0039-6109/92 $0.00 + .20
INTESTINAL ISCHEMIA
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY Paul G. Horgan, MCh, FRCS, FRCSI, and Thomas F. Gorey, MCh, FRCSI
With increased life expectancy, mesenteric vascular disease is being more commonly encountered in modern surgical practice. Most often, acute mesenteric ischemia has been viewed as a lethal disease affecting the elderly. There are, however, encouraging reports of the potential for earlier diagnosis and treatment, resulting in an improved outcome." 3, 13, 14 Although more patients with acute mesenteric ischemia are surviving today, the diagnosis even in these patients is frequently delayed. The operating surgeon is then faced with ischemic intestine, and further successful management is dependent on determining accurately the viability of the involved bowel. If all nonviable bowel is not resected, perforation and sepsis are inevitable. Bowel that is viable, but that has sustained irreversible damage to a portion of the wall, may later develop ischemic colitis or stricture. On the other hand, resection of long lengths of ischemic intestine capable of surviving may unnecessarily create the short-bowel syndrome. Thus, preservation of even a few extra centimeters of small intestine may make the difference between a patient capable of absorbing an adequate oral intake and an intestinal cripple dependent on long-term parenteral nutrition with all its attendant difficulties. The visual assessment of viability of the intestine is notoriously unreliable," and as a consequence, a number of intraoperative techniques have been developed to aid accurate diagnosis. This review analyzes frequently used diagnostic aids and outlines recently described From the Department of Surgery, Mater Misericordiae Hospital, University College Dublin, Dublin, Ireland
SURGICAL CLINICS OF NORTH AMERICA VOLUME 72 • NUMBER 1 • FEBRUARY 1992
143
144
HORGAN & GOREY
techniques from the experimental laboratory that have found clinical applicability and which may have a diagnostic role in the future (Table 1). CLINICAL ASSESSMENT OF INTESTINAL VIABILITY
The first evaluation of the bowel is visual assessment after the abdomen is opened. The color of the intestine depends on the stage of the mesenteric vascular obstruction (whether early or late) and whether it is of arterial or venous origin. Venous occlusion characteristically results in hemorrhagic engorgement of the bowel and mesentery. The dark hue of deoxygenated blood may resemble infarction, prompting a decision to resect viable bowel and resulting in unnecessary loss of intestine. In contrast, early arterial obstruction produces little change in the appearance of the intestine. Classically, the surgeon undertakes revascularization of the intestine or release of any mechanical cause of strangulation before determining intestinal viability. The bowel is then wrapped in warm saline packs to effect local vasodilation and a period of 15 minutes allowed to pass. Intestinal viability is then assessed by judging color, visible vessel pulsations, and peristaltic activity. Only when complete infarction of the intestine has occurred and the bowel is distended, thin walled, and green or black can a reliable diagnosis of nonviability be confidently made. Revascularization of a segment of intestine may achieve the return of mesenteric vessel pulsations through the arcades of the mesentery to the bowel wall, but irreversible necrosis may already have occurred by this stage. Nonocclusive mesenteric ischemia is being increasingly recognized as the underlying pathology in intestinal infarction, accounting for approximately 20% of mesenteric infarctions.": 43 In this setting, Table 1. SUMMARY OF TESTS OF INTESTINAL VIABILITY Test Clinical judgment Fluorescence Surface Fluorometer Doppler scanning Laser Doppler analysis pH studies Tetrazolium analysis Radionuclide scanning Surface oximetry Photoplethysmography Myoelectric analysis
Clinical (C)I Laboratory (L)*
Expense
+
C C C C C C L L
L/C L L
*Clinical methods also have laboratory applications.
Accuracy
+ +++ + +++
++ +
+++ ++ +++
++
++
+++
++
+++ + ++ ++
++ ++ ++
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
145
mesenteric pulsations may persist despite a low possibility of intestinal survival. Many patients with extensive intestinal ischemia are hypotensive at laparotomy, and restoration of blood pressure is needed to return visible arterial pulsations to the mesenteric arcades even after definitive revascularization procedures. When a decision is made to resect a segment of intestine, active bleeding from the cut ends is an excellent predictor of viability and anastomotic safety. However, if no active bleeding is found, an unnecessary enterotomy has been made with compromise of peritoneal cavity integrity secondary to release of proliferating luminal bacteria. Visible peristalsis ceases in ischemic intestine and returns after revascularization if the bowel is viable. However, peristaltic action may persist for some time after the onset of irreversible vascular compromise, and nonviable intestine may show anoxic spasms that are easily mistaken for peristaltic activity. These considerations limit the usefulness of this assessment. Bulkley and colleagues" estimated clinical criteria to have a sensitivity of 78% and a specificity of 91%. However, such clinical endpoints resulted in a 46% rate of unnecessary resection for a predictive value of 64%. Because of the difficulties in subjective evaluation of intestinal viability, the surgeon must make use of the available methods of objective assessment.
INTRAVASCULAR DYES
The intravascular injection of certain vital dyes results in their rapid distribution throughout the body. With a patent mesenteric vascular system and viable intestine, a characteristic visual pattern of dye uptake can be observed. Fluorescein is most widely used for this purpose, as it is actively taken up by viable intestine and fluoresces when exposed to ultraviolet light. The safety of intravenous fluorescein was established in 1942 when Herrlin and colleagues documented its use for evaluation of the mesenteric vasculature in 500 patients." There have been occasional reports of nausea and vomiting and rare anaphylactic reactions after fluorescein injection. 27 Following release of obstruction and revascularization of the intestine, all peritoneal fluid is aspirated from the intestine. Fluorescein (1000 mg) is then injected intravenously, and an ultraviolet lamp is used to illuminate the intestine. One of three principal patterns of fluorescence will be seen: a homogenous yellow-green appearance, as seen in normal bowel; a hyperfluorescent hyperemic pattern; or a finely granular, reticular pattern. Patchy fluorescence or areas of nonfluorescence are evidence of nonviability (Fig. 1).10 The technique is practical, rapid, accurate, and inexpensive, but experience is necessary to appreciate the decreased intensity of fluorescence that indicates doubtful viability. This subjective interpretation is a limiting feature of this test. Stolar and Randolph used the fluorescein technique to predict
146
HORGAN & GOREY
Figure 1. Gross and fluorescence pictures showing normal, hyperemic, and nonfluorescent bowel segments.
