- Email: [email protected]
Evaluation of ischemic intestine by Doppler ultrasound
Evaluation of lschemic Intestine by Doppler Ultrasound
MD, Columbus,
Marc Cooperman,
Edward
Ohio
W. Martin, Jr., MD, Columbus,
Larry C. Carey, MD, Columbus,
Ohio
Ohio
The viability of ischemic intestine may be extremely di i’ficult to evaluate at operation. Both experimental and clinical studies have shown that clinical criteria of intestinal viability such as bowel color and presence or absence of mesenteric pulsations and peristalsis may be inaccurate [I-7]. Basing operative decisions solely on the clinical appearance of the iscxhemic intestine may result in unnecessary resect ion of viable intestine or, conversely, failure to resect nonviable bowel that undergoes frank infarction. As a result, some surgeons recommend a second-look laparotomy 24 hours after the first operation to reassess bowel of uncertain viability [8]; however, this exposes an often seriously ill patient to the risks of in :+econd major operative procedure. 1,aboratory studies show that Doppler ultrasound is a reliable technique for determining the viability of experimentally created ischemic intestine [ri,Y]. In the experimental animal, Doppler ultrasound has al40 proved sufficiently precise to select the optimal point of’ resection of ischemic small and large intesti,le in order to avoid anastomotic disruption or St ricturr secondary to ischemia [~,Io]. Our study was dtlsignrd to evaluate the clinical usefulness of Doppler ultrasound in the int.raoperative management 01 patients with intestinal &hernia. Material
and Methods
Uuring an IH month period beginning in July 1977, twenty-three patients who underwent laparotomy were found to have intestinal ischemia. Twenty-five segments 01 hmall or large intestine were of’ questionable viability in ! hesr Zi patients. The causes of intestinal &hernia were (+)sed locq~ obstruction (nine patients), incarcerated hernia (five). at herosclerosis (three), volvulus (two), trauma (one), low cardiac output (one), mesenteric venous thrombosis Fwm
the Department
lumbus. Reprint Tenth
requests
Avenue.
Presented Al mentary
Volume
of Surgery.
The Ohio
State
University
Hospitals,
Co-
Ohlo should
at the Tract.
139.
be addressed
Columbus. 20th
New
January
Ohlo Annual Orleans.
1980
to Marc
Cooperman,
MD, 410 West
43210. Meeting Louwana,
of the May
Society
for Surgery
22-23.
1979
of the
(one) and metastatic carcinoma (one patient). Vascular compromise involved the small intestine in 18 patients and the colon in 5 patients. At operation, after the cause of intestinal &hernia was corrected when possible, t,he viability of the involved intestine was initially evaluated by the surgeon according to the clinical criteria of bowel color, peristalsis and mesenteric pulsations. On the basis of these observations, the surgeon made a preliminary decision regarding the viability of the ischemic segment. A 9mHz Doppler pencil probe calibrated to a Doppler flowmeter (Parks Electronics, model 806) was passed along the antimrsenteric surface of the ischemic intestine (Figure I ). Before use, probes were gas-sterilized and the tip was coated with sterile water-soluble gel to enhance contact with the bowel wall. The probe was lightly applied to the intestinal wall at a 45’ angle. Final operative decisions were based solely on the results of the Doppler examination. If arterial flow signals were detected throughout the entire segment of ischemic intestine, the segment was considered viable. II’ arterial flow signals were absent in the wall of the ischemic segment of’ howel, it was considered nonviable and was resected. Margins of’ resection were selected according to IIoppler findings; proximal and distal margins were chosen at the last point along the antimesenteric horder at which an arterial flow signal could be detected. Doppler arterial signals were only judged to be either present or absent; no effort was made to evaluate the arterial wave forms. The presence or absence of venous flow signals within the howel wall was not taken into account in the assessment of intestinal viability. Histologic examination of all resected specrmens was performed. Second-look laparotomies were not perf’ormed. Results
Four segments of ischemic intestine were considered viable on the basis of both clinical criteria and the presence of Dofiler arterial signals. None of these segments was resected, and the uncomplicated postoperative course of the patients confirmed the viability of the involved segments of howel.
73
Cooperman
et al
Technique
~
Figure 1. The Doppler probe is lightly applied at a 45O angle to the bowel wall. Arterial flow signals must be present within the wall of the intestine itself.
Figure 3. Small bowel series obtained in the same patient as in Figure 2. A normal mucosalpattern is present. There is no evidence of stricture or fistula formation.
