Right Colonic Arterial Anatomy Implications for Laparoscopic Surgery Antonio Garcia-Ruiz, M.D., Jeffrey W. Milsom, M.D., Kirk A. Ludwig, M.D., Pierenrico Marchesa, M.D.

From the Colorectal Surgery Research Unit, Colorectal Surgery Department, The Cleveland Clinic Foundation, Cleveland, Ohio

PURPOSE: Hemorrhagic complications can be a major cause of conversion and/or morbidity during laparoscopic intesti- nal surgery. The limited exposure currently provided in laparoscopic intestinal resection demands a precise knowl- edge of mesenteric vascular anatomy to avoid such compli- cations and to expedite the procedure. Most surgical texts depict a "normal pattern" of arterial supply to the right colon consisting of three arterial branches (ileocolic artery, right colic artery, and middle colic artery) arising indepen- dently from the superior mesenteric artery (SMA). Based on previous reports and clinical observations, we hypothesized that the right colic artery arises infrequently from the SMA, and most commonly, there are only two colonic arteries arising independently from the SMA. METHODS: We per- formed detailed dissections of the SMA in 56 human cadav- ers. RESULTS: We found the ileocolic artery in all of our cases and the middle colic artery in 55 of 56 cadavers but only six cases of a right colic artery emanating directly from SMA. CONCLUSIONS: Our data, combined with review of published anatomic studies, lead us to conclude that in the vast majority of cases there are only two independent branches arising from SMA that supply the large intestine, the ileocolic and the middle colic arteries. The right colic artery directly arising from SMA is unusual (10.7 percent). This knowledge may help lower the risk of vascular com- plications during laparoscopic intestinal surgery. [Key words: Anatomy; Colectomy; Dissection; Intraoperative complications; Laparoscopy; Surgery, Laparoscopic]

Garcla-Ruiz A, Milsom JW, Ludwig KA, Marchesa P. Right colonic arterial anatomy: implications for laparoscopic sur- gery. Dis Colon Rectum 1996;39:906-911.

I ncorpora t ion of laparoscopic techniques into the

gastrointestinal surgeon 's a rmamentar ium has led

to a renewal in the interest in the ana tomy of mesen-

teric arteries. Colonic resections have b e c o m e com-

m o n procedures using laparoscopic techniques, 1-1~

and inability to palpate vessels, coup led with use of

techniques that ligate these "mesenteric vessels" in- tracorporeally, 1>13 requires a t ho rough k n o w l e d g e of mesenter ic anatomy. 14-16 Ana t om y of mesenter ic ar-

teries is also important w h e n an intestinal resection

Poster presentation at the meeting of The American Society of Colon and Rectal Surgeons, Montreal, Quebec, Canada, May 7 to 12, 1995. Address reprint requests to Dr. Milsom: Department of Colorectal Surgery/All1, The Cleveland CIinic Foundation, 9500 Euclid Ave- nue, Cleveland, Ohio 44195.

for cancer is per formed (i.e., with proximal vascular ligation and wide en bloc resection). 1' 14-21

Not all authors agree on wha t defines the normal colonic vascular anatomy. 22' 23 This lack of ag reement

brings not only cont roversy but also confusion. Con-

sequences of this confus ion may potentially lead to

surgical complications.

LITERATURE REVIEW

Mthough references dated earlier than the 16th century mention "meseraic vessels," the anatomy is not expla ined precisely. 24-3~ Historically, French anat-

omist Jean Riolan (1580-1657) supposed ly wrote the

first anatomic treatise in which co lon vascularity was descr ibed in detail. 19' 28 Nevertheless, in searching

th rough his texts, 31 w e did not find any reference to a

particular colic artery or to the intermesenteric arcade

actually n a m e d after him.