intestinal viability and described characteristic visual patterns of fluorescence seen immediately and 24 hours after reperfusion." Gorey reported that fluorescein testing was 96% sensitive and 95% specific in identifying nonviable intestine but was less useful, having a 17% falsepositive rate, in venous occlusions." Bulkley et al found the fluorescein technique to be superior to both clinical assessment and Doppler ultrasound examination in a series of 28 patients with intestinal ischemia." Mann and his colleagues" reported that fluorescence was more accurate than Doppler ultrasound in determining viability. They further reported that fluorescein staining occurred in tissue samples distal to the limits of blood flow as detected by the Doppler probe. Furthermore, nonfluorescing intestine within 1 cm of the stained bowel retained viability because of the lesser nutrient requirements of resting smooth muscle. Those authors went on to recommend, however, that such segments not be used for anastomosis, as some degree of mucosal ischemia was invariably present. Pearse et al found that intravenous fluorescein had a sensitivity of
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
147
88% in assessing early intestinal ischemia in an operative canine
model." However, in two cases, histologic changes consistent with irreversible ischemia were found within the zone of fluorescein staining considered to be normal. In these two cases, late fluorescence may have occurred, the dye perfusing well into areas of eventual mucosal necrosis. This work illustrates that evaluation of fluorescence must be made within the first 2 or 3 minutes because subsequent assessments may be less accurate. Paes et al found that the fluorescein test was of high reliability in the intraoperative determination of intestinal viability in an analysis of 38 patients with mesenteric ischemia." The problem of subjectivity with fluorescein testing has been addressed by Silverman, Hurford, and Cooper." who have described fiberoptic fluorometry, a method of quantifying the detected fluorescence. In this method, a branched fiberoptic light guide transmits blue light to the fluorescein in the bowel being examined. A photomultiplier tube then picks up and quantifies the fluorescence in dye fluorescence (OF) units. Computer software is used to store and analyze the data with standardized graphic patterns indicating the presence of viable or nonviable intestine. The accuracy of prediction of viability is increased from 53% for qualitative fluorescence to 98% for quantitative measuremerit." Carter and associates have described a dynamic assessment of perfusion by measuring both intestinal wall uptake and elimination of intravenously injected fluorescein." They reported that qualitative fluorescence was inaccurate because ischemic intestine with a hyperfluorescent staining distribution often progressed to necrosis. Fluorometric quantitation correctly identified hyperfluorescent segments that were viable. A number of other dyes have been evaluated experimentally in the assessment of bowel viability. Injection of trypan blue into the superior mesenteric artery of rats with observation of the intestinal uptake has been reported to have an accuracy of 84% for predicting bowel nonviability." Patent b1ue V dye'" and bromphenol" have also been investigated in experimental studies with some reported success, but fluorescein remains the only agent commonly used in clinical practice.
DOPPLER ULTRASOUND STUDIES
Doppler ultrasound utilizes the basic concept that the frequency of sound is shifted when reflected from moving objects such as the cellular components of blood. Doppler ultrasound apparatus is capable of detecting flow in vessels as small as digital arteries and has widespread use in the management of peripheral vascular disease. The technique has been modified for intraoperative use and has been found to be capable of evaluating intestinal viability accurately. The Doppler probe, which is gas sterilized for intraoperative use, is light and simple to operate and will detect flow in arteries and veins
148
HORGAN & GOREY
as small as vessels within the bowel wall. The precision of the examination is dependent on the correct application of the probe in relation to vessel location and depth; most probes used intraoperatively penetrate tissue to a depth of 1 em. Wright and Hobson" were the first to use Doppler ultrasound to study intestinal viability. They reported that the presence of intestinal blood flow correlated with viability as judged at second-look laparotomy 24 to 48 hours later. Pulsatile flow detected by Doppler scanning at the mesenteric and antimesenteric borders of the intestinal wall was found to be a reliable indicator of viability both in animal experiments and in three patients with mesenteric ischemia secondary to superior mesenteric artery thrombosis. 32, 44 Cooperman et aP6 demonstrated that Doppler scanning could help delineate the limits of resection of ischemic intestine and placement of sites of anastomosis. Histologic assessment showed that an anastomosis within 1 em of the last audible Doppler signal would heal. Progressive degrees of intestinal necrosis occurred 2 and 3 em beyond the last audible Doppler signal. The same group later confirmed the clinical usefulness and accuracy of Doppler in 23 patients with intestinal ischemia secondary to a variety of pathologies. IS Here, the decision to embark on a bowel resection was made on the basis of Doppler evaluation alone. Of 25 segments in 23 patients, 10 were judged nonviable clinically, but because arterial flow within the segments was detected by Doppler ultrasound, none was resected. All 23 patients had an uneventful postoperative course. Two segments were clinically viable but were resected as Doppler signals were absent, and histopathologic examination confirmed nonviability. Pearse et al" used an operative canine model to compare intravenous fluorescein and Doppler ultrasound in the assessment of bowel viability. The arterial supplies to five segments of bowel were ligated in each of six preconditioned dogs, and the limits of arterial perfusion at sites of resection were determined and subsequently correlated with intestinal viability as judged from histopathologic specimens. Doppler ultrasound resulted in two false-negative examinations, both in the transition zone, where flow was detected but was not sufficient to maintain tissue viability. Those authors speculated that the Doppler examination detected flow signals and rejected background noise that did not arise from the region of interest. In addition, there were six false-positive results, where adequate blood flow was not detected but the bowel appeared viable on histologic examination. These errors were attributed by the authors to technical or operator error. Overall, Doppler ultrasound was 88% sensitive in assessing ischemic intestinal segmerits." Brolin et al" reported that two clinical features of intestinal ischemia-color and visible peristalsis-were as reliable in predicting viability and healing ability of anastomoses as Doppler ultrasound. In this work, the intestine was pink and viable at the point of the last audible Doppler signal in 40 of 60 observations. These findings were in agreement with the earlier observations of Cooperman et al." and the
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
149
investigators concluded that an audible Doppler signal was rarely found in bowel that was adjudged ischemic clinically by the operating surgeon. However, visibly ischemic bowel without audible Doppler signals was seen to heal without complications." This study suggests that both Doppler ultrasound and clinical assessment may overdiagnose nonviability. Rotering et a137 observed that ultrasound signals tended to disappear even within normally perfused intestine, and there was also a tendency to record signals from other sites such as the mesenteric vessels. Considerable ambiguity was reported in the interpretation of the presence or absence of a signal, and this difficulty in interpretation was exaggerated when the examiner employed Doppler testing infre' quently. The accuracy of Doppler ultrasound in the investigation of ischemic intestine was refined by the technique of laser Doppler velocimetry, which produces noninvasive, real-time, continuous measurements of blood flow. The probe detects Doppler shift of backscattered laser light proportional to the velocity of the red blood cells in the microcirculation. Doppler ultrasound, in comparison, relies on a frequency shift in sound waves. The depth of tissue penetration by laser light is 1 mm, and a blood flow of 1.0 mm per second can be detected. Operator error may occur with this technique, as inclusion of a large vessel beneath the probe will not give a reliable indication of tissue blood flow. Similarly, compression of the bowel wall with the probe will decrease tissue blood flow and lead to an incorrect judgment of nonviability. Shepherd and Riedel" reported the continuous measurement of intestinal blood flow by laser Doppler techniques. In the same year, Field et apo were using this method to measure mucosal blood flow in canine intestine. The use of a suction cup was advocated by some authors to maintain a constant optical coupling without tissue compression.l- 20 Oohata et al used a probe holder to obtain stable and reproducible flow rates." In that study, laser Doppler was used to measure the blood flow of the colon and ileum in 10 dogs with surgically devascularized segments of intestine, The investigators found that the technique as compared with the hydrogen gas technique was a useful method of assessing the degree of intestinal ischemia by measuring submucosal blood flow. A significant limitation of Doppler ultrasound or laser Doppler velocimetry is the impracticability of screening large areas of intestine. Moreover, laser Doppler is expensive and may have intrinsic problems. Ahn et all reported on its extreme sensitivity to movement artifacts and questioned whether individual readings of serosal and mucosal blood flow did not reflect total blood flow in the entire bowel wall. Also, undue manipulation of the intestine may lead to loss of the Doppler ultrasound signal, whereas examination of the bowel in situ may result in detection of false signals from underlying loops. It may therefore be useful to combine Doppler methods with fluorescein testing. Suspect nonfluorescing segments of intestine may then be carefully tested by Doppler techniques.
