Vesicular Blood Flow After Ligation of the Internal Iliac Arteries in Low Anterior Resection or A b d o m i n o p e r i n e a l Resection Sotaro Sadahiro, M.D., Hideki Ishida, M.D., Toshiyuki Suzuki, M.D., Kennji Ishikawa, M.D., Tomoo Tajima, M.D., Hiroyasu Makuuchi, M.D. From the Department of Surgery, Tokai UniverMty, School of Medicine, Kanagawa, Japan Sadahiro S, Ishida H, Suzuki T, Ishikawa K, Tajima T, Makuuchi H. Vesicular blood flow after ligation of the internal lilac arteries in low anterior resection or abdominoperineal resection. Dis Colon Rectum 1999:42:1475-1479.
PURPOSE: Bilateral ligation of the internal iliac arteries has
been reported to be a safe procedure in pelvic surgery because there are five collateral pathways. Some of the five pathways are surgically interrupted after resection of the rectum and two cases in which necrosis developed in the perineum were reported. The aim of the study was to assess the degree of safety and blood flow reducing efficacy of internal iliac artery ligation in rectal cancer surgery. METHODS: The subjects were 23 patients with advanced rectal cancer. Tissue blood flow on the surface of the bladder was measured using a laser Doppler flow meter when unilateral or bilateral internal iliac artery were clamped at a central site or at a peripheral site. RESULTS: Tissue blood flow of the bladder before clamping the internal iliac artery was 6 to 74 ml/min/100 g. Blood flow in the right half of the bladder decreased significantly when the right and both internal iliac arteries were clamped (both, P < 0~01), but it did not decrease significantly when only the left internal itiac artery was damped. The results were the same whether the central site or peripheral site was clamped. When the central site was clamped, there was no difference between the decrease in blood flow in the right half of the bladder whether the right internal iliac artery was clamped or both internal lilac arteries were clamped. By contrast, when the peripheral site was clamped, the decrease in blood flow in the right haft of the bladder was much greater when both internal iliac arteries were clamped than when the right internal lilac artery alone was clamped (P < 0.01). The results in the left haft were the same as in the right half. Blood flow became 33 to 110 (mean, 73; median, 75) percent of the value before clamping when both internal iliac arteries were clamped at the central site, and 18 to 114 (mean, 52; median, 47) percent when both hltemal lilac arteries were clamped at the peripheral site. No changes in the color of the bladder or other pelvic organs were observed while the internal iliac arteries were clamped. CONCLUSION: Our study suggests that bilateral internal iliac artery ligation causes a temporary decrease in blood flow to the pelvic organs, but the reduction is not great enough to induce necrosis histologically. We recommend the ligation of the internal iliac arteries at the point below the takeoff of the superior gluteal artery to gain a considerable blood flow reducing effect on the pelvic organs. [Key-words: Internal itiac artery; Rectal surgery; Pelvic blood flow]
T
h e internal iliac artery (IIA) is t h e m a j o r b l o o d s u p p l y to t h e pelvis a n d p e l v i c organs, a n d IIA