Perhaps the first anatomist w h o descr ibed the

branches of the superior mesenter ic artery (SMA) was

Bar to lomeo Eustachi (circa 1500-1574). He depic ted

them with particular detail when , in 1552, he pre-

pared a series of anatomic illustrations (Fig. 1). Un-

fortunately, he died before publ ishing his anatomic

work. His texts are lost, but his magnificent illustra-

tions survived to be printed and credited later, in a

text made by Giovanni Maria Lancisi, in 1714.24, 28, 32, 33

During the 17th and 18th centuries, anatomic de- scriptions proliferated, 28' 29, 34, 35 and a concep t of a

normal pat tern appea red for the colonic b lood sup-

ply. It consisted o f three colic arteries (middle, right,

and ileocolic) arising f rom the SMA and two or more

colic arteries (left and sigmoidal) arising f rom the

inferior mesenter ic artery. It was not until the 19th

century, especially w h e n abdomina l surgery began to develop, that scientific and technical advances led to

the apprecia t ion of wide variations in mesenter ic cir- culation.26, 36 Nevertheless, interest in these variations

was simply anatomic curiosity because surgeons ' at-

906

Vol. 39, No. 8 RIGHT COLONIC ARTERIAL ANATOMY 907

Figure 1. Eustachian anatomic illustration showing, per- haps for the first time, the superior mesenteric vessels, divisions, and mesenteric lymph nodes in detail. The middle colic artery and ileocolic artery are correctly drawn. A right colic branch is depicted emanating from the ileocolic artery. An accessory middle colic (directed to the splenic flexure) is present.

tention was primarily focused on avoidance of infec- tious complications.

As the field of intestinal surgery advanced, over the

present century, challenge of performing more com-

plex resections and anastomoses highlighted the pres-

ence of vascular variants. This brought more detailed and careful anatomic studies. 18'19'37-39 Several of

them form the basis of our current anatomic concepts on blood supply to the colon. However, the old per-

ception of a normal pattern (by definition the most

frequently found) persisted unchanged in general terms (Fig. 2). Even today, despite recent anatomic and surgical studies 23' 40-43 that widely emphasize the

mistake, most medical textbooks still accept as a nor-

mal pattern of the colonic vasculature one that we believe is an infrequent variant. 44-56 Whenever vari-

ants were considered, their incidence was referred to without specifying its origin 52' 550r with vague terms such as "usually, ''46' 49 ,,frequently,,,5s, 54 or "often, ''48

which lead to nothing but an unclear image of colonic vasculariW. In reviewing extensive literature devoted to the variable colonic blood supply, we have found many discrepancies.

Figure 2. Illustration of the so-called normal pattern for the colonic blood supply. This concept has prevailed despite evidence supporting that it is infrequent (10.7 percent in our series). (Permission for this figure was granted by Springer Verlag Inc., 175 Fifth Avenue, New York, New York 10010.)

N O M E N C L A T U R E

Despite multiple efforts to unify anatomic terms,18, 22, 23 a controversy persists about colic arter-

ies. There is no uniform terminology. For many au-

thors, a colic artery is named independent of its ori- gin.18, 19, 38 For other studies 23 (including ours), the

name "colic artery" has been reserved for those with

an independent origin from the superior or inferior

mesenteric arteries. Otherwise, the vessel should be

called "colic branch." This issue is mostly semantic in character, and settling the controversy is beyond the

scope of this article. However, for the purposes of this

study, a named artery to the right colon arises directly from the SMA. Thus, our main endpoint was to define

h o w many colic vessels originated from the superior mesenteric vessels and to assess the precise location of their origin.

METHODS

We studied the anatomy of the SMA and its colonic branches by careful dissection in 56 adult cadavers.