150
HORGAN & GOREY
pH STUDIES AND TONOMETRY
The loss of the vascular supply to the wall of the intestine results in a rapid shift from aerobic to anerobic metabolism. Anaerobic glycolysis produces a rise in tissue pC02 and a fall in pH. Myers et a131 studied the relation between surface pH and pC02 of intestinal blood and viability. They found that after ligation of the mesenteric vessels, intestinal pH fell and pC02 rose, but the latter returned to normal after intestinal revascularization. However, return of pH and pC02 to normal was seen even in intestine that proved to be nonviable, suggesting that changes in intramural pH and pC02 depend on blood flow and not viability. Confirmatory findings were reported by Katz et al in 1974,25 who found no relation between mucosal pH shifts and ultimate viability. However, serosal pH values with electromyography were found to be helpful in predicting viability. With equivocal electromyographic activity, an alkalotic serosal pH (7.95-8.40) was considered to indicate irreversible ischemic damage." The poor predictive accuracy of mucosal or serosal pH and pC02 testing remains the principal obstacle to its widespread acceptance.
SURFACE OXIMETRY
On the basis of their successful use of transcutaneous oxygen monitoring in critically ill patients with and without low-flow shock, Tremper and Shoemaker were prompted to investigate the use of surface oxygen tension (PS02) measurements to assess the adequacy of perfusion of intra-abdominal organs and tissues." They studied the effects of local perfusion on PS02 in the small intestine and correlated bowel PS02 with viability and ability to heal. Readings taken just prior to anastomosis were found to predict viability at 48 hours. Anastomoses performed on bowel with less than 30% of the predevascularization PS02 became necrotic. One third of the anastomoses leaked when made with bowel having a PS02 between 30% and 50% of baseline, and at PS02 values above 50% of the initial normal value, all anastomoses healed. Those authors concluded that surface oximetry allowed accurate intraoperative assessment of bowel perfusion." Because the PS02 electrode measures a surface area only 3 mm in diameter, segments of patchy ischemia may be missed with this technique, particularly after a global ischemic event such as a superior mesenteric artery embolism or venous thrombosis. Nevertheless, the method does have promise for the future, as it is simple, accurate, inexpensive, and available in most operating rooms. Combination of surface oximetry with intravascular fluorescein assessment may allow questionably viable areas of intestine to be evaluated by detailed PS02 analysis. De Nobile, Guzzetta, and Patterson" have described a canine model
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
151
of ischemic intestine in which viability was assessed by measurement of pulse oximetry of the bowel serosal surface. They demonstrated an excellent correlation between normal intestinal wall and peripheral tissue oxygen saturation and found that in bowel adjacent to an ischemic segment with a normal wall oxygen saturation, that this could reliably define the limitation of viable intestine, as confirmed histopathologically. INFRARED PHOTOPLETHYSMOGRAPHY
Photoplethysmography monitors changes in tissue blood volume content by detecting alterations in reflected infrared light as a function of its absorption by hemoglobin. Eldrup-Jorgensen et aF9 described the usefulness of photoplethysmography as an aid in the assessment of amputation levels in vascular surgery. Thorn et al" assessed the same technique in the determination of viability of pedicle flaps in plastic surgical reconstructions. Pearse et aP6 reported the use of photoplethysmography in identifying early intestinal ischemia in a canine model. Photoplethysmography was performed by first establishing the maximal signal from the surface of the normal stomach as a reference and subsequently mapping the serosal and mucosal surfaces of the bowel segments across bowel margins. Waveform patterns of pulsatility were obtained and classified as being normal, absent, or demonstrating 500/0 of the maximal deflection. Those workers found that waveforms showing 50% of the normal maximal deflection accurately predicted the limits of intestinal necrosis. Unlike Doppler ultrasound, no contact gel was required, and the technique was found to be highly sensitive to changes in blood flow. In ischemic segments, a pattern of blood flow ranging from normal to diminished to absent was demonstrated. However, there were segments with persistent pulsatility as detected by photoplethysmography that demonstrated mucosal necrosis histologically. Furthermore, attempts to quantitate the photoplethysmographic waveforms proved impossible because of the variations in the emission-detection ratio of infrared light unrelated to tissue blood volume. The technique may have usefulness in the future with further refinement. MYOELECTRIC ANALYSIS
Experimental studies by Khin and Daniel" and later by Guisan et aF3 demonstrated that ischemia has predictable effects on the patterns of slow wave activity in the wall of the small intestine. The frequency of such slow waves was shown to decrease progressively with prolongation of warm ischemia time. Chou" studied the relation between intestinal blood flow and bowel motility. He found that spontaneous spike burst activity was significantly decreased after 4 hours of ischemia or a longer duration of ischemia that resulted in destruction of both
152
HORGAN & GOREY
ganglionic and smooth muscle cells. Electric stimulation of such ischemic small intestine generated diminished spike potentials.": 23 Cabot and Kohatsu? attempted to quantitate myoelectric assessment of bowel viability. They found that a warm ischemic time of as much as 18 hours did not completely destroy the capacity of smooth muscle cells to generate recordable spike potentials. After revascularization of ischemic bowel, not only did the intestine consistently survive, but it demonstrated persistent, albeit diminished, contractility. 9 Brolin et a1 4- 6 designed a strain gauge probe capable of quantitative measurement of intestinal ischemic damage. The probe, called the electrical contractility meter, was clipped to the serosal surface of intestine, which also was connected to a constant current stimulus source by a small cable. The source delivered a succession of 12 electrical impulses to the intestine. The strain gauges on the probe detected smooth muscle responses producing visible contractile responses, recording them on a strip chart. In normal bowel, it was possible to detect contractions without stimulation but the addition of electrical stimulation enhanced the magnitude and speed of contraction. Using the meter, Brolin et al' reported a consistent correlation between increasing threshold stimulus level (TSL) (the current in milliamperes necessary to produce a clearly defined smooth muscle contraction) and deteriorating bowel color and disappearance of both visible peristalsis and Doppler signals in the intestinal wall, peripheral arterioles, and marginal artery. They found that readings in the 30 to 50 mAmp range represented ischemic but viable bowel. The same group in 19896 designed a series of experiments to define exactly the boundaries of viability in intestine judged ischemic by myoelectric assessment. In a canine model, five methods of assessment of intestinal viability were compared: threshold stimulus level, bowel color, peristaltic activity, Doppler ultrasound, and histologic evaluation of the resection margin. Three of the five methods-color, peristalsis, and early histologic findings-did not correlate well with intestinal survival rates. However, Doppler ultrasound and myoelectric assessment measured by the contractility meter were statistically correlated with late intestinal viability. Despite the success of this technique, there is an element of subjectivity in interpreting the quantitative recordings. Artifact on the baseline of the strip chart may be misinterpreted as slow low-amplitude smooth muscle contractions. Brolin and his colleagues are engaged in the development of a modified device with a self-contained microprocessor capable of coordinating multiple functions such as stimulus control, response monitoring, and data display with a built-in feature for rejection of artifactual readings. Clinical application of such a method of myoelectric assessment of intestinal viability is awaited with interest and may prove to be a simple and reliable technique for routine use in the operating room.
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
153
SUMMARY Acute intestinal ischemia and infarction remain serious clinical problems despite early operative intervention. Accurate intraoperative assessment of intestinal viability is essential in determining the limits of resection in patients with intestinal infarction. Clinical features of bowel viability such as color and peristalsis do not correlate uniformly with bowel survival, and as a result, several techniques have been developed to assess intestinal blood flow at the time of operation. The requirements of an ideal viability test are: 1. The technique must have ready availability, preferably in every operating theater dealing with abdominal emergencies. 2. The necessary equipment must not be cumbersome or require specialized personnel. 3. The method must be accurate with a minimum of false-negative results and, more importantly, few false positives. A falsenegative result leaves in situ nonviable bowel, which may lead to early perforation and late stricturing. This situation may be recoverable with further surgical intervention, however. On the other hand, a false-positive assessment of bowel viability results in the resection of potentially recoverable intestine, which is lost forever and may represent a vital difference for morbiditymortality and long-term nutrition. 4. The technique must be objective and be reproducible. 5. The method must be cost effective. To date, only two tests have found widespread acceptance and clinical applicability: fluorescein assessment and Doppler studies either with ultrasound or as refined in laser velocimetry. Although other techniques may be of some value today or in the future, the most practical approach would appear to be to use fluorescein assessment under a modified Wood's lamp as the initial method of evaluating intestinal viability and either Doppler ultrasound or perfusion fluorometry for any areas of particularly doubtful viability.