Figure 2. Severely ischemic small intestine after release of a strangulating obstruction due to adhesions after a staging laparotomy. Doppler arterial signals were clearly audible, and the bowel proved viable.
Nine segments of intestine were judged nonviable on the basis of both clinical criteria and absent Doppler arterial flow signals. All nine were resected, and subsequent histologic examination confirmed either severe ischemia or infarction. Ten segments of ischemic bowel were judged, on the basis of examination by the operating surgeon, to be of extremely doubtful viability and would have been resected on the basis of clinical examination alone. However, Doppler arterial signals were readily detected within the bowel wall of these segments, confirming the presence of arterial flow (Figure 2). Accordingly, none of the segments was resected, and the subsequent benign clinical course of the patients demonstrated the viability of the ischemic area of intestine. Two of these patients, in whom ischemic
74
loops of small intestine secondary to strangulating closed loop obstructions were not resected, passed small amounts of blood by rectum in the early postoperative period. However, small bowel barium radiologic examination 2 to 3 months postoperatively demonstrated normal small intestine with no evidence of stricture or fistula formation (Figure 3). Two segments of intestine were judged clinically to be viable, but Doppler arterial signals were absent. Both of these segments were resected despite their clinical appearance. Histologic examination demonstrated severe ischemic changes in both segments, There was one death in this series of 23 patients, for a mortality of 4.3 percent. It occurred in an elderly woman with severe cardiac failure secondary to aortic valvular regurgitation whose preoperative diagnosis was mesenteric vascular insufficiency. Despite palpable pulsations in the superior mesenteric artery, no Doppler arterial signals could be detected in the wall of the small intestine or the ascending or
The American
Journal
of Surgery
Doppler
1r;t.Isverse colon. The bowel appeared slight,lv dusky itt (olor hut viable. The patient died during the earl!: I)~~~tc)perafi\:e period because of’ cardiac f’ailure. l’()stm()rtem examination confirmed patchy necrosis t tlroughotit the small intestine and the ascending and t r;tns~~erse (melon. Comments ‘I’hr gross appearance ot’ ischemic intestine may he tllisle:tdirq to the surgeon. As clinical experience and exl)eritnental studies have shown, subjective criteria 01’intestinal viability after release of a st,rangulating oh:,tructiort or emholectomy of’ the superior mesenteric. artery tnay he quite inaccurate. Bowel that is tlrtsky in color tnay still have suf’ficient blood flow to he \,inl)le. i\I’ter blood flow is restored, improvement it1 : he grist appearance of’ viable hut severely ischtarnit- howe may he so slow that unnecessary resection k ~)erI’orrnc~d. (‘onversely, bowel in which irreversible vascular thrombosis has occurred may not yet have hacl srtf’t’icirnt time to exhibit the gross appearance ot’ j’rank ittf’arction. !\Jurnerous techniques have been devised to determine ot).jectively the viability of ischemic intestine 11.i.571. However, none has gained wide clinical ;rpl,lic.atiort owing either to the complexity of’ the eytlipmenf or time required or to the lack of’absolute prchdic,t i1.e accuracy. i)opplt~r ultrasound examination is established as an acc~~r~~l.r, rapid technique for assessing arterial :rncl \‘enouh Mood flow. It is widely used in peripheral va~ular disease and, consequently, the necessary +q~tipntent is available in most major hospitals. The I )c’pglrr prohe is gas-st,erilizahle f’or intraoperative I~s(‘. ‘I’he tip should be coated with a st,erile watersoluble gel. It’ it is lightly applied at a 45” angle to the intrst inal wall, arterial and venous flow signals are re;ldily cletected. (:wre tnust be taken not to exert cbxc,es
Volume
139,
January
1980
Ultrasound in Intestinal lschemia
order to avoid anastomotic stricture or disruption secondary to incorporation of’ devitalized tissue into the suture line. The applicability of’ this technique in selecting margins of’ resection of’ ischemic colon has also heen demonstrat,ed experimentally 1III 1,showing that a Doppler arterial signal must he present within 1 cm ot’ the margins of resection to avoid a high incidence of’ anastomot,ic disruption or st rictllre. Our study demonstrat,ed the clinical usefulness of this technique. The return of’ arterial f’l(18wsignals within the ischetnic bowel wall was an a(‘(~ rate index of’ intestinal viability. (‘onversely, t hr absence of’ arterial flow signals was an objective measure of’ irreversible ischemia or infarction. Of’ the 25 segments of ischemic intestine observed in 23 patients, the clinical judgment oft he