Our main focus was the pattern of branching of the SMA close to the root of the mesentery, specifically

studying the right colonic arterial pedicles up to the point at which they anastomose to the marginal ar- tery. Our 56 dissections were performed in situ (in the abdomen) in nonselected cadavers. The only exclu- sion criteria were the inability to recognize the anat-

908

omy because of previous surgery or intra-abdominal pathology. We did no radiologic or perfusion study. All dissections were per formed by the same team of

surgeons, using standard surgical scissors, forceps, and other simple dissection tools. After xiphoid to

pubis midline laparotomy and careful inspection of intra-abdominal organs, the small bowel was dis-

placed laterocaudally and the transverse colon ceph-

alad, giving access to the right aspect of the mesen-

teric root. A transverse incision was made in the

per i toneum to identify and isolate the proximal por- tion of the superior mesentedc vein and artery. Dis- section was then continued first caudally and then

cephalad, following the path of the superior mesen-

teric vessels, identifying all primary divisions until anastomoses to the colonic marginal artery (Drum-

mond's) and vein. Fourteen cadavers were made available to us by the

Education Department and 5 at the Pathology Depart-

ment of Cleveland Clinic Foundation, Cleveland,

Ohio, 6 at the Depar tamento de Investigaci6n y

Ensefianza, Hospital Central Militar, M~xico City, and 31 at the Anatomy Department of the Case Western Reserve University, Cleveland, Ohio, during a one-

year period. All corpses were either bequested or

considered unclaimed according to federal regula- tions. Detailed descriptions and sketches of spatial

relations of SMA and vein and colonic branches were

recorded. This information allowed us to establish the most frequent pattern of vascular supply to the right

colon, that is, the normal pattern and its many varia-

tions.

RESULTS

Of 56 adult cadavers, 29 were male and 27 were

female. None of them was discarded from the study because of abdominal surgery or pathology.

Incidence of each particular artery in our series,

compared with other anatomic series, is shown in

Table 1. The ileocolic artery was constantly present, and incidence of right colic artery was extremely low in our study. Blood supply to the ascending colon

was mostly from a branch emanating from the ileo-

colic artery (66 percent), the middle colic artery (23.3 percen0, or, infrequently (10.7 percent), a direct branch from the SMA as the right colic artery. Thus, as we stated earlier, in the case in which the origin of that vessel was not the SMA, the right colic artery was considered absent and in its place was noted a right colic branch coming from the ileocolic or middle colic

GARCiA-RUIZ ETAL Dis Colon Rectum, August 1996

Table 1. Incidence of Colic Arteries Arising from Superior

Mesenteric Artery* (Literature Review)

Ileocolic Author Year n

Artery

Right Middle Colic Colic Artery Artery

Sonneland et aL ~8 1958 600 100 29 96 Steward and 1933 40 100 40 95

Rankin ~9 VanDamme and 1990 156 100 13 99

Bonte 23 Basmajian 3z 1955 45 100 38 82 Jamieson and 1909 23 100 ? ?

Dobson 39 Michels 42 1965 400 100 38 78 Nelson et aL43 1988 50 100 34 97 Present study 1996 56 100 10.7 98.2

* Values noted are percentages.

Table 2. No. of Colic Arteries Arising from Superior Mesenteric

Artery* (Literature Review)

Author Year n l 2 3 4

S o n n e l a n d e t a l . 18 1958 600 1.8 66.6 30.9 1.2 Steward and 1933 40 ? 60 ? ?

Rankin 19 Basmajian 3z 1955 45 0 64.4 31.1 4.5 Jamieson and 1909 23 ? >50 <50 ?

Dobson 39 Present study 1996 56 0 89.3 10.7 0

* Values noted are percentages.

artery. Regarding the middle colic artery, its presence was recorded in 98.2 percent of cadavers. When

present, it was a single artery in 94.6 percent and double in 3.6 percent of the series (in both cases, the right colic artery was absent). We found two cases of anomalous origin for the middle colic artery: in one of

them, the only artery supplying the transverse colon had its origin from the hepatic artery. Its path came along with the SMA through the groove behind the

neck of the pancreas. The other case was an acces-

sory middle colic artery, arising from the distal portion of the splenic artery and directed to the splenic flex- ure. The middle colic artery was absent in only one of

our dissections. In this case, we found the right colon artery present. Although reported in some other se- ries, we did not find any other variant arrangement of

the middle colic artery. Comparative analysis of the total number of colonic

arterial pedicles arising directly from the SMA are summarized in Table 2. These data were not discern- ible in some other reports to which we have referred.