ligation has b e e n u s e d to c o n t r o l l i f e - t h r e a t e n i n g h e m o r r h a g e in p e l v i c t r a u m a 1 a n d obstetrics a n d gyn e c o l o g y , 2-4 to d e c r e a s e b l e e d i n g c a u s e d b y s u r g e r y for a d v a n c e d rectal cancer, 5, 6 b l a d d e r cancer, 7 a n d g y n e c o l o g i c cancer,< 9 a n d to facilitate t h e d i s s e c t i o n in p e l v i c surgery. B e c a u s e t h e r e are five collateral p a t h w a y s , i . 3 bilateral IIA ligation h a s b e e n r e p o r t e d to b e a safe p r o c e d u r e that d o e s n o t give rise to a n y c o m p l i c a t i o n s P , s, s. s N e v e r t h e l e s s , Tajes ~° r e p o r t e d a case of necrosis of the buttocks and gluteus maximus muscle, a n d A n d r i o l e a n d S u g a r b a k e r 11 r e p o r t e d a case o f n e c r o s i s o f the b l a d d e r , vagina, a n d p e r i n e u m , after bilateral ligation o f the IIAs. S k i n n e r 7 a n d A n d riole a n d S u g a r b a k e r n s t a t e d that the IIA s h o u l d b e l i g a t e d b e l o w the t a k e o f f o f the s u p e r i o r gluteal artery as a m e a n s o f p r e v e n t i n g h i p c l a u d i c a t i o n a n d p e r i n e a l necrosis, respectively. I n t h e c a s e r e p o r t e d b y A n d r i o l e a n d S u g a r b a k e r , h o w e v e r , the b l a d d e r a n d the v a g i n a b o t h n e c r o s e d t o g e t h e r w i t h p e r i n e u m s i m u l t a n e o u s l y . W h e t h e r a d e q u a t e b l o o d s u p p l y to the p e l v i c o r g a n s is m a i n t a i n e d w h e n t h e ligation is p l a c e d after the t a k e o f f o f the s u p e r i o r gluteal artery has to b e c o n f i r m e d . M o r e o v e r , after s u r g e r y for rectal cancer, s o m e o f the five collateral b l o o d f l o w c h a n nels r e p o r t e d to f u n c t i o n after b i l a t e r a l tIA ligation a r e i n t e r r u p t e d surgically. T h e r e f o r e , to e l u c i d a t e t h e d e g r e e o f safety a n d b l o o d f l o w r e d u c i n g efficacy o f IIA
Poster presentation at the meeting of The American Society of Colon and Rectal Surgeons, San Antonio, Texas, May 2 to 7, 1998. Address reprint requests to Dr. Sadahiro: Bohseidai Isehara-shi Kanagawa, 259-1193, Japan. 1475
ligation in rectal c a n c e r surgery, w e t e m p o r a r i l y interr u p t e d IIA b l o o d f l o w i n t r a o p e r a t i v e l y a n d a s s e s s e d the effect o n tissue b l o o d f l o w in the b l a d d e r .
1476
SADAHIRO E T A L PATIENTS AND
METHODS
The subjects of this investigation were 23 surgicat patients with advanced rectal cancer. There were 18 males; m e a n age was 60.9 + 9.1 (mean _+ standard deviation) years. Every patient was diagnosed to belong to Stage 2 or 3 preoperatively. No patient received irradiation before surgery. All patients gave their informed consent. Surgery was performed in the lithotomy position under general anesthesia in every case. The procedure was low anterior resection in 10 cases and abdominoperineal resection, in the other 13 cases. None of the patients had apparent invasion to the adjacent organs or to the sidewall of the pelvis. Therefore, every operation was judged to be curative. After resecting the rectum, the p r o b e of a tissue blood flowmeter was fixed to the right or left surface of the bladder, and the IIA was clamped with a bulldog forceps. The sites chosen to clamp the IIA were a central site (proximal site) located immediately after the IIA branches off the c o m m o n lilac artery and a peripheral site (distal site) located b e l o w the takeoff of the superior gluteal artery (Fig. 1). Tissue blood flow was measured at the surface of the bladder w h e n the right tIA was clamped, w4mn the left IIA was clamped, and w h e n both IIAs were clamped; blood flow in the right half and left half of the bladder were measured separately. Tissue blood flow was mea-
Dis Colon Rectum, November 1999
sured three minutes after clamping with a laser Doppler tissue blood flowmeter (Advance, Tokyo, Japan). A paired t-test was used for statistical analysis, and t percent was adopted as the significance level.
