21-23 Thus, the objectives of this study were to examine the IIA anatomy, anatomic location, and relationships of its posterior division branches and to correlate these findings to IIA ligation.
M ATERIALS AND M ETHODS The common and internal iliac arteries were dissected out bilaterally in 37 unembalmed and 17 embalmed female cadavers. The cadavers were obtained from
the Willed Body Program at the University of Texas at Southwestern Medical Center in Dallas. This study was considered exempt by the University of Texas Southwestern Medical Center Institutional Review Board in accordance with the Code of Federal Regulations, Title 45. Age, height, and weight at the time of death, as well as cause of death, were available for the majority of donors. None of the cadavers had evidence of prior vascular surgery involving the pelvis. The abdominal cavity was opened, the rectosigmoid was tied, and the bowel proximal to this level was removed. The retroperitoneal space was entered at the level of the aortic bifurcation and the common iliacs were dissected and followed to their point of division into external and internal iliac arteries (Figure 1). The fat and loose connective tissue surrounding the internal iliac artery and vein was removed and the posterior division branches were identified. The course of each posterior division branch was traced. The iliolumbar was followed superiorly toward the false pelvis in which branches were noted to supply the iliacus, psoas major, and quadratus lumborum muscles. The superior gluteal was followed until it exited the pelvis between the lumbosacral nerves. The lateral sacrals were followed medially towards the anterior sacral foramina. The relationship between the IIA and the internal iliac vein and venous plexus was noted. The lengths of the common and internal iliac arteries were recorded. The IIA was measured from the point of bifurcation of the common iliac to the origin of the first posterior division branch (Figure 2). Branching patterns of the three posterior division branches, iliolumbar, lateral sacral, and superior gluteal were documented. The craniocaudal width of the first posterior division branch was also noted (Figure 2). The length of the IIA and the craniocaudal width of the posterior division branches were added to calculate the average length from the common iliac artery bifurcation at which posterior division branches would be spared; this was called the combined length (Figure 2). Two SDs were added
FIGURE 2
Internal iliac artery
A, Internal iliac artery length. B, Craniocaudal width of posterior division branch. C, Combined length. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
to the mean combined length to estimate the distance from the common iliac artery bifurcation in which posterior division branches would be spared in 95% of cases. Measurements were taken twice using calipers and a 10-cm plastic ruler with the pelvis in the supine position. Statistical analysis was performed using SigmaStat 2.03 statistical software (Systate Software, Inc, Inc, San Jose, CA). Continuous variables were summarized by means, medians, standard deviations (SDs), and ranges. Qualitative data were summarized by counts and percentages. P ⬍ .05 was considered statistically significant.
R ESULTS Study population characteristics Limited demographic data were available on all cadavers examined (Table 1). Mean age at time of death was 79.6 years (range, 45-103 yrs). Average body mass index was 23.3 kg/m2. Fifty-three cadavers were white and 1 was African American.
Common iliac artery The mean length of the common iliac artery was 57.0 (range, 30-94) mm on the left and 55.2 (range, 25-91) mm on the right. These values represent the average lengths in the 37 unembalmed specimens only because the majority of the common iliac vessels were severed dur-
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SGS Meeting Papers TABLE 1
Demographics of study population Demographic characteristic
Value
Total number cadavers, n
54
Age, mean ⫾ SD (y)
79.6 ⫾ 12.7
........................................................................................................... ...........................................................................................................
Race, n (%)
..................................................................................................
White
53 (98)
..................................................................................................
African American
1 (2)
...........................................................................................................
23.3 ⫾ 4.8
Body mass index, mean ⫾ SD (kg/m2)
...........................................................................................................
Reported cause of death, n (%)
..................................................................................................
Cardiopulmonary
23 (42.6)
Cancer
18 (33.3)
Neurologic
10 (18.5)
www.AJOG.org 54) on the right (Figure 3). In the remaining specimens, posterior division branches arose independently from the internal iliac, with the IL noted as the first branch in 28.3%, the LS in 5.7%, and the SG in 3.8% (Table 3 and Figure 4). In all cadavers, posterior division branches originated from the dorsal and lateral aspect of the artery. The SG coursed laterally and inferiorly through numerous internal iliac venous branches before exiting the pelvis through the greater sciatic foramen. The average width of the first branch of the posterior division was 4.6 (range, 2-9) mm on the left and 5.3 (range, 2-12) mm on the right.