Vol. 39, No. 8 RIGHT COLONIC ARTERIAL ANATOMY

We found no case with only one arterial pedicle

(ileocolic artery) supplying the right half of the colon.

In our series, the vast majority (89.3 percent) had two

colonic arterial pedicles originating from the SMA (Fig. 3); only 10.7 percent had three. There were no cases, in our study, in which the SMA had more than three colonic pedicles.

Average lengths of colonic pedicles (distance from its origin to its first point of branching) arising from

SMA are in Table 3. Ileocolic artery was nearly twice as long as right and middle colic vessels.

Finally, an intermesenteric Riolan's arcade is de-

fined as an arterial branch proximal to the marginal

artery, which arises from the left side of the middle

colic artery, travels shortly to the left through the

mesentery of the transverse colon, and then turns caudally through the retroperi toneum to anastomose to the ascending branch of the left colic artery or the

inferior mesenteric artery. Incidence of Riolan's ar- cade has been reported in up to 12 percent 23 but was

not present in any of our cases.

D I S C U S S I O N

Our study showed some similarities with other

large anatomic series that describe the variant anat- omy of the SMA. A c o m m o n finding in previous re-

ports, and in our own, is the abundance of variants

Figure 3. Arterial arrangement of the colic arteries arising from superior mesenteric arteries in 89.3 percent (left figure) and 10.7 percent (right figure) of our 56 dissec- tions. (Permission for this figure was granted by Springer Verlag Inc., 175 Fifth Avenue, New York, New York 10010.)

Table 3. Length of Colic Arteries Arising from Superior

Mesenteric Artery

909

Artery Length Before Branching

Mean in mm Mean in mm

Middle colic 32.8 3-70 Right colic 45.2 20-70 Ileocolic 67.4 20-120

and the rather uncommon occurrence of the so-called

normal pattern found in most surgical textbooks.

This classic description showing the right colic ar- tery as a direct branch of the SMA was found by

Sonneland e t al. 18 in 23.8 percent of 600 cadavers and in a 38 percent of 200 by Michaels. 41 Our report of

10.7 percent was similar to that of VanDamme and Bonte 23 (13 percent).

Although most surgeons are aware of vascular vari- ations in the mesentery, the inaccurate portrayal of

the commones t form of right colonic blood supply has likely propagated misunderstandings of the true

normal pattern. The spreading of this misconception is likely because most of these anatomic studies were issued before 196018' 19, 37-39 or had been published in

anatomic magazines 43 (not widely available) or highly specialized books 23' 42, 57, 58 with titles more attractive

to vascular surgeons and anatomists than to general or colorectal surgeons. An actual need for a detailed

understanding of these variants may not be necessary in conventional right colon surgery, because these

vessels are generally grasped, clamped, and ligated

within their mesentery without any real need to ac- curately identify them.

Discrepancies be tween authors ( i .e . , incidence of

right colic artery ranges from 10.7-40. percent) could be attributed to semantic matters. 23 However, there is

no doubt that the number of arteries to the right colon arising independently from the SMA is, in most cases,

only two (namely middle colic and ileocolic arteries), instead of three as typically depicted.

What is the current clinical interest of these ana-

tomic findings? During laparoscopic colon surgery,

these vessels must be isolated without the possibility of direct palpation. By using our technique of right hemicolectomy,15, 16 we make a proximal ligation of

the mesenteric vessels before colon mobilization, so

we must anticipate where arteries branch from the SMA. Furthermore, we have to take into account that the extent of resection for colon cancer is determined by the necessity for wide excision of not just the

910

tumor but also the lymphatics that accompany the main colic arteries supplying the involved seg- ment.2,, 44, 59 This entails ligation of the appropriate

colic arteries at their origin in the SMA. 1' s5, 20 There-

fore, arterial supply to the specific segment of colon

being operated on must be identified and ligated

proximally to offer the patient, according to our cur-

rent practice, the best possible "oncologic" operation.