References 1. Ahn H, Lindhagen J, Nilsson GE, et al: Evaluation of laser Dopp!er flowmetry in the assessment of intestinal blood flow in the cat. Gastroenterology 88:951, 1985 2. Boley 5J, 5prayregen S, Veith FJ: Initial results of an aggressive roentgenologic and surgical approach to acute mesenteric ischemia. Surgery 82:848, 1977 3. Boley SJ, Feinstein FR, Sammartano R. New concept in the management of emboli of the superior mesenteric artery. Surg Gynecol Obstet 153:561, 1981 4. Brolin RE, Semmlow JL, Mackensie JW: Quantitative evaluation of bowel viability. Proc IEEE Front Eng Comput Health Care 6:320, 1984 5. Brolin RE, Semmlow JL, Mackenzie JW, et al: Quantitative myoelectric determination of bowel viability. J 5urg Res 41:557, 1986 6. Brolin RE, 5emmlow JL, Sehonanda A, et al: Comparison of five methods of assessment of intestinal viability. Surg Gynecol Obstet 168:6, 1989
154
HORGAN & GOREY
7. Bulkley G, Zuidema G, Hamilton S, et al: Intraoperative determination of small intestinal viability following ischemic injury. Ann Surg 193:628, 1981 8. Bussemaker JB, Lindeman J: Comparison of methods to determine viability of small intestine. Ann Surg 176:97, 1972 9. Cabot RM, Kohatsu S: The effects of ischaemia on the electrical and contractile activities of the canine small intestine. Am J Surg 136:242, 1978 10. Carter M, Fantani G, Sammartano R, et al: Qualitative and quantitative fluorescence for determining intestinal viability. Am J Surg 147:117, 1984 11. Chou CC: Relationship between intestinal blood flow and motility. Annu Rev Physiol 44:29, 1982 12. Chung RS: Blood flow in colonic anastomoses. Ann Surg 206:335, 1987 13. Clark RA, Gallant TE: Acute mesenteric ischemia: Angiographic spectrum. AJR 142:555, 1984 14. Clavien PA, Muller C, Harder F: Treatment of mesenteric infarction. Br J Surg 74:500, 1987 15. Cooperman M, Martin EW, Carey LC: Evaluation of ischemic intestine by Doppler ultrasound. Am J Surg 139:73, 1980 16. Cooperman M, Pall WG, Martin EW, et al: Determination of viability of ischemic intestine by Doppler ultrasound. Surgery 83:705, 1978 17. De Nobile J, Guzzetta P, Patterson K: Pulse oximetry as a means of assessing bowel viability. J Surg Res 48:21, 1990 18. Dineen P, Goulian 0, McSherry CK: A method of demonstrating intestinal viability. Am J Gastroenterol 45:335, 1966 19. Eldrup-Jorgensen SV, Schwartz SI, Wallace JD: A method for clinical evaluation of peripheral circulation: Photoelectric hemodensitometry. Surgery 59:505, 1966 20. Field AD, Fondacaro JD, Halloway G, et al: Measurement of mucosal blood flow in the canine intestine with laser Doppler velocimetry. Life Sci 31:1509, 1982 21. Gorey TF: Prediction of intestinal recovery after ischaemic injury due to arterial, venous and mixed arterial and venous icclusions. J R Soc Med 73:631, 1980 22. Gorey TF, O'Sullivan M: Prognostic factors in extensive mesenteric ischaemia. Ann R ColI Surg Engl 70:191, 1988 23. Guisan YJ, Hreno A, Gurd FN: Effect of acute ischaemia on the motility of the small bowel in the awake dog. Eur Surg Res 7:32, 1975 24. Herrlin JO [r, Glasser ST, Lange K: New methods for determining the viability of the bowel. Arch Surg 45:785, 1942 25. Katz S, Wahab A, Murray W, et al: New parameters of viability in ischemic bowel disease. Am J Surg 127:136, 1974 26. Khin J, Daniel EE: The effects of ischemia on intestinal nerves and electrical slow waves. Am J Dig Dis 15:959, 1970 27. La Piana FG, Penner R: Anaphylactoid reaction to intravenously administered fluorescein. Arch Ophthalmol 79:161, 1968 28. Locke R, Hauser CJ, Shoemaker WC: The use of surface oximetry to assess bowel viability. Arch Surg 119:1252, 1984 29. Mann A, Fazio VM, Lucas FV: A comparative study of the use of fluorescein and the Doppler device in the determination of intestinal viability. Surg Gynecol Obstet 154:53, 1982 30. Myers MB, Cherry G: Use of vital dyes in the evaluation of the blood supply of the colon. Surg Gynecol Obstet 149:97, 1969 31. Myers MB, Cherry G, Gesser J: Relationship between surface pH and PCO z and the vascularity and viability of the intestine. Surg Gynecol Obstet 134:787, 1972 32. O'Donnell JA, Hobson RW: Operative confirmation of Doppler ultrasound in evaluation of intestinal viability. Surgery 83:705, 1978 33. Oohata Y, Mibu R, Hotokezaka M, et al: Comparison of blood flow assessment between laser Doppler velocimetry and the hydrogen gas clearance method in ischemic intestine in dogs. Am J Surg 160:511, 1990 34. Paes E, Vollmar JF, Hutschenreiter S, et al: Mesenteric infarct: New aspects of diagnosis and therapy. Chirurg 59:828, 1988 35. Papachristou 0, Fortner JG: Prediction of intestinal viability by intraarterial dye injection: A simple test. Am J Surg 132:572, 1976
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
155
36. Pearse WH, Jones ON, Warren GH, et al: The use of infrared photoplethysmography in identifying early intestinal ischaemia. Arch Surg 122:308, 1987 37. Rotering RH, Dixon LA, Holloway JA, et al: A comparison of the HeNe laser and ultrasound Doppler systems in the determination of viability of ischemic canine intestine. Ann Surg 196:705, 1982 38. Shepherd AP, Riedel GL: Continuous measurement of intestinal mucosal blood flow by laser Doppler velocimetry. Am J PhysioI242:G668--G672,1982 39. Silverman DG, Murford WE, Cooper HS, et al: Quantification of fluorescein distribution to strangulated rat ileum. J Surg Res 34:179-186, 1983 40. Stolar CJ, Randolf JG: Evaluation of ischaemic bowel viability with a fluorescent technique. J Ped Surg 13:221-225, 1978 41. Thorn FL, Geargiade NG, Wheeler WE, et al: Photopletysmography as an aid in determining the viability of pedicle flaps. Plast Reconstr Surg 44:279, 1969 42. Tremper KK, Shoemaker WC: Transcutaneous oxygen monitoring of critically ill patients with and without low flow shock. Crit Care Med 9:706, 1981 43. Wilson C, Gupta R, Gilmour DG, et al: Acute superior mesenteric ischaemia. Br J Surg 74:279, 1987 44. Wright GB, Hobson RW: Prediction of intestinal viability using Doppler ultrasound techniques. Am J Surg 129:642, 1975
Address reprint requests to Thomas F. Gorey, MCh, FRCSI Department of Surgery Mater Misericordiae Hospital University College Dublin 47 Eccles Street Dublin 7, Ireland
INTESTINAL ISCHEMIA
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY Paul G. Horgan, MCh, FRCS, FRCSI, and Thomas F. Gorey, MCh, FRCSI