.................................................................................................. .................................................................................................. ..................................................................................................
Other
3 (5.6)
Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
ing transection of the embalmed cadavers.
IIA The mean length of the IIA was 26.8 (range, 0-52) mm on the left and 27.0 (range, 0-49) mm on the right (Table 2).
Posterior division branches The iliolumbar (IL), lateral sacral (LS), and superior gluteal (SG) arose from a common trunk in 61.5 % (32 of 52) of cadavers on the left and in 63.0% (34 of
The mean combined length of the IIA plus posterior division branches was 28.6 (range, 2-56) mm with an SD of 11.0 mm.
Internal iliac vein and tributaries The location of the internal iliac vein relative to the IIA and posterior division branches was examined in 15 pelvic halves on the right and 17 on the left. The vein was located dorsal and lateral to the artery in 70.6% (12 of 17) of pelvic halves on the left and 93.3% (14 of 15) on the right (Figure 5). In the remaining pelvic halves, the internal iliac vein was noted medial and inferior to the artery. Multiple tributaries of the internal iliac vein
Length (mm) Mean ⴞ SD
Median
Range
P value ⬍.001
Left internal iliac
.....................................................................................................................................................................................................................................
Unembalmed
37
29.0 ⫾ 9.6
29.5
7-52
Embalmed
17
21.8 ⫾ 11.6
24.0
0-38
Total
54
26.8 ⫾ 10.7
27.0
0-52
..................................................................................................................................................................................................................................... ..................................................................................................................................................................................................................................... ..............................................................................................................................................................................................................................................
Right internal iliac
.002
.....................................................................................................................................................................................................................................
Unembalmed
37
29.0 ⫾ 10.4
29.5
0-49
Embalmed
17
22.6 ⫾ 8.1
24.5
0-31
Total
54
27.0 ⫾ 10.1
27.5
0-49
..................................................................................................................................................................................................................................... ..................................................................................................................................................................................................................................... ..............................................................................................................................................................................................................................................
P value for embalmed vs unembalmed. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
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Left pelvic half of embalmed cadaver showing the LS, SG, and IL arteries branching from a common trunk (indicated by asterisk).
were always noted on the pelvic sidewall lateral to the internal iliac artery.
C OMMENT
Lengths of internal iliac arteries n
Left pelvic half of embalmed cadaver
Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
Combined length of IIA plus posterior division branches
TABLE 2
Artery
FIGURE 3
American Journal of Obstetrics & Gynecology DECEMBER 2007
When performing an IIA ligation, the surgeon should not only achieve hemostasis but also must be cognizant of avoiding iatrogenic injury to nearby vital structures. The ureter courses just medial to the IIA near the origin of the posterior division branches and must be identified and displaced medially. The bifurcation of the common iliac artery into external and internal iliacs must be unequivocally identified and the IIA traced distally to prevent unintentional ligation of the external iliac artery. Ideally, one would ligate the IIA distal to the posterior division branches because buttock claudication and necrosis have been associated with ligation proximal to these branches.16-18 In this study, posterior division branches arose from a common trunk in the majority of cases, on average 2.7 cm from the common iliac artery bifurcation. When the craniocaudal width of this first branch is taken into consideration, the mean combined distance from the common iliac artery bifurcation where posterior division branches would be spared was 3.2 cm. However, to avoid these branches in 95% of cases, the addition of 2 SDs to the mean combined distance is necessary. This yields an average
SGS Meeting Papers
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TABLE 3
Frequency distribution of first posterior division branch Posterior division Left, branch n (%)
Right, n (%)
Common trunk
32 (61.5) 34 (63.0)
Iliolumbar
14 (26.9) 16 (29.6)
........................................................................................................... ...........................................................................................................
Lateral sacral
3 (5.8)
3 (5.6)
Superior gluteal
3 (5.8)
1 (1.8)
...........................................................................................................
Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
distance of 5 cm from the common iliac artery bifurcation. In a study of the IIA in 22 fresh female cadavers, Terek et al24 reported an average length of 38.4 mm on the left and 40.2 mm on the right. The 39th edition of Gray’s Anatomy25 also reports the length of each IIA to be approximately 4 cm. These values differ significantly from ours. The references cited in Gray’s Anatomy do not comment on whether these measurements were obtained in embalmed or unembalmed cadavers, and neither of these sources provide detailed descriptions regarding the methodology used to obtain measurements. In our study, we found a significant difference in the average length of the IIA between embalmed (22.2 mm) and unembalmed (29.0 mm) cadavers (Table 2). It is unclear whether this difference FIGURE 4
Right pelvic half of embalmed cadaver
Right pelvic half of embalmed cadaver with IL artery arising as the first branch, separately from the SG and LS. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
was related to the effects of the embalming process on the arteries or to increased pliability of unembalmed tissue leading to measurement overestimates. In the study by Terek et al,24 mean cadaver age was not reported, but the age range was 13-76 years. The average age in our study was 80 years (range, 45-103). Although unlikely to account for more than 1 cm difference in average length, it is possible that changes associated with aging and/or atherosclerosis can affect the length of the vessels. Additionally, in our study, the iliolumbar artery was noted to be the first posterior division branch in 28% of cadavers, arising independently from the superior gluteal and lateral sacrals. The location of this branch from the common iliac artery bifurcation was highly variable and was even noted to arise from the proximal portion of the IIA just at the point of bifurcation of the common iliac. Because this vessel coursed superiorly toward the false pelvis and behind or posterior to the common iliac vessels and lumbosacral nerve trunk, identification required more detailed dissection. We do not know whether this vessel was taken into consideration when measuring the IIA length in the aforementioned studies. Because we considered this branch as one of the points of reference to measure the length of the IIA, our data could potentially be skewed to reflect a shorter IIA length. Based on our data, the posterior division branches should be encountered, on average, 3.2 cm from the common iliac artery bifurcation. To spare the posterior division branches in 95% of cases, or 2 SDs from the mean, a ligation distance of 5 cm from the common iliac artery bifurcation is a safe recommendation. It should be stressed, however, that blind ligation of the IIA artery, at any location, is never advocated. Even in the setting of acute hemorrhage, a surgeon must maintain control and obtain adequate exposure to avoid causing further iatrogenic injury. Posterior division branches were always noted to arise from the dorsal and lateral aspect of the IIA. Although the IL and LS branches coursed superiorly and medially within the pelvis, respectively, the SG coursed laterally and inferiorly through the
FIGURE 5
Right pelvic half of unembalmed cadaver
Right pelvic half of unembalmed cadaver showing the most common location of the internal iliac vein, lateral to the artery. Bleich. Posterior division of the internal iliac artery. Am J Obstet Gynecol 2007.
internal iliac venous tributaries prior to exiting the pelvis through the greater sciatic foramen. Therefore, when passing a clamp around the IIA to retrieve a ligating suture, the surgeon should be aware of the lateral location of these veins relative to the arteries. Accordingly, lateral to medial placement of the clamp is advisable to avoid vein laceration and difficult-to-control venous bleeding. Although performed less frequently than in years past, IIA ligation continues to be a surgical alternative in select cases of pelvic hemorrhage, in both obstetric and gynecologic settings. In the event of acute hemorrhage, a detailed dissection of the IIA is not always feasible. Thus, understanding the approximate location, orientation, and anatomic relationships of the IIA and its posterior division branches should aid in preventing further blood loss and other potentially severe complications such as ureteral injury, vein laceration, and ligation of the external iliac artery. The relationship of the IIA to the ureter, internal iliac vein, and pelvic sidewall veins warrants that IIA ligation be performed only by surgeons with sufficient surgical skill and a thorough understanding of pelvic anatomy. f REFERENCES 1. Obstetrical hemorrhage. In: Cunningham FG, Leveno KJ, Bloom SL, Hauth JC, Gilstrap LC 3rd,
DECEMBER 2007 American Journal of Obstetrics & Gynecology
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SGS Meeting Papers Wenstrom KD, eds. Williams obstetrics. 22nd ed. New York: McGraw-Hill; 2005. p. 828-9. 2. Obstetrics in broad perspective. In: Cunningham FG, Leveno KJ, Bloom SL, Hauth JC, Gilstrap LC 3rd, Wenstrom KD, eds. Williams obstetrics. 22nd ed. New York: McGraw-Hill; 2005. p. 7-8. 3. Kelly HA. Ligation of both internal arteries for hemorrhage in hysterectomy for carcinoma uteri. Bull Johns Hopkins Hosp 1894;5:53-4. 4. Burchell RC. Physiology of internal iliac artery ligation. J Obstet Gynaec Br Commonw 1968;75:642-51. 5. Evans S, McShane P. The efficacy of internal iliac artery ligation in obstetric hemorrhage. Surg Gynecol Obstet 1985;160:250-3. 6. Clark SL, Phelan JP, Yeh SY, Bruce SR, Paul RH. Hypogastric artery ligation for obstetric hemorrhage. Obstet Gynecol 1985;66:353-6. 7. Das BN, Biswas AK. Ligation of internal iliac arteries in pelvic haemorrhage. J Obstet Gynaecol Res 1998;24:251-4. 8. Papp Z, Tóth-Pál E, Papp C, Sziller I, et al. Hypogastric artery ligation for intractable pelvic hemorrhage. Int J Gynaecol Obstet 2005; 92:27-31. 9. Arango HA, Hoffman MS, Roberts WS, et al. Does ligation of the hypogastric artery at the time of radical hysterectomy and lymphadenectomy decreased blood loss: results of a prospective randomized trial. Int J Gynecol Cancer 1999; 9:137-40.
