Superior By Michael
Mesenteric
L. Ritchey,
Artery Injury During Nephrectomy for Wilms’ Tumor
Kevin P. Lally, Gerald
M. Haase,
Stephen
J. Shochat,
and Panayotis
P. Kelalis
Lackland AFB, Texas; Denver, Colorado; Stanford, California; and Rochester, Minnesota l latrogenic injury to the aorta or its major branches during nephrectomy for Wilms’ tumor in children is rarefy reported but may be more common than is currently acknowledged. We identified four patients with ligation of the superior mesenteric artery (SMA) that occurred during nephrectomy for nephroblastoma and another child in whom SMA thrombosis developed postoperatively. All of the tumors were on the left side. Interruption of the SMA was recognized intraoperatively in all four children, and primary repair was done. In three patients, appearance of the bowel remained normal before repair of the injury. Three of the arteries were repaired by primary reanastomosis, and one was joined with an interpositioned hypogastric artery graft. None of these patients had gastrointestinal complications postoperatively. In the fifth patient, SMA thrombosis developed after repair of an aortic tear during nephrectomy. This patient required subsequent small bowel resection for bowel infarction and died in the perioperative period. Every surgeon treating children with Wilms’ tumor should be aware of the possibly distorted vascular anatomy and take precautions to avoid such a significant injury. Attempts at early ligation of the vessels may not be justified until the renal vasculature is clearly identified.
MATERIALS
AND
METHODS
3 instances 1 of
a 3-year-old
a
14-cm a transverse
Copyright o 1992 by W.B. Saunders Company INDEX WORDS: Wilms’tumor, nephrectomy; cations, superior mesenteric artery injury.
surgical compli-
I
ATROGENIC injury to the aorta or its major branches during nephrectomy for Wilms’ tumor in children has rarely been reported.1*2 Identification of the major visceral arteries is essential in the surgical management of these large childhood renal masses. Recent experience with a superior mesenteric artery (SMA) injury during removal of a large Wilms’ tumor prompted a review of this problem. In this report, the recognition and management of SMA injuries in children are addressed. From the Departments of Urology and Pediatric Surgery, ryirford Hall USAF Medical Center, Lackland AFB, TX; fhe Department of Pediatric Surgery, The Children’s Hospital, Denver, CO; the Division of Pediatric Surgery, Stanford University Medical Center, Stanford, CA; and the Department of Urology, Mayo Clinic and Mayo Foundation, Rochester, MN. Date accepted: January 21,199l. Supported in part by Research Grant CA-42324 from the National Institutes of Health. Principal investigators at participating institutions also received support from the National Cancer Institute. The opinions expressed herein are those of the authors and do not necessan’ly reflect the views of the United States Air Force. Address reprint requests to Panayotis P. Kelalis, MD, Depatiment of Urology, Mayo Clinic, 200 First St SW, Rochester, MN 55905. Copyright 8
612
6 months a 2-year-old 12-cm a transverse A vessel
A 32-month-old a lo-cm a transverse
a pulse
5 (May),
a
SUPERIOR MESENTERIC
ARTERY INJURY
The child had no complications in the postoperative period. Chemotherapy was started on postoperative day 3, but radiation to the left flank with 10 Gy given over 9 days was delayed until postoperative day 30 because of concerns about irradiation of the vascular anastomosis. The patient had no evidence of disease at &month follow-up, and no disturbances of bowel function were reported. Case 4, A 14-cm renal mass was removed from a 28-month-old girl through a transverse abdominal incision. The renal hilum was approached early. After nephrectomy was completed, it was noted that the SMA had been interrupted, but there had been no change in bowel color. The SMA was repaired with a hypogastric artery graft positioned between the cut ends of the SMA. There were no postoperative complications. However, arteriography performed on postoperative day 2 showed that the graft was not patent. No further intervention was done for the vascular occlusion, because the patient was doing well. The patient was taking a regular diet on postoperative day 4, and chemotherapy was begun on postoperative day 7. Radiation therapy was not given. The patient had no evidence of disease at U-month follow-up and was asymptomatic. Case 5. Preoperative evaluation in a 5-year-old girl with gross hematuria and a 14-cm left renal mass showed that she had pulmonary involvement. Radical nephrectomy was performed through a transverse abdominal incision. The aorta and left renal vein were identified early, and the tumor was removed. After removal of the kidney, gross residual tumor remained adjacent to the aorta. In an attempt to remove the residual tumor, the aorta was injured, requiring repair with a Gore-Tex patch. The suprarenal portion of the aorta was compressed for over 1 hour during this procedure. The bowel showed good color at the end of the operation. Postoperatively. the patient had persistent ileus and later became febrile, with increased abdominal distention. Exploratoly surgery was performed on postoperative day 6, and she was found to have a bowel infarction with thrombosis of the SMA. The infarcted bowel was resected, but the artery was not repaired. The patient died of sepsis 3 days later.