With increased life expectancy, mesenteric vascular disease is being more commonly encountered in modern surgical practice. Most often, acute mesenteric ischemia has been viewed as a lethal disease affecting the elderly. There are, however, encouraging reports of the potential for earlier diagnosis and treatment, resulting in an improved outcome." 3, 13, 14 Although more patients with acute mesenteric ischemia are surviving today, the diagnosis even in these patients is frequently delayed. The operating surgeon is then faced with ischemic intestine, and further successful management is dependent on determining accurately the viability of the involved bowel. If all nonviable bowel is not resected, perforation and sepsis are inevitable. Bowel that is viable, but that has sustained irreversible damage to a portion of the wall, may later develop ischemic colitis or stricture. On the other hand, resection of long lengths of ischemic intestine capable of surviving may unnecessarily create the short-bowel syndrome. Thus, preservation of even a few extra centimeters of small intestine may make the difference between a patient capable of absorbing an adequate oral intake and an intestinal cripple dependent on long-term parenteral nutrition with all its attendant difficulties. The visual assessment of viability of the intestine is notoriously unreliable," and as a consequence, a number of intraoperative techniques have been developed to aid accurate diagnosis. This review analyzes frequently used diagnostic aids and outlines recently described From the Department of Surgery, Mater Misericordiae Hospital, University College Dublin, Dublin, Ireland
SURGICAL CLINICS OF NORTH AMERICA VOLUME 72 • NUMBER 1 • FEBRUARY 1992
143
144
HORGAN & GOREY
techniques from the experimental laboratory that have found clinical applicability and which may have a diagnostic role in the future (Table 1). CLINICAL ASSESSMENT OF INTESTINAL VIABILITY
The first evaluation of the bowel is visual assessment after the abdomen is opened. The color of the intestine depends on the stage of the mesenteric vascular obstruction (whether early or late) and whether it is of arterial or venous origin. Venous occlusion characteristically results in hemorrhagic engorgement of the bowel and mesentery. The dark hue of deoxygenated blood may resemble infarction, prompting a decision to resect viable bowel and resulting in unnecessary loss of intestine. In contrast, early arterial obstruction produces little change in the appearance of the intestine. Classically, the surgeon undertakes revascularization of the intestine or release of any mechanical cause of strangulation before determining intestinal viability. The bowel is then wrapped in warm saline packs to effect local vasodilation and a period of 15 minutes allowed to pass. Intestinal viability is then assessed by judging color, visible vessel pulsations, and peristaltic activity. Only when complete infarction of the intestine has occurred and the bowel is distended, thin walled, and green or black can a reliable diagnosis of nonviability be confidently made. Revascularization of a segment of intestine may achieve the return of mesenteric vessel pulsations through the arcades of the mesentery to the bowel wall, but irreversible necrosis may already have occurred by this stage. Nonocclusive mesenteric ischemia is being increasingly recognized as the underlying pathology in intestinal infarction, accounting for approximately 20% of mesenteric infarctions.": 43 In this setting, Table 1. SUMMARY OF TESTS OF INTESTINAL VIABILITY Test Clinical judgment Fluorescence Surface Fluorometer Doppler scanning Laser Doppler analysis pH studies Tetrazolium analysis Radionuclide scanning Surface oximetry Photoplethysmography Myoelectric analysis
Clinical (C)I Laboratory (L)*
Expense
+
C C C C C C L L
L/C L L
*Clinical methods also have laboratory applications.
Accuracy
+ +++ + +++
++ +
+++ ++ +++
++
++
+++
++
+++ + ++ ++
++ ++ ++
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
145
mesenteric pulsations may persist despite a low possibility of intestinal survival. Many patients with extensive intestinal ischemia are hypotensive at laparotomy, and restoration of blood pressure is needed to return visible arterial pulsations to the mesenteric arcades even after definitive revascularization procedures. When a decision is made to resect a segment of intestine, active bleeding from the cut ends is an excellent predictor of viability and anastomotic safety. However, if no active bleeding is found, an unnecessary enterotomy has been made with compromise of peritoneal cavity integrity secondary to release of proliferating luminal bacteria. Visible peristalsis ceases in ischemic intestine and returns after revascularization if the bowel is viable. However, peristaltic action may persist for some time after the onset of irreversible vascular compromise, and nonviable intestine may show anoxic spasms that are easily mistaken for peristaltic activity. These considerations limit the usefulness of this assessment. Bulkley and colleagues" estimated clinical criteria to have a sensitivity of 78% and a specificity of 91%. However, such clinical endpoints resulted in a 46% rate of unnecessary resection for a predictive value of 64%. Because of the difficulties in subjective evaluation of intestinal viability, the surgeon must make use of the available methods of objective assessment.
INTRAVASCULAR DYES
The intravascular injection of certain vital dyes results in their rapid distribution throughout the body. With a patent mesenteric vascular system and viable intestine, a characteristic visual pattern of dye uptake can be observed. Fluorescein is most widely used for this purpose, as it is actively taken up by viable intestine and fluoresces when exposed to ultraviolet light. The safety of intravenous fluorescein was established in 1942 when Herrlin and colleagues documented its use for evaluation of the mesenteric vasculature in 500 patients." There have been occasional reports of nausea and vomiting and rare anaphylactic reactions after fluorescein injection. 27 Following release of obstruction and revascularization of the intestine, all peritoneal fluid is aspirated from the intestine. Fluorescein (1000 mg) is then injected intravenously, and an ultraviolet lamp is used to illuminate the intestine. One of three principal patterns of fluorescence will be seen: a homogenous yellow-green appearance, as seen in normal bowel; a hyperfluorescent hyperemic pattern; or a finely granular, reticular pattern. Patchy fluorescence or areas of nonfluorescence are evidence of nonviability (Fig. 1).10 The technique is practical, rapid, accurate, and inexpensive, but experience is necessary to appreciate the decreased intensity of fluorescence that indicates doubtful viability. This subjective interpretation is a limiting feature of this test. Stolar and Randolph used the fluorescein technique to predict
146
HORGAN & GOREY
Figure 1. Gross and fluorescence pictures showing normal, hyperemic, and nonfluorescent bowel segments.