surgeon based on the gross appearance of’ the howel differed from the 1)oppler ultrasound findings in I :! segments (48 percent ). In each case, the Doppler findings were proved accurate either by the suhseyuent clinical course of’ the patient or by histologic examination of’ the resected specimen. Ten unnecessary resect ions of’viahle intestine were avoided hy the use of’ Doppler ultrasound, and two segments of’irreversihl:\r ischemic int.estine that would otherwise ha\:e heen lef’t within the ahdotnen were resected. In addition, Doppler ultrasound proved accurate in all l:i segments in which the Doppler findings were in agreement with the surgeon’s subjective assessment of’ the viahilit,y of’ the bowel. A second-look laparotomy was not necessary in any patient in this series. FVith this technique, the critical criterion predicting vi,ability of’ischetnic intestine after restoration of blood flow is the presence of’audihle arterial flow signals in the bowel wall itself throughout the ischemic :iegment of’ intestine. \:enous flow signals are easily dift’erentiated f’rom arterial signals and should not he considered decisive. Arterial flow within the mesenteric vessels alone is also not adequate evidence. No ef’f’o’rtwas made in our study to analyze I)oppler arterial wave forms, although such analysis has been usef’ul in peripheral vascular disease. As a predictor of’ intestinal viability. on1y the presence or absence of’ audible arterial flow signals needs 10 he considered. The m;tjor advantages of’ I)oppler ultrasound examination as an objective technique t’or drtermining intestinal viability include its great predic?ive accuracy, its, simplicity and its rapidity ot’ perf’ormance. The use c,f I)oppler ultrasound of’ten reduces operating titne. When arterial flow signals are present,, it. is unnecessary to wait f’or improvement irt i he gross
75
Cooperman
et al
appearance of the bowel. Similarly, when irreversible &hernia is present, the Doppler probe can be used to select viable margins of resection. Our study demonstrated that Doppler ultrasound examination is far more accurate than subjective appraisal of intestinal viability based on the gross appearance of the bowel. We hope that application of this technique in operations for intestinal ischemia will diminish morbidity and mortality. The need for second-look laparotomy should be eliminated. Summary Intraoperative Doppler ultrasound examination of ischemic intestine was used to determine viability and to establish margins of resection, even when the findings differed from the surgeon’s clinical appraisal. Ten of 25 segments in 23 patients were clinically judged nonviable, but because arterial flow within the segments was detected by Doppler ultrasound, none was resected. The subsequent benign clinical courses of the patients demonstrated the viability of the segments. Two segments were judged clinically viable, but because Doppler signals were absent, both were resected. Histologic examination demonstrated severe ischemic changes in both segments. Nine segments were judged both by clinical criteria and by Doppler ultrasound examination to be nonviable, and all nine were resected. Histologic examination confirmed ischemia or infarction in all. Doppler ultrasound was a more reliable intraoperative predictor of viability of ischemic intestine than clinical assessment alone, and its use averted postoperative complications and unnecessary second-look procedures. References 1. Bussemaker JB, Lindeman J. Comparison of methods to determine viability of small intestine. Ann Surg 1972; 176: 97. 2. Glotzer DJ, Villegas AH, Anekamaya S, Shaw RS. Healing of the intestine in experimental bowel infarction. Ann Surg 1962; 155:183. 3. Jensen CB, Smith GA. Clinical study of 51 cases of mesenteric infarction. Surgery 1956; 40:930. 4. Katz S. Wahab A, Murray W, Williams L. New parameters of viability in ischemic bowel disease. Am J Surg 1974; 127: 136. 5. Moosa AR, Skinner DB, Stark U, Hoffer P. Assessment of bowel viability using technetium-tagged albumin microspheres. J Surg Res 1974; 16:466. 6. Wright CB. Hobson RW. Prediction of intestinal viability using Doppler ultrasound technics. Am J Surg 1975; 129:642. 7. Zarins CK, Skinner DB, Rhodes BA, Janes AE. Prediction of the viability of revascularized intestine with radioactive microspheres. Surg Gynecol Obstet 1974; 138:676. 8. Boley SJ. Schwartz SS, Williams LF. Vascular disorders of the
76
intestine. New York: Appleton-Century-Crofts, 197 1:5 16. 9. Cooperman M, Pace WG, Martin EW Jr, Pflug B, Keith LM, Evans WE, Carey LC. Determination of viability of ischemic intestine by Doppler ultrasound. Surgery 1978; 83:705. 10. Cooperman M, Martin EW Jr, Evans WE, Carey LC. Assessment of anastomotic blood supply by Doppler ultrasound in operations upon the colon. Surg Gynecol Obstet 1979; 149: 15.