613
30% to 50%.4-6 The poor survival is due to several factors, including delay in treatment, multiple associated injuries, and simultaneous venous damage. The safe period of intestinal ischemia in humans is unknown but is probably less than 12 hours.6 Degree of collateral circulation, hypotension, and any associated venous injury will alter the length of this safe interval. FulIen et al4 attempted to classify SMA injuries by anatomic zones and physiological grades of ischemia (Fig 1). Zone 1 is that portion of the SMA proximal to the first major branch; zone 2 is the segment between the inferior pancreaticoduodenal and middle colic arteries; zone 3 is the segment distal to the middle colic artery; and zone 4 involves the segmental branches. Injuries in zones 3 and 4 may produce no ischemia or ischemia of a small segment of bowel. Lucas et al6 also suggested that lesions distal to the first jejunal branch can be safely ligated but that injuries proximal to the first jejunal branch require repair. However, there is great variability in the degree of ischemia produced at a given level of injury. These recommendations presume patency of the inferior mesenteric artery. Simultaneous ligation of both the SMA and the inferior mesenteric artery is contraindicated.’ An understanding of the normal anatomy of the
DISCUSSION
The factors that predisposed these children to SMA injury were analyzed. These children were all 5 years old or younger, the peak age range for nephroblastoma. The aorta and its branches are quite small at this age, allowing them to be mistaken for the renal artery. Of importance, all of these tumors were on the left side, and the aorta and its branches are in close proximity to these left-sided lesions. The renal masses can be very large relative to the size of the child. Resultant distortion of the bowel mesentery draped over the tumor can cause further difficulty in identifying the anatomy. Although four of the patients had a renal vein thrombus, in only one case was this apparent at the time of surgery. In this child, extensive local tumor advancement also accounted for the difficult hilar dissection. None of the other operative notes described any major difficulty with intraoperative bleeding or hilar invasion that might have caused difficulty in identifying the hilar vessels. Most clinical reports on treatment of SMA injuries involve trauma patients. The injuries are uncommon, but the mortality in most series is high, ranging from
Fig 1. Artist’s conception of superior mesentaric artery circulation, showing the classification by anatomic zones. A, aorta; IPD, inferior pancreaticoduodenal artery; R col, right colic; Jejun, jejunal. (Reprinted with permission of Williams &Wilkins Co.‘)
614
intestinal blood supply is necessary to identify those areas that are critical to maintaining the viability of the bowel. The intestines are protected from ischemia by an abundant collateral circulation that can vary enormously in distribution from one person to another.s Collateral pathways open immediately when a major vessel is occluded. The reduction in blood flow that the bowel can tolerate without damage is remarkable. Boley et al9 showed that a reduction in blood flow of more than 75% is necessary to induce morphologic changes in the bowel. Lillehei et allo found that 7 of 10 mongrel dogs they studied tolerated up to 3 hours of complete SMA occlusion if the collateral circulation to the small bowel was not disturbed. If all collateral circulation was occluded, only 1 of 10 dogs survived after 3 hours of occlusion of the SMA. Complete ligation of the venous drainage of the bowel is tolerated even less well than arterial occlusion.” Operative determination of intestinal viability can be difficult. The clinical criteria of bowel color, arterial pulsations, and intestinal peristalsis can be misleading.12 The intestine may seem viable by serosal appearance at the initial operation, but later fullthickness necrosis develops. Likewise, unnecessary resection of bowel may be performed on the basis of clinical criteria alone. Intraoperatively, the viabiIity of the intestine can be assessed by several additional techniques: fluorescent indication testing,r2 Doppler flow study,13 and measurement of the postresection mean pressure of the distal arterial stump.14 For an intraoperative injury, these steps indicate whether the bowel is viable through collateral blood supply. The difficulty in the clinical assessment of bowel viability (for example, normal serosal appearance) may also impair the detection of a vascular injury. The frequency of SMA injury in this series of patients is low, but its incidence could well be underestimated. The lack of relevant signs and symptoms during and after