intestinal viability and described characteristic visual patterns of fluorescence seen immediately and 24 hours after reperfusion." Gorey reported that fluorescein testing was 96% sensitive and 95% specific in identifying nonviable intestine but was less useful, having a 17% falsepositive rate, in venous occlusions." Bulkley et al found the fluorescein technique to be superior to both clinical assessment and Doppler ultrasound examination in a series of 28 patients with intestinal ischemia." Mann and his colleagues" reported that fluorescence was more accurate than Doppler ultrasound in determining viability. They further reported that fluorescein staining occurred in tissue samples distal to the limits of blood flow as detected by the Doppler probe. Furthermore, nonfluorescing intestine within 1 cm of the stained bowel retained viability because of the lesser nutrient requirements of resting smooth muscle. Those authors went on to recommend, however, that such segments not be used for anastomosis, as some degree of mucosal ischemia was invariably present. Pearse et al found that intravenous fluorescein had a sensitivity of
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
147
88% in assessing early intestinal ischemia in an operative canine
model." However, in two cases, histologic changes consistent with irreversible ischemia were found within the zone of fluorescein staining considered to be normal. In these two cases, late fluorescence may have occurred, the dye perfusing well into areas of eventual mucosal necrosis. This work illustrates that evaluation of fluorescence must be made within the first 2 or 3 minutes because subsequent assessments may be less accurate. Paes et al found that the fluorescein test was of high reliability in the intraoperative determination of intestinal viability in an analysis of 38 patients with mesenteric ischemia." The problem of subjectivity with fluorescein testing has been addressed by Silverman, Hurford, and Cooper." who have described fiberoptic fluorometry, a method of quantifying the detected fluorescence. In this method, a branched fiberoptic light guide transmits blue light to the fluorescein in the bowel being examined. A photomultiplier tube then picks up and quantifies the fluorescence in dye fluorescence (OF) units. Computer software is used to store and analyze the data with standardized graphic patterns indicating the presence of viable or nonviable intestine. The accuracy of prediction of viability is increased from 53% for qualitative fluorescence to 98% for quantitative measuremerit." Carter and associates have described a dynamic assessment of perfusion by measuring both intestinal wall uptake and elimination of intravenously injected fluorescein." They reported that qualitative fluorescence was inaccurate because ischemic intestine with a hyperfluorescent staining distribution often progressed to necrosis. Fluorometric quantitation correctly identified hyperfluorescent segments that were viable. A number of other dyes have been evaluated experimentally in the assessment of bowel viability. Injection of trypan blue into the superior mesenteric artery of rats with observation of the intestinal uptake has been reported to have an accuracy of 84% for predicting bowel nonviability." Patent b1ue V dye'" and bromphenol" have also been investigated in experimental studies with some reported success, but fluorescein remains the only agent commonly used in clinical practice.
DOPPLER ULTRASOUND STUDIES
Doppler ultrasound utilizes the basic concept that the frequency of sound is shifted when reflected from moving objects such as the cellular components of blood. Doppler ultrasound apparatus is capable of detecting flow in vessels as small as digital arteries and has widespread use in the management of peripheral vascular disease. The technique has been modified for intraoperative use and has been found to be capable of evaluating intestinal viability accurately. The Doppler probe, which is gas sterilized for intraoperative use, is light and simple to operate and will detect flow in arteries and veins
148
HORGAN & GOREY
as small as vessels within the bowel wall. The precision of the examination is dependent on the correct application of the probe in relation to vessel location and depth; most probes used intraoperatively penetrate tissue to a depth of 1 em. Wright and Hobson" were the first to use Doppler ultrasound to study intestinal viability. They reported that the presence of intestinal blood flow correlated with viability as judged at second-look laparotomy 24 to 48 hours later. Pulsatile flow detected by Doppler scanning at the mesenteric and antimesenteric borders of the intestinal wall was found to be a reliable indicator of viability both in animal experiments and in three patients with mesenteric ischemia secondary to superior mesenteric artery thrombosis. 32, 44 Cooperman et aP6 demonstrated that Doppler scanning could help delineate the limits of resection of ischemic intestine and placement of sites of anastomosis. Histologic assessment showed that an anastomosis within 1 em of the last audible Doppler signal would heal. Progressive degrees of intestinal necrosis occurred 2 and 3 em beyond the last audible Doppler signal. The same group later confirmed the clinical usefulness and accuracy of Doppler in 23 patients with intestinal ischemia secondary to a variety of pathologies. IS Here, the decision to embark on a bowel resection was made on the basis of Doppler evaluation alone. Of 25 segments in 23 patients, 10 were judged nonviable clinically, but because arterial flow within the segments was detected by Doppler ultrasound, none was resected. All 23 patients had an uneventful postoperative course. Two segments were clinically viable but were resected as Doppler signals were absent, and histopathologic examination confirmed nonviability. Pearse et al" used an operative canine model to compare intravenous fluorescein and Doppler ultrasound in the assessment of bowel viability. The arterial supplies to five segments of bowel were ligated in each of six preconditioned dogs, and the limits of arterial perfusion at sites of resection were determined and subsequently correlated with intestinal viability as judged from histopathologic specimens. Doppler ultrasound resulted in two false-negative examinations, both in the transition zone, where flow was detected but was not sufficient to maintain tissue viability. Those authors speculated that the Doppler examination detected flow signals and rejected background noise that did not arise from the region of interest. In addition, there were six false-positive results, where adequate blood flow was not detected but the bowel appeared viable on histologic examination. These errors were attributed by the authors to technical or operator error. Overall, Doppler ultrasound was 88% sensitive in assessing ischemic intestinal segmerits." Brolin et al" reported that two clinical features of intestinal ischemia-color and visible peristalsis-were as reliable in predicting viability and healing ability of anastomoses as Doppler ultrasound. In this work, the intestine was pink and viable at the point of the last audible Doppler signal in 40 of 60 observations. These findings were in agreement with the earlier observations of Cooperman et al." and the
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
149
investigators concluded that an audible Doppler signal was rarely found in bowel that was adjudged ischemic clinically by the operating surgeon. However, visibly ischemic bowel without audible Doppler signals was seen to heal without complications." This study suggests that both Doppler ultrasound and clinical assessment may overdiagnose nonviability. Rotering et a137 observed that ultrasound signals tended to disappear even within normally perfused intestine, and there was also a tendency to record signals from other sites such as the mesenteric vessels. Considerable ambiguity was reported in the interpretation of the presence or absence of a signal, and this difficulty in interpretation was exaggerated when the examiner employed Doppler testing infre' quently. The accuracy of Doppler ultrasound in the investigation of ischemic intestine was refined by the technique of laser Doppler velocimetry, which produces noninvasive, real-time, continuous measurements of blood flow. The probe detects Doppler shift of backscattered laser light proportional to the velocity of the red blood cells in the microcirculation. Doppler ultrasound, in comparison, relies on a frequency shift in sound waves. The depth of tissue penetration by laser light is 1 mm, and a blood flow of 1.0 mm per second can be detected. Operator error may occur with this technique, as inclusion of a large vessel beneath the probe will not give a reliable indication of tissue blood flow. Similarly, compression of the bowel wall with the probe will decrease tissue blood flow and lead to an incorrect judgment of nonviability. Shepherd and Riedel" reported the continuous measurement of intestinal blood flow by laser Doppler techniques. In the same year, Field et apo were using this method to measure mucosal blood flow in canine intestine. The use of a suction cup was advocated by some authors to maintain a constant optical coupling without tissue compression.l- 20 Oohata et al used a probe holder to obtain stable and reproducible flow rates." In that study, laser Doppler was used to measure the blood flow of the colon and ileum in 10 dogs with surgically devascularized segments of intestine, The investigators found that the technique as compared with the hydrogen gas technique was a useful method of assessing the degree of intestinal ischemia by measuring submucosal blood flow. A significant limitation of Doppler ultrasound or laser Doppler velocimetry is the impracticability of screening large areas of intestine. Moreover, laser Doppler is expensive and may have intrinsic problems. Ahn et all reported on its extreme sensitivity to movement artifacts and questioned whether individual readings of serosal and mucosal blood flow did not reflect total blood flow in the entire bowel wall. Also, undue manipulation of the intestine may lead to loss of the Doppler ultrasound signal, whereas examination of the bowel in situ may result in detection of false signals from underlying loops. It may therefore be useful to combine Doppler methods with fluorescein testing. Suspect nonfluorescing segments of intestine may then be carefully tested by Doppler techniques.