Variants involving colic arteries are also of clinical

importance when a vascular pedicle will determine

the segment of the colon to be used for replacing the

esophagus or the bladder. 6~ Operations that require

incision of the supposed avascular area of the trans-

verse mesocolon, like retrocolic anastomoses (where

a variant middle colic artery could be injured) also

require an understanding of some fine points of mes- enteric vascular anatomy. 49-53 Although bleeding

caused by injuring such variant vessels may be trou-

blesome, sometimes clamping with an instrument,

either conventional or laparoscopic, in a hurried way

could lead to further damage instead of hemostasis. 61

C O N C L U S I O N S

In the vast majority (89.3 percent) of cases in our

study, only two colonic arterial pedicles arose indepen-

dently from the SMA. The right colic artery is an uncom-

mon branch (10.7 percent) of the SMA. The ileocolic

artery is the only constant branch of the SMA to the right

half of the colon. A detailed knowledge of the right and

transverse coloNc blood supply and its many variations

may be of benefit when performing a safe and efficient

laparoscopic (or conventional) right colon surgery.

A C K N O W L E D G M E N T S

The authors thank the Historical Division, Cleve-

land Health Sciences Library, and the Department of

Anatomy, Case Western Reserve University Medical

School, for devoted and invaluable cooperation with

our Research Unit during this project.

REFERENCES

1. Davis MD, Ballantyne GH. Colorectal cancer. In: Ballan- tyne GH, Leahy PF, Madlin IM, eds. Laparoscopic surgery. Philadelphia: WB Saunders, 1994:233-56.

2. Dean PA, Beart RWJr, Nelson H, Elftmann TD, Schlinkert RT. Laparoscopic-assisted segmental colectomy: early Mayo Clinic experience. Mayo Clin Proc 1994;69:834-40.

3. Elf*mann TD, Nelson H, Ota DM, Pemberton JH, Beart RW. Laparoscopic-assisted segmental colectomy: surgi- cal techniques. Mayo Clin Proc 1994;69:825-33.

GARCiA-RUIZ E T A L Dis Colon Rectum, August 1996

4. Falk PM, Beart RW, Wexner SD, e t al. Laparoscopic colectomy: a critical appraisal. Dis Colon Rectum 1993; 36:28--34.

5. Franklin ME, Rosenthal D, Norem RF. Prospective eval- uation of laparoscopic colon resection v e r s u s open co- lon resection for carcinoma. Surg Endosc 1995;9:811-6.

6. Monson JR, Darzi A, Carey PD, Guillou PJ. Prospective evaluation of laparoscopic-assisted colectomy in an un- selected group of patients. Lancet 1992;340:831-3.

7. Ortega AE, Beart RW Jr, Steele GD Jr, Winchester DP, Greene FL. Laparoscopic bowel surgery registry: pre- liminary results. Dis Colon Rectum 1995;38:681-6.

8. Peters RW, Barrels TL. Minimally invasive colectomy: are the potential benefits realized? Dis Colon Rectum 1993;36:751-6.

9. Plasencia G, Jacobs M, Verdeja JC, Viamonte MIII. Laparoscopic-assisted sigmoid colectomy and low an- terior resection. Dis Colon Rectum 1994;37:829-33.

10. Senagore AJ, Luchtefeld MA, MackeiganJM, Mazier WP. Open colectomy v e r s u s laparoscopic colectomy: are there differences? Am Surg 1993;59:549-54.

11. Monson JR, Guillou PJ. Complications of laparoscopic surgery for cancer and their avoidance. Surg Clin North Am 1994;3:745-758.

12. Phillips EH, Franklin M, Carroll BJ, Fallas MJ, Ramos R, Rosenthat D. Laparoscopic colectomy. Ann Surg 1992; 216:703-7.