RESULTS Tissue blood flow at the bladder surface before clamping the IIA was 6 to 74 ml/min/100 g (Tables 1 and 2). Blood flow in the right half of the bladder decreased significantly w h e n the right and both IIAs were clamped (both P < 0.01), but it did not decrease significantly w h e n only the left IIA was clamped. The results were the same whether the central site (proximal site) or peripheral site (distal site) was clamped, and the results for blood flow in the left half of the bladder were the same as in the right side (Tables 3 and 4). When the central site was clamped, there was no difference b e t w e e n the decrease in blood flow in the right half of the bladder whether the right IIA was clamped or both IIAs were clamped. By contrast, w h e n the peripheral site was clamped, the decrease in b l o o d flow in the right half was m u c h greater w h e n both IIAs were clamped than w h e n the right IIA alone was clamped (P < 0.01). The results in the left half of the bladder were the same as in the right half. Blood flow at the surface of the bladder w h e n both
ExternaJ Iliac Artery
~c Artery
Urinar~
Figure 1. Diagrammatic view of the right side of the pelvis. The internal iliac artery (IIA) was clamped at the point immediately after the IIA branches off the common iliac artery as the central site. IIA was clamped at the point below the takeoff of the superior gluteal artery as the peripheral site.
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T a b l e 1. Tissue Blood Flow at the Right Half of the Urinary Bladder
Patient No.
Gender
Age
Before Clamping
1 2 3 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23
M M M F F M M M M M M M F M M M M F M
58 74 43 64 60 50 72 67 59 51 54 58 60 6O 48 47 69 69 63
41 * 25 53 59 22 66 18 31 14 15 2t.5 10 30.5 39 29 72.5 19 42 48
Clamping at the Central Site Right IIA
Left IIA
Both IIAs
25.5 29
27 52
23 29.5
19.5 34 14 31 14 8.5 20.5 8 19.5 19 28 54 15 33 34
20.5 62 14 32 13 13.5 22.5 9 25 37 27 54 16 43 48
19 35 14 30 12 10.5 21.5 6.5 18 20 28 51 12 29 34
Clamping at the Peripheral Site Right IIA
Left IIA
Both IIAs
12 18.5 6.5 13 13 11 7 21 16 12
20 25.5 28.5 61 19.5 20 7 21 16 12
12 10.5 6.5 8 11 9 7 19 16 8
4 27 14 30 50 11 36 28
9 33.5 19 30 68 19 42 48
4 19 7.5 30 50 11 36 28
IIA = internal iliac artery. * ml/min/100 g.
IIAs were clamped at the central site was 33 to 110 (mean, 73; median, 75) percent of the value before clamping, and 18 to 114 (mean, 52; median, 47) percent w h e n both IIAs were clamped at the peripheral site. No changes in the color of the bladder or other pelvic organs were observed while the IIAs were clamped. DISCUSSION The values of tissue blood flow in the bladder ranged widely, because the laser Doppler flowmeter used for this experiment measured the tissue blood flow only in the area within a radius of I mm around the probe. 12 Therefore, we fL,ced the probe on the surface of the bladder by suturing and compared the values before and after clamping using a paired t-test. The IIA is the main blood supply of the pelvis and pelvic viscera. There are five collateral channels: 1) both ovarian arteries from the aorta, 2) the branches of the inferior epigastric artery from the external iliac arteries, 3) the superior hemorrhoidal artery from the inferior mesenteric artery, 4) the circumflex and perforating branches of the deep femoral arteries, and 5) the lower lumbar arteries from the aorta, a, 3 and it is said that hip claudication, sloughing, and bladder