150
HORGAN & GOREY
pH STUDIES AND TONOMETRY
The loss of the vascular supply to the wall of the intestine results in a rapid shift from aerobic to anerobic metabolism. Anaerobic glycolysis produces a rise in tissue pC02 and a fall in pH. Myers et a131 studied the relation between surface pH and pC02 of intestinal blood and viability. They found that after ligation of the mesenteric vessels, intestinal pH fell and pC02 rose, but the latter returned to normal after intestinal revascularization. However, return of pH and pC02 to normal was seen even in intestine that proved to be nonviable, suggesting that changes in intramural pH and pC02 depend on blood flow and not viability. Confirmatory findings were reported by Katz et al in 1974,25 who found no relation between mucosal pH shifts and ultimate viability. However, serosal pH values with electromyography were found to be helpful in predicting viability. With equivocal electromyographic activity, an alkalotic serosal pH (7.95-8.40) was considered to indicate irreversible ischemic damage." The poor predictive accuracy of mucosal or serosal pH and pC02 testing remains the principal obstacle to its widespread acceptance.
SURFACE OXIMETRY
On the basis of their successful use of transcutaneous oxygen monitoring in critically ill patients with and without low-flow shock, Tremper and Shoemaker were prompted to investigate the use of surface oxygen tension (PS02) measurements to assess the adequacy of perfusion of intra-abdominal organs and tissues." They studied the effects of local perfusion on PS02 in the small intestine and correlated bowel PS02 with viability and ability to heal. Readings taken just prior to anastomosis were found to predict viability at 48 hours. Anastomoses performed on bowel with less than 30% of the predevascularization PS02 became necrotic. One third of the anastomoses leaked when made with bowel having a PS02 between 30% and 50% of baseline, and at PS02 values above 50% of the initial normal value, all anastomoses healed. Those authors concluded that surface oximetry allowed accurate intraoperative assessment of bowel perfusion." Because the PS02 electrode measures a surface area only 3 mm in diameter, segments of patchy ischemia may be missed with this technique, particularly after a global ischemic event such as a superior mesenteric artery embolism or venous thrombosis. Nevertheless, the method does have promise for the future, as it is simple, accurate, inexpensive, and available in most operating rooms. Combination of surface oximetry with intravascular fluorescein assessment may allow questionably viable areas of intestine to be evaluated by detailed PS02 analysis. De Nobile, Guzzetta, and Patterson" have described a canine model
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
151
of ischemic intestine in which viability was assessed by measurement of pulse oximetry of the bowel serosal surface. They demonstrated an excellent correlation between normal intestinal wall and peripheral tissue oxygen saturation and found that in bowel adjacent to an ischemic segment with a normal wall oxygen saturation, that this could reliably define the limitation of viable intestine, as confirmed histopathologically. INFRARED PHOTOPLETHYSMOGRAPHY
Photoplethysmography monitors changes in tissue blood volume content by detecting alterations in reflected infrared light as a function of its absorption by hemoglobin. Eldrup-Jorgensen et aF9 described the usefulness of photoplethysmography as an aid in the assessment of amputation levels in vascular surgery. Thorn et al" assessed the same technique in the determination of viability of pedicle flaps in plastic surgical reconstructions. Pearse et aP6 reported the use of photoplethysmography in identifying early intestinal ischemia in a canine model. Photoplethysmography was performed by first establishing the maximal signal from the surface of the normal stomach as a reference and subsequently mapping the serosal and mucosal surfaces of the bowel segments across bowel margins. Waveform patterns of pulsatility were obtained and classified as being normal, absent, or demonstrating 500/0 of the maximal deflection. Those workers found that waveforms showing 50% of the normal maximal deflection accurately predicted the limits of intestinal necrosis. Unlike Doppler ultrasound, no contact gel was required, and the technique was found to be highly sensitive to changes in blood flow. In ischemic segments, a pattern of blood flow ranging from normal to diminished to absent was demonstrated. However, there were segments with persistent pulsatility as detected by photoplethysmography that demonstrated mucosal necrosis histologically. Furthermore, attempts to quantitate the photoplethysmographic waveforms proved impossible because of the variations in the emission-detection ratio of infrared light unrelated to tissue blood volume. The technique may have usefulness in the future with further refinement. MYOELECTRIC ANALYSIS
Experimental studies by Khin and Daniel" and later by Guisan et aF3 demonstrated that ischemia has predictable effects on the patterns of slow wave activity in the wall of the small intestine. The frequency of such slow waves was shown to decrease progressively with prolongation of warm ischemia time. Chou" studied the relation between intestinal blood flow and bowel motility. He found that spontaneous spike burst activity was significantly decreased after 4 hours of ischemia or a longer duration of ischemia that resulted in destruction of both
152
HORGAN & GOREY
ganglionic and smooth muscle cells. Electric stimulation of such ischemic small intestine generated diminished spike potentials.": 23 Cabot and Kohatsu? attempted to quantitate myoelectric assessment of bowel viability. They found that a warm ischemic time of as much as 18 hours did not completely destroy the capacity of smooth muscle cells to generate recordable spike potentials. After revascularization of ischemic bowel, not only did the intestine consistently survive, but it demonstrated persistent, albeit diminished, contractility. 9 Brolin et a1 4- 6 designed a strain gauge probe capable of quantitative measurement of intestinal ischemic damage. The probe, called the electrical contractility meter, was clipped to the serosal surface of intestine, which also was connected to a constant current stimulus source by a small cable. The source delivered a succession of 12 electrical impulses to the intestine. The strain gauges on the probe detected smooth muscle responses producing visible contractile responses, recording them on a strip chart. In normal bowel, it was possible to detect contractions without stimulation but the addition of electrical stimulation enhanced the magnitude and speed of contraction. Using the meter, Brolin et al' reported a consistent correlation between increasing threshold stimulus level (TSL) (the current in milliamperes necessary to produce a clearly defined smooth muscle contraction) and deteriorating bowel color and disappearance of both visible peristalsis and Doppler signals in the intestinal wall, peripheral arterioles, and marginal artery. They found that readings in the 30 to 50 mAmp range represented ischemic but viable bowel. The same group in 19896 designed a series of experiments to define exactly the boundaries of viability in intestine judged ischemic by myoelectric assessment. In a canine model, five methods of assessment of intestinal viability were compared: threshold stimulus level, bowel color, peristaltic activity, Doppler ultrasound, and histologic evaluation of the resection margin. Three of the five methods-color, peristalsis, and early histologic findings-did not correlate well with intestinal survival rates. However, Doppler ultrasound and myoelectric assessment measured by the contractility meter were statistically correlated with late intestinal viability. Despite the success of this technique, there is an element of subjectivity in interpreting the quantitative recordings. Artifact on the baseline of the strip chart may be misinterpreted as slow low-amplitude smooth muscle contractions. Brolin and his colleagues are engaged in the development of a modified device with a self-contained microprocessor capable of coordinating multiple functions such as stimulus control, response monitoring, and data display with a built-in feature for rejection of artifactual readings. Clinical application of such a method of myoelectric assessment of intestinal viability is awaited with interest and may prove to be a simple and reliable technique for routine use in the operating room.
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
153
SUMMARY Acute intestinal ischemia and infarction remain serious clinical problems despite early operative intervention. Accurate intraoperative assessment of intestinal viability is essential in determining the limits of resection in patients with intestinal infarction. Clinical features of bowel viability such as color and peristalsis do not correlate uniformly with bowel survival, and as a result, several techniques have been developed to assess intestinal blood flow at the time of operation. The requirements of an ideal viability test are: 1. The technique must have ready availability, preferably in every operating theater dealing with abdominal emergencies. 2. The necessary equipment must not be cumbersome or require specialized personnel. 3. The method must be accurate with a minimum of false-negative results and, more importantly, few false positives. A falsenegative result leaves in situ nonviable bowel, which may lead to early perforation and late stricturing. This situation may be recoverable with further surgical intervention, however. On the other hand, a false-positive assessment of bowel viability results in the resection of potentially recoverable intestine, which is lost forever and may represent a vital difference for morbiditymortality and long-term nutrition. 4. The technique must be objective and be reproducible. 5. The method must be cost effective. To date, only two tests have found widespread acceptance and clinical applicability: fluorescein assessment and Doppler studies either with ultrasound or as refined in laser velocimetry. Although other techniques may be of some value today or in the future, the most practical approach would appear to be to use fluorescein assessment under a modified Wood's lamp as the initial method of evaluating intestinal viability and either Doppler ultrasound or perfusion fluorometry for any areas of particularly doubtful viability.