13. Wexner SD, Johansen OB, Nogueras JJ, Jagelman DG. Laparoscopic total abdominal colectomy: a prospective trial. Dis Colon Rectum 1992;35:651-5.

14. Decanini C, Milsom JW, Bohm B, Fazio VW. Laparo- scopic oncologic abominoperineal resection. Dis Colon Rectum 1994;37:552-8.

15. Milsom JW, Bohm B, Decanini C, Fazio VW. Laparo- scopic oncologic proctosigmoidectomy with low colo- rectal anastomosis in a cadaver Model. Surg Endosc 1994;8:1117-23.

16. Milsom JW, Lavery IC, Church JM, Stolfi VM, Fazio VW. Use of laparoscopic techniques in colorectal surgery: preliminary study. Dis Colon Rectum 1994;37:215--8.

17. Mayo CW. Blood supply of the colon: surgical consid- erations. Surg Clin North Am 1955;35:1117-22.

18. SonnelandJ, Anson BJ, Beaton LE. Surgical anatomy of the arterial supply to the colon from the superior mes- enteric artery based upon a study of 600 specimens. Surg Gynecol Obstet 1958;106:385-98.

19. Steward JA, Rankin FW. Blood supply of the large intes- tine: its surgical considerations. Arch Surg 1933;26:843-91.

20. Surtees P, Ritchie JK, Phillips RK. High v e r s u s low liga- tion of the inferior mesenteric artery in rectal cancer. Br J Surg 1990;77:618-21.

21. Turnbull RB, Kyle K, Watson FR, Spratt J. Cancer: the influence of the no-touch isolation technique on sur- vival rates. Ann Surg 1967;166:420-5.

22. International Anatomical Nomenclature Committee.

Vol. 39, No. 8

Nomina anatomica. 5th ed. Baltimore: Williams & Wilkins, 1983.

23. VanDamme JP, Bonte J. Vascular anatomy in abdominal surgery. Germany: ThiemeMedical Publishers, 1990.

24. Choulant L. History and bibliography of anatomic illus- tration. Translated by M. Frank. Chicago: The University of Chicago Press, 1920.

25. Harris CR. The heart and the vascular system in ancient Greek medicine. London: Oxford, 1973.

26. Leonardo RA. History of surgery. New York: Froben Press, 1943.

27. Saunders JB, O'Malley CD. The illustrations from the works of Andreas Vesalius. Cleveland: World Publish- ing, 1950.

28. Singer C. A short history of anatomy from the Greeks to Harvey: the evolution of anatomy. New York: Dover Publications, 1957.

29. Singer C. The evolution of anatomy. London: Kegan Paul, Trench, Trubner, 1925.

30. Willius F, Dry T. A history of the heart end the circula- tion. Philadelphia: WB Saunders, 1948.

31. Riolan J. A sure guide or, the best and nearest way to physick and chyrurgery: that is to say, the arts of healing by medicine, and manual operation. Translated by N. Culpeper and V. Rand. London: Peter Cole, 1657.

32. Gillispie CC. Dictionary of scientific biography. New York: Charles Scribner's Sons, 1975.

33. Lancisi JM. Tabulae anatomicae Bartholomaei Eustachii, quas e tenebris tandem vindicatas . . . . praefatione nos- tique illustrativ ac publici juris fecit Jo. Maria Lancisius. Rome: Laurentii & Thoma. Plagiarini Bibliopol, 1728.

34. Goddard PB. Plates of the arteries with references; for the use of medical students. Philadelphia: TK & PG Collins, 1839.

35. Quain R. The anatomy of the arteries of the human body and its applications to pathology and operative surgery. London: Taylor and Walton, 1844.