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www.AJOG.org 10. Gharoro EP. Surgical management of early stages of cervical cancer: the value of internal iliac artery ligation. J Obstet Gynaecol 2003;23:44-7. 11. American College of Obstetricians and Gynecologists. Postpartum hemorrhage. Practice bulletin no. 76, October 2006. Washington, DC: American College of Obstetricians and Gynecologists. 12. O’Leary JA. Uterine artery ligation in the control of postcesarean hemorrhage. J Reprod Med 1995;40:189-93. 13. Cruikshank SH, Stoelk EM. Surgical control of pelvic hemorrhage: bilateral hypogastric artery ligation and method of ovarian ligation. South Med J 1985;78:539-43. 14. Badawy SZ, Etman A, Singh M, Murphy K, Mayelli T, Philadelphia M. Uterine artery embolization: the role in obstetrics and gynecology. Clin Imaging 2001;25:288-95. 15. Hansch E, Chitkara U, McAlpine J, Yasser E, Dake MD, Razavi MK. Pelvic arterial embolization for control of obstetrical hemorrhage: a five year experience. Am J Obstet Gynecol 1999;180:1454-60. 16. Iliopoulos JI, Howanitz PE, Pierce GE, Kueshkerian SM, Thomas JH, Hermreck AS. The critical hypogastric circulation. Am J Surg 1987;154:671-5. 17. Picone AL, Green RM, Ricotta JR, May AG, DeWeese JA. Spinal cord ischemia following operations on the abdominal aorta. J Vasc Surg 1986;3:94-103.
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18. Seagraves A, Rutherford RB. Isolated hypogastric artery revascularization after previous bypass for aortoiliac occlusive disease. J Vasc Surg 1987;5:472-4. 19. Management of postpartum hemorrhage. In: Gilstrap LC 3rd, Cunningham FG, VanDorsten JP, eds. Operative obstetrics. 2nd ed. New York: McGraw-Hill; 2002. p. 410-1. 20. Jones HW 3rd, Rock WA Jr. Control of pelvic hemorrhage. In: Rock JA, Jones HW 3rd, eds. TeLinde’s operative gynecology. 9th ed. Philadelphia: Lippincott Williams & Wilkins; 2003. p. 437-41. 21. Ashley FL, Anson BJ. The hypogastric artery in American whites and negroes. Am J Phys Anthropol 1941;28:381-95. 22. Braithwaite JL. Variations in origin of the parietal branches of the internal iliac artery. J Anat 1953;86:423-30. 23. Roberts WH, Krishingner GL. Comparative study of human internal iliac artery based on Adachi classifications. Anat Rec 1967; 158:191-6. 24. Terek MC, Saylam C, Orhan M, Yilmaz A, Oztekin K. Surgical anatomy of the posterior division of the internal iliac artery: the important point for internal iliac artery ligation to control pelvic haemorrhage. Aust N Z J Obstet Gynaecol 2004;44:374. 25. Healy JC, Borley NR, Mundy A. True pelvis, pelvic floor and perineum. In: Standring S, ed. Gray’s anatomy. 39th ed. Edinburgh: Elsevier; 2005. p. 1360-1.