References 1. Ahn H, Lindhagen J, Nilsson GE, et al: Evaluation of laser Dopp!er flowmetry in the assessment of intestinal blood flow in the cat. Gastroenterology 88:951, 1985 2. Boley 5J, 5prayregen S, Veith FJ: Initial results of an aggressive roentgenologic and surgical approach to acute mesenteric ischemia. Surgery 82:848, 1977 3. Boley SJ, Feinstein FR, Sammartano R. New concept in the management of emboli of the superior mesenteric artery. Surg Gynecol Obstet 153:561, 1981 4. Brolin RE, Semmlow JL, Mackensie JW: Quantitative evaluation of bowel viability. Proc IEEE Front Eng Comput Health Care 6:320, 1984 5. Brolin RE, Semmlow JL, Mackenzie JW, et al: Quantitative myoelectric determination of bowel viability. J 5urg Res 41:557, 1986 6. Brolin RE, 5emmlow JL, Sehonanda A, et al: Comparison of five methods of assessment of intestinal viability. Surg Gynecol Obstet 168:6, 1989
154
HORGAN & GOREY
7. Bulkley G, Zuidema G, Hamilton S, et al: Intraoperative determination of small intestinal viability following ischemic injury. Ann Surg 193:628, 1981 8. Bussemaker JB, Lindeman J: Comparison of methods to determine viability of small intestine. Ann Surg 176:97, 1972 9. Cabot RM, Kohatsu S: The effects of ischaemia on the electrical and contractile activities of the canine small intestine. Am J Surg 136:242, 1978 10. Carter M, Fantani G, Sammartano R, et al: Qualitative and quantitative fluorescence for determining intestinal viability. Am J Surg 147:117, 1984 11. Chou CC: Relationship between intestinal blood flow and motility. Annu Rev Physiol 44:29, 1982 12. Chung RS: Blood flow in colonic anastomoses. Ann Surg 206:335, 1987 13. Clark RA, Gallant TE: Acute mesenteric ischemia: Angiographic spectrum. AJR 142:555, 1984 14. Clavien PA, Muller C, Harder F: Treatment of mesenteric infarction. Br J Surg 74:500, 1987 15. Cooperman M, Martin EW, Carey LC: Evaluation of ischemic intestine by Doppler ultrasound. Am J Surg 139:73, 1980 16. Cooperman M, Pall WG, Martin EW, et al: Determination of viability of ischemic intestine by Doppler ultrasound. Surgery 83:705, 1978 17. De Nobile J, Guzzetta P, Patterson K: Pulse oximetry as a means of assessing bowel viability. J Surg Res 48:21, 1990 18. Dineen P, Goulian 0, McSherry CK: A method of demonstrating intestinal viability. Am J Gastroenterol 45:335, 1966 19. Eldrup-Jorgensen SV, Schwartz SI, Wallace JD: A method for clinical evaluation of peripheral circulation: Photoelectric hemodensitometry. Surgery 59:505, 1966 20. Field AD, Fondacaro JD, Halloway G, et al: Measurement of mucosal blood flow in the canine intestine with laser Doppler velocimetry. Life Sci 31:1509, 1982 21. Gorey TF: Prediction of intestinal recovery after ischaemic injury due to arterial, venous and mixed arterial and venous icclusions. J R Soc Med 73:631, 1980 22. Gorey TF, O'Sullivan M: Prognostic factors in extensive mesenteric ischaemia. Ann R ColI Surg Engl 70:191, 1988 23. Guisan YJ, Hreno A, Gurd FN: Effect of acute ischaemia on the motility of the small bowel in the awake dog. Eur Surg Res 7:32, 1975 24. Herrlin JO [r, Glasser ST, Lange K: New methods for determining the viability of the bowel. Arch Surg 45:785, 1942 25. Katz S, Wahab A, Murray W, et al: New parameters of viability in ischemic bowel disease. Am J Surg 127:136, 1974 26. Khin J, Daniel EE: The effects of ischemia on intestinal nerves and electrical slow waves. Am J Dig Dis 15:959, 1970 27. La Piana FG, Penner R: Anaphylactoid reaction to intravenously administered fluorescein. Arch Ophthalmol 79:161, 1968 28. Locke R, Hauser CJ, Shoemaker WC: The use of surface oximetry to assess bowel viability. Arch Surg 119:1252, 1984 29. Mann A, Fazio VM, Lucas FV: A comparative study of the use of fluorescein and the Doppler device in the determination of intestinal viability. Surg Gynecol Obstet 154:53, 1982 30. Myers MB, Cherry G: Use of vital dyes in the evaluation of the blood supply of the colon. Surg Gynecol Obstet 149:97, 1969 31. Myers MB, Cherry G, Gesser J: Relationship between surface pH and PCO z and the vascularity and viability of the intestine. Surg Gynecol Obstet 134:787, 1972 32. O'Donnell JA, Hobson RW: Operative confirmation of Doppler ultrasound in evaluation of intestinal viability. Surgery 83:705, 1978 33. Oohata Y, Mibu R, Hotokezaka M, et al: Comparison of blood flow assessment between laser Doppler velocimetry and the hydrogen gas clearance method in ischemic intestine in dogs. Am J Surg 160:511, 1990 34. Paes E, Vollmar JF, Hutschenreiter S, et al: Mesenteric infarct: New aspects of diagnosis and therapy. Chirurg 59:828, 1988 35. Papachristou 0, Fortner JG: Prediction of intestinal viability by intraarterial dye injection: A simple test. Am J Surg 132:572, 1976
OPERATIVE ASSESSMENT OF INTESTINAL VIABILITY
155
36. Pearse WH, Jones ON, Warren GH, et al: The use of infrared photoplethysmography in identifying early intestinal ischaemia. Arch Surg 122:308, 1987 37. Rotering RH, Dixon LA, Holloway JA, et al: A comparison of the HeNe laser and ultrasound Doppler systems in the determination of viability of ischemic canine intestine. Ann Surg 196:705, 1982 38. Shepherd AP, Riedel GL: Continuous measurement of intestinal mucosal blood flow by laser Doppler velocimetry. Am J PhysioI242:G668--G672,1982 39. Silverman DG, Murford WE, Cooper HS, et al: Quantification of fluorescein distribution to strangulated rat ileum. J Surg Res 34:179-186, 1983 40. Stolar CJ, Randolf JG: Evaluation of ischaemic bowel viability with a fluorescent technique. J Ped Surg 13:221-225, 1978 41. Thorn FL, Geargiade NG, Wheeler WE, et al: Photopletysmography as an aid in determining the viability of pedicle flaps. Plast Reconstr Surg 44:279, 1969 42. Tremper KK, Shoemaker WC: Transcutaneous oxygen monitoring of critically ill patients with and without low flow shock. Crit Care Med 9:706, 1981 43. Wilson C, Gupta R, Gilmour DG, et al: Acute superior mesenteric ischaemia. Br J Surg 74:279, 1987 44. Wright GB, Hobson RW: Prediction of intestinal viability using Doppler ultrasound techniques. Am J Surg 129:642, 1975
Address reprint requests to Thomas F. Gorey, MCh, FRCSI Department of Surgery Mater Misericordiae Hospital University College Dublin 47 Eccles Street Dublin 7, Ireland