dysfunction ordinarily do not occur even w h e n the IIAs are ligated on both sides. 3, 6, s, 13 After resection of the rectum, however, the superior hemorrhoidal artery is lost, and the ovarian arteries may also be surgically interrupted in some cases. Tajes 1° and Andriole and Sugarbaker 11 reported cases in which necrosis developed in the perineum after surgical resection of the rectum, during which they ligated the IIAs on both sides. In Andriole's case there was a previous history of radiation therapy; the bladder, vagina, and perineum became necrotic; and the patient died. Skinner 7 stated that if the IIA is ligated after the takeoff of the superior gluteat artery, buttock claudication is avoided. Andriole and Sugarbaker 11 also recommended ligation of the IIA after the superior gtuteal artery branches off, but did not mention anything about changes in blood flow to the bladder. Lipschutz 14 has classified the morphology of the IIA into five types, but the superior vesical artery and the inferior vesical artery, which both supply the bladder, branch off after the takeoff of the superior gluteal artery in all five types. Thus, it appears that w h e n the IL¢ is ligated after the takeoff of the superior gluteal artery, blood flow in the superior vesicai artery and the inferior vesical artery is interrupted at a point
SADAHtRO E T A L
1478
Dis Coton Rectum, November 1999
Table 2. Tissue Blood Flow at the Left Half of the Urinary Bladder
Patient No,
Gender
4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23
M M F M F F M M M M M M M F M M M M F M
Age
Clamping at the Central Site
Clamping at the Peripheral Site
Before Clamping
Right IIA
Left IIA
Both llAs
Right IIA
Left IIA
Both IIAs
25* 30.6 21 18 59 22 18 13 13 70 33.5 24 6 24.5 30 22 31.5 62 20 42
23 32.5 17.5 9 45 14 14 8.3 14 74 29 20 6 21.5 30.5 22 28 60 20 42
21 22 18 6 38 14 14 7 12 66 21 17.5 6 12 18 18 22 60 13 38
20 25 18 6 24 14 11.5 6 11 54 23 10.5 6 11.5 19 18 16 60 14 38
28 25 23 6.5
16 13.5 18 3.8
16 12.5 12 4
17 22 11.5 11 62
15 17.5 5 11 50
14 17 5 11 40
20 7 15 21.5 22.5 27.5 50 24 42
5 3 14.5 15 22 15 42 15 36
4.3 3 10 7.5 21.5 15 26 14 36
77 67 61 70 64 60 50 72 67 59 51 54 58 60 60 48 47 69 69 63
IIA = internal lilac artery. * ml/min/100 g.
Table 3. Tissue Blood Flow when IIA was Clamped at the Central Site
Right half of the bladder Left half of the bladder
Table 4. Tissue Blood Flow when IIA was Clamped at the Peripheral Site
Vessel Clamped
Vessel Clamped
Right IIA Left IIA Both IIAs
Right IIA Left IIA Both IIAs
~ ,i,
$
IIA = internal lilac artery. $ = Decrease in comparison with the value before clamping (P < 0.01).
close to their central portion, and blood flow to the bladder is reduced even more. Accordingly, in this study we measured blood flow to the bladder w h e n the site where the ItA was clamped was central to the takeoff of the superior gluteal artery and w h e n it was clamped peripheral to the takeoff. Blood flow in the Madder decreased w h e n the IIA was clamped on the same side whether the site of the clamping was central or peripheral, and did not decrease when the contralateral IIA alone was damped. When the IIA was clamped central to the takeoff of the superior gluteal artery, there was no significant difference between the decrease in blood flow w h e n the
Right half of the bladder Left half of the bladder
$ $
~ ~$
IIA = internal lilac artery. $ = Decrease in comparison with the value before clamping (P < 0.01). ~J, = Decrease in comparison with the value when one of the IIAs was clamped (P < 0.01).