Discussion Abdool R. Moossa (Chicago, IL): The problem of the potentially ischemic bowel can be divided into three sections. The obviously gangrenous bowel segment or the obviously viable one presents no difficulty to the operating surgeon. It is the “doubtful” segment which is edematous and hemorrhagic after revascularization that creates a dilemma; clinical assessment in this situation may be erroneous. The authors had only 12 patients in this third category. They resected 2 bowel segments and left 10 behind; fortunately all the patients had an uneventful recovery. I disagree somewhat with their experimental design. I would rather that they had assessed these bowel segments clinically, looked at the Doppler “results” and put everything back in all cases. Then they should have performed a second-look laparotomy in all 12 patients. We would then have known for certain the relative merits of the Doppler versus clinical assessment. At the moment their data are highly suggestive but by no means conclusive. If the thesis proves true, they have given us a quick and simple solution to a difficult problem in the operating room and the Doppler will become a valuable addition to the general surgeon’s operative armamentarium. One other word of caution. Some of Dr. Cooperman’s patients have been followed up for only a short time, especially those who had bloody diarrhea postoperatively; they may still present with stenotic bowel at a later date. I have three questions for Dr. Cooperman: First, how does he manage patients with mesenteric venous thrombosis? Second, has he looked at the Doppler pattern of a routine bowel anastomosis? Third, what does a “flattening” in the Doppler wave form signify clinically?
M. Michael Eisenberg (Minneapolis, MN): I congratulate Drs. Cooperman, Martin and Carey on their innovative approach to the use of the Doppler in the evaluation of potentially morbid bowel. I have some reservations concerning this technique. Ischemic bowel is notoriously progressive; one potential problem in this regard includes the possibility that while during operation the Doppler may give a positive flow finding, within a matter of hours or a day or two progression of the underlying disorder may cause infarction and may require a second-look operation. The second reservation I have concerns a rather large group of patients with ischemic bowel with whom we come in contact but who were not on your list: those patients who have cardiac arrhythmia, those who are taking digitalis preparations or vasopressors, and those who infarct their
The American Journal of Surgery
Doppler Ultrasound
t)owel. These
patients’ bowel tissues, when examined by show no evidence of large or even medillm-sized arterial involvement, but only end-artery and cazillary involvement. I would appreciate knowing whether you think the Doppler flow that you measure provides any re.ll insight as to the level of small vessel disease. Yinally. in the patient with 4 or 6 feet of questionable t)( wel, is it possible to use the Doppler to effectively examine every area of bowel? Patchy necrosis, for example, is Jways a possibility in these patients, as is mucosal slough without serosal and muscularis involvement.. I wonder if’the risk in using the Doppler technique in a la ‘ge number of patients will be significantly different t,han that of resection and primary anastomosis on questionable t)owrl of a short length. I realize that it is another situation if there is a midgut volvulus with involvement of everything l’rt)rn the ligament of’ Treitz to the ileocecal valve, but with sl-art segments of bowel are you saving the patient signific.mt risk? Alternatively, is the risk of reoperation for a second look (which I do not particularly endorse) significantly worse than t,he risk one takes using a really indirect technique?
t h.2 pathologist,
Nathaniel M. Matolo (Davis, CA): Are you using this technique in patients undergoing resection of an abdominal aortic aneurysm to determine whether the blood flow is adequate after ligation of the inferior mesenteric artery? Paul H. Jordan, Jr. (Houston, TX): In peripheral vascular disease Doppler ultrasound seems to play its most important role when the pressure is known. Is the Doppler an effective measurement when the pressure in the gut is n4)t knowll? Dr. Cabot (Denver, CO): I agree with Dr. Eisenberg about the problem of incomplete mesenteric insufficiency and the problem it poses to the surgeon intraoperatively. I ,Nould like to ask Dr. Cooperman to comment further on the exact nature of his method: are audible pulsatile sounds 1,:; the Doppler sufficient evidence of viability? Marc Cooperman (closing): Two patients in our study d d pass some gross blood by rectum postoperatively. Roth of’ these patients had large areas of ischemic small intestine ir which LQpler signals were present. A small bowel series was obtained in these patients 3 and 6 months postoperatively. and both were entirely normal. In answer to Dr. Moossa’s questions about whether this is useful in venous infarction, we feel it is. We have done an experimental study in which the venous drainage of’ a I(~op of intestine was occluded, and we found that in a relal ivcly short time Doppler arterial signals disappeared within the bowel wall. On release of the occluding clamp o 1 t.he venous drainage in those loops of bowel that subsequently proved viable, L)oppler arterial signals within the h )WPI WillI itself returned.