surgery could easily lead to nonrecognition. After ligation of the SMA, three of the children reported here did not have ischemic-appearing bowe1 prior to repair of the injury. This result may be due in part to the short interval from the time of injury to discovery, since four of our patients were identified by the intraoperative finding of a ligated mesenteric vessel. The lack of clinical findings in three of the cases could also be the result of ligation of the SMA in zone 3 or 4, as described by Fullen et a1.4The level of SMA ligation was not clearly stated in any of the operative notes. Inadvertent ligation might be expected to occur more distally because of the displacement of the mesenteric vessels away from the aorta by a large renal mass crossing the midline. Ligation of a
RITCHEY ET AL
more distal segment could result in minimal or no ischemia. The operative management of the SMA injury is dictated to a large measure by the type of injury. Primary end-to-end anastomosis was used in two of the patients. In another child, the cut end of the SMA was attached end to side to the aorta. It may be difficult to mobilize the SMA to obtain additional length because of the multiple branches in its proximal portion. Nonmobilization can make it difficult to accomplish a repair without tension. An interposition graft may be needed if there is not enough length for a primary reanastomosis. Simple ligation should be considered for only the more distal injuries (zone 4) or if clinical circumstances preclude vascular repair. Despite the admonition that SMA ligation is not well tolerated in the child (because of inadequate collateral circulation),7 there were no adverse clinical effects in case 4 in this series even though occlusion of the SMA repair was found on postoperative day 2. The clinical outcome after repair of these intraoperative injuries was better than might be expected. This may be accounted for by the absence of any venous injuries. Acute bowel complications, such as ileus or bowel loss, did not develop in any of our patients with an intraoperative diagnosis of SMA ligation. Only in the patient with SMA thrombosis did bowel infarction develop, probably because of occlusion of the proximal segment of the SMA and the long interval before discovery of the injury. The potential for SMA injury should be kept in mind during excision of all left-sided Wilms’ tumors. Prevention of this complication requires careful identification of the aorta and its branches. One cannot assume that all vessels in the region of the renal hilum are supplying the kidney. The mesenteric vessels can be quite adherent to the mass and appear to enter the kidney. The renal artery should be traced to the kidney to ensure its destination. This can be accomplished only by proper surgical exposure. One maneuver that may be helpful involves incising the posterior peritoneum from the base of the cecum to the ligament of Treitz. This allows one to elevate the right colon and small bowel out of the abdomen and provides excellent visualization of the aorta and the SMA. If exposure is limited, attempts at early ligation of the vessels may not be justified until the renal vasculature is clearly identified. Previous reports from the National Wilms’ Tumor Study have shown that early ligation of the renal vessels has no effect on ultimate outcome.15 In some cases, mobilization of the tumor may be necessary to allow precise identification of the renal vessels. In addition, if there is significant local extension preventing an adequate
SUPERIOR MESENTERIC
615
ARTERY INJURY
and accurate dissection, consideration should be given to adjuvant chemotherapy or radiation therapy (or both) and delayed nephrectomy after tumor shrinkage. One specific issue that must be addressed in children with Wilms’ tumor who incur SMA injuries is the effect of subsequent abdominal irradiation. Treatment of one patient was postponed for 1 month because irradiating the arterial repair caused concern. There are reports of radiation-induced vascular injury after radiotherapy in childhood.r6J7 Changes in the artery indistinguishable from atherosclerosis have
been reported.ls Fonkalsrud et all9 irradiated the femoral arteries in dogs with 40 Gy in 10 fractions given over 10 days. They found both acute endothelial injury and chronic changes of the vessel wall. The vessel becomes prone to stenosis from intimal thickening and periadventitial fibrosis. No reports are available on the effects of radiotherapy on newly created vascular anastomoses. Three of the five children in the present study received postoperative abdominal radiation. The dose ranged from 12 to 20 Gy, and none of these children was noted to have any adverse side effects due to the irradiation.