ipsilateral IIA was clamped and both IIAs were clamped, but when the IIA was clamped peripheral to the branch point of the superior gluteal artery, blood flow that had decreased as a result of clamping the ipsilaterat IIA decreased even more when both IIAs were clamped. The percentage decrease in blood flow as a result of clamping both hAs was greater (mean, 48 percent) w h e n the clamp was peripheral than when the clamp was central (mean, 27 percent). These findings do not conflict with the principle that the more peripherally a blood vessel is ligated, the greater the decrease in blood
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LIGATION OF THE INTERNAL ILIAC ARTERIES
1479
flow to the organs it supplies becomes. H o w the collat-
REFERENCES
eral channels to the bladder differ when the clamp is central and peripheral to the takeoff of the superior
1. Seavers R, Lynch J, Ballard R, Jemigan S, Johnson J. Hypogastric artery ligation for uncontrollable hemorrhage in acute pelvic trauma. Surgery 1964;55:516-9. 2. Salzberg AM, Fuller WA, Hoge RH. The surgical management of profuse hemorrhage from uterine carcinoma. Surg Gynecol Obstet 1953;97:773-5. 3. Reich WJ, Nechtow MJ. Ligation of the internal iliac (hypogastric) arteries: a life-saving procedure for uncontrollable gynecologic and obstetric hemorrhage. J Int Coll Surg 1961;36:157-68. 4. Leventhal ML, Lash AF, Grossman A. Hemorrhage from carcinoma of the cervix. Surg Gynecot Obstet 1938;67: 102-4. 5. Swinton NW, Moszkowski E, Snow JC. Cancer of the colon and rectum, a statistical study of 608 patients. Surg Clin North Am 1959;39:745-52. 6. Enget GC, Singmaster L, Ligation of internal iliac arteries to facilitate abdominoperineal resection for malignancy of the rectum. Surgery 1962;52:867-70. 7. Skinner DG, Technique of radical cystectomy. Urol Clin North Am 1981;8:353-66. 8. Siegel P, Mengert WF. Internal iliac artery ligation in obstetrics and gynecology. JAMA 1961;178:1059-62. 9. Kelly HA. Ligation of both internal iliac arteries for hemorrhage in hysterectomy for carcinoma uteri. Bull Johns Hopkins Hosp 1894;5:53-4. 10. Tajes RV. Ligation of the hypogastric arteries and its complications in resection of cancer of the rectum. Am J Gastroenterot 1956;26:612-8. 11. Andriole GL, Sugarbaker PH. Perineal and bladder necrosis following bilateral internal iliac artery ligation. Report of a case. Dis Colon Rectum 1985;28:183-4. 12. Shepherd Ap, Riedel GL. Continuous measurement of intestinal mucosal blood flow by laser-Doppler velocimetry. Am J Physiol 1982;242:G668-72. 13. Shafiroff BGP, Grillo EB, Baron H. Bilateral ligation of the hypogastric arteries. Am J Surg 1959;98:34-40. 14. Lipshutz B. A composite study of the hypogastric artery and its branches. Ann Surg 1918;67:584-608.
gluteal artery is unknown. In regard to the long-term effects of interrupting blood flow by IIA ligation, Shafiroff et al. 13 reported that the pelvic viscera displayed marked blanching immediately after they ligated both IIAs in dogs, but that their color had almost completely returned to normal by the end of two weeks. We, however, did not observe any change in the color of the pelvic viscera while both IIAs w e r e clamped. In view of the results of our o w n study and the fact that hardly any" complications have ever occurred in patients w h o s e IIAs were ligated bilaterally in the past, it was concluded that bilateral IIA ligation causes a temporary decrease in blood flow to the pelvic organs, but the reduction is not great enough to induce necrosis histologically. With regard to the site of IIA ligation, based on the purpose of this procedure, i.e., to reduce blood flow to the rectum, bladder,
uterus, vagina, and surrounding tissue, w e recomm e n d ligation at a site peripheral to the takeoff of the superior gluteal artery. Skinner 7 and Andriole and Sugarbaker 11 also r e c o m m e n d e d ligation at the point b e l o w the takeoff of the superior gluteal artery, but their reasons w e r e to prevent perineal necrosis and hip ctaudication, and differ from our own. Based on our findings, although ligation b e l o w the takeoff of the superior gluteal artery has a considerable bloodflow-reducing effect on the pelvic organs, caution is necessary in patients whose collateral circulation is inadequate because of irradiation or severe arteriosclerosis; it might give rise to serious complications in the bladder, uterus, and vagina.