36. Rutkow IM. Surgery: an illustrated history. St. Louis: Mosby-Year Book, 1993.

37. Basmajian JV. The main arteries of the large intestine. Surg Gynecol Obstet 1955;101:585-91.

38. Jamieson JK, Dobson JF. The lymphatics of the colon. J R Soc Med 1909;2:149-74.

39. Jamieson JK, Dobson JF. The lymphatics of the colon. Ann Surg 1909;50:1077-90.

40. Kornblith PL, Boley SJ, Whitehouse BS. Anatomy of the splachnic circulation. Surg Clin North Am 1992;72:1-30.

41. Michels NA. Blood supply and anatomy of the upper abdominal organs. Philadelphia: Lippincott, 1955.

42. Michels NA, Siddharth P, Kornblith PL, Parke WW. The variant blood supply to the descending colon, rectosig- moid and rectum based on 400 dissections. Its impor- tance in regional dissections: a review of medical liter- ature. Dis Colon Rectum 1965;8:251-78.

RIGHT COLONIC ARTERIAL ANATOMY 911

43. Nelson TM, Pollak R, Jonasson O, Abcarian H. Ana- tomic variants of the celiac, superior mesenteric, and

inferior mesenteric arteries and their clinical relevance. Clin Anat 1988;1:75-91.

44. Goligher J, Duthie H, Nixon H. Surgery of the anus, rectum and colon. 5th ed. London: Bailliere Tindall, 1984.

45. Gordon PH, Nivatvongs S. Principles and practice of surgery for the colon, rectum and anus. St. Louis: Qual- ity Medical Publishing, 1992.

46. Hollinshead WH. Anatomy for surgeons. 2rid ed. New York: Harper & Row, 1971.

47. Keighley MR, Williams NS. Surgery of the anus, rectum and colon. Philadelphia: WB Saunders, 1993.

48. Williamson RC, Mortensen NJ. Anatomy of the large intestine. In: Kirsner JB, Shorter RG, eds. Diseases of the colon, rectum and anal canal. Baltimore: Williams & Wilkins, 1988:1-22.

49. Nora PF. Operative surgery: principles and techniques. 3rd ed. Philadelphia: WB Saunders, 1990.

50. Roslyn JJ, Zinner MJ. The biological basis of modern surgical practice. In: Sabiston DC. Textbook of surgery. 14th ed. Philadelphia: WB Saunders, 1991:899-903.

51. Ellis H. Resection of the colon. In: Schwartz SI, Ellis H. Maingot's abdominal operations. 9th ed. Norwalk: Appleton & Lange, 1989:1049-75.

52. Kodner IJ, FI T RD, FleshmanJW, Bimbaum EH. Colon, rectum and anus. In: Schwartz SI, Shires GT, Spencer FC. Principles of surgery. 6th ed. New York: McGraw- Hill, 1994:1191-306.

53. Skandalakis JE, Gray SW, Rowe JS. Anatomical complica- tions in general surgery. New York: McGraw-Hill, 1983.

54. Thorek P. Anatomy in surgery. 3rd ed. New York: Springer-Verlag, 1985.

55. Williams PL, Warwick R. Gray's anatomy. 36th ed. Phil- adelphia: WB Saunders, 1980.

56. Romolo JL. Embryology and anatomy of the colon. In: Zuidema GD. Shackelford's surgery of the alimentary tract. 3rd ed. Philadelphia: WB Saunders, 1991:3-15.

57. Marston A. Vascular disease of the gastrointestinal tract: pathophysiology, recognition and management. Balti- more: Williams & Wilkins, 1986.

58. Zerin JM, DiPietro MA. Mesenteric vascular anatomy at CT: normal and abnormal appearances. Radiology

1991;179:739-42. 59. Toyota S, Ohta H, Anazawa S. Rationale for extent of

lymph node dissection for right colon cancer. Dis Colon Rectum 1995;38:705-11.

60. Ventemiglia R, Khalil KG, Frazier OH, Mountain CF. The role of preoperative mesenteric arteriography in colon interposition. J Thorac Cardiovasc Surg 1977;74:98-104.

61. Nordestgaard AG, Bodily KC, Osborne RW, ButtorffJD. Major vascular injuries during laparoscopic procedures. Am J Surg 1995;169:543-5.