REFERENCES 1. Ehrlich RM: Complications of Wilms’ tumor surgery. Ural Clin North Am 10:399-406,1983 2. Rickham PP: Malignant tumours involving the genitourinary system in childhood, in Johnston JH, Scholtmeijer RJ (eds): Problems in Paediatric Urology. Amsterdam, Netherlands, Excerpta Medica, 1972. pp 180-236 3. Ritchey ML, Othersen HB Jr, de Lorimier AA, et al: Renal vein involvement with nephroblastoma: A report of the National Wilms’ Tumor Study-3. Eur Urol 12139-144, 1990 4. Fullen WD, Hunt J. Altemeier WA: The clinical spectrum of penetrating injury to the superior mesenteric arterial circulation. J Trauma 12:656-663.1972 5. Accola KD, Feliciano DV, Mattox KL, et al: Management of injuries to the superior mesenteric artery. J Trauma 26:313-318, 1986 6. Lucas AE, Richardson JD, Flint LM, et al: Traumatic injury of the proximal superior mesenteric artery. Ann Surg 193:30-34, 1981 7. Bhanot SC, Beaufils A, Leiter E: Importance of collateral circulation of bowel in urologic surgery. J Urol 123:893-894,198O 8. Moskowitz M, Zimmerman H, Felson B: The meandering mesenteric artery of the colon. AJR Am J Roentgen01 92:10881099.1964 9. Boley SJ, Brandt LJ. Veith FJ: Ischemic disorders of the intestines. Curr Probl Surg 15:1-85, 1978 10. Lillehei RC, Goott B, Miller FA: The physiological response of the small bowel of the dog to ischemia including prolonged in vim preservation of the bowel with successful replacement and survival. Ann Surg 150:543-559, 1959
11. Nelson LE, Kremen AJ: Experimental occlusion of the superior mesenteric vessels with special reference to the role of intravascular thrombosis and its prevention by heparin. Surgery 28:819-826, 1950 12. Marfuggi RA, Greenspan M: Reliable intraoperative prediction of intestinal viability using a fluorescent indicator. Surg Gynecol Obstet 152:33-35,198l 13. Hobson RW II, Wright CB, O’Donnell JA, et al: Determination of intestinal viability by Doppler ultrasound. Arch Surg 114:165-168, 1979 14. Ernst CB, Hagihara PF, Daugherty ME, et al: Inferior mesenteric artery stump pressure: A reliable index for safe IMA ligation during abdominal aortic aneurysmectomy. Ann Surg 187: 641-645.1978 15. Leape LL, Breslow NE, Bishop HC: The surgical treatment of Wilms’ tumor: Results of the National Wilms’ Tumor Study. Ann Surg 187:351-356,1978 16. Lee DH, Sapire D, Markowitz R, et al: Radiation injury to abdominal aorta and iliac artery sustained in infancy. S Afr Med J 50:658-660, 1976 17. Colquhoun J: Hypoplasia of the abdominal aorta following therapeutic irradiation in infancy. Radiology 86:454-456, 1966 18. Lindsay S, Entenman C, Ellis EE, et al: Aortic arteriosclerosis in the dog after localized aortic irradiation with electrons. Circ Res 10:61-67, 1962 19. Fonkalsrud EW, Sanchez M, Zerubavel R, et al: Serial changes in arterial structure following radiation therapy. Surg Gynecol Obstet 145:395-400, 1977