Volume
139, January
1980
in Intestinal
lschemia
We have used this technique in routine screening of intestinal anastomoses. We have a series 01’ 1% small and large bowel resections in which the operating surgeon chose the initial points of resection based on the appearance of the bowel and then checked the margins with the Doppler hoth before and after completion of t,he anastomo,sis. In this study 8 of the 1% patients were found to have absent Doppler arterial signals on one side of the anast omosis. and these anas omoses were immediately revised. An additional ;i to 1‘Linches of bowel were resected in order tg) go hack to an easily alldible arterial flow signal. In one patient, despite the absence of arterial signals, the operating surgeon felt the howrl looked sufficiently viable to leave it in place. Seven days later the patient underwent rrexploration for peritonitis and leakage from the anastomosis was found. In answer to the question of whether the wave form is important. we have found that it is not. The I)oppler findings predictive of viability appear to be an all-or-none phenomenon. The presence 01’arterial flow signals. even if they are reduced in caliber, indicates sufficient flow for subsequent intestinal viability. In regard to Dr. Eisenberg’s questions, I am certain that in some disease processes there is underlying progression of the intestinal ischemia. The majority of’patients we dealt with had I.,losed loop obstructions from adhesions or superior mesenteric artery emboli which, once corrected, should not be progressive. (“ertainly a I)opplrr arterial reading of the bowel wall at one point in time I:ould not he assumed t#r)be equally predictive in a patient. with ischemia hased on low flow. 1l:e feel we are measuring extremely small vessels in this study because these are the vessels present within the bowel wall itself’, and readings are taken (In the antimesentrric, surface where the vascular supply is the most precarious. We do not pay any attention to finl:iings within the mesenteric arcade itself, but depend on flow within the bowel wall. 1 think t,he second-look procedure does hold some risk; one sul)jrcts a critically ill patient to a majln- operative procedure. Certainly if any of the patients in whom we left ischemic: intestine within the abdominal cavity had deteriorated clinically, we would have performed a second look to reassess bowel viability. Fortunately. all of these patients did so well that this was unnecessary. Yes. we have used this technique in patients undergoing resection of abdominal aneurysms. I)rs. M’right and Hobson have used this as well, and found that if t Ihere is loss of’ arterial si;:nals within the sigmoid colon when the inferior mesentrric. artery is ligated, the inf’erior mesenteric, Lressel should be reimplanted. The I)oppler appears to be eff’ect ivri without pressure measurements or wave forms. As I said, it appears to be an all-or-norle phenomenon, and the only thing ncJcessary to know is njhether arterial flow is present.
77
MD, Columbus,
Marc Cooperman,
Edward
Ohio
W. Martin, Jr., MD, Columbus,
Larry C. Carey, MD, Columbus,
Ohio
Ohio
The viability of ischemic intestine may be extremely di i’ficult to evaluate at operation. Both experimental and clinical studies have shown that clinical criteria of intestinal viability such as bowel color and presence or absence of mesenteric pulsations and peristalsis may be inaccurate [I-7]. Basing operative decisions solely on the clinical appearance of the iscxhemic intestine may result in unnecessary resect ion of viable intestine or, conversely, failure to resect nonviable bowel that undergoes frank infarction. As a result, some surgeons recommend a second-look laparotomy 24 hours after the first operation to reassess bowel of uncertain viability [8]; however, this exposes an often seriously ill patient to the risks of in :+econd major operative procedure. 1,aboratory studies show that Doppler ultrasound is a reliable technique for determining the viability of experimentally created ischemic intestine [ri,Y]. In the experimental animal, Doppler ultrasound has al40 proved sufficiently precise to select the optimal point of’ resection of ischemic small and large intesti,le in order to avoid anastomotic disruption or St ricturr secondary to ischemia [~,Io]. Our study was dtlsignrd to evaluate the clinical usefulness of Doppler ultrasound in the int.raoperative management 01 patients with intestinal &hernia. Material
and Methods
Uuring an IH month period beginning in July 1977, twenty-three patients who underwent laparotomy were found to have intestinal ischemia. Twenty-five segments 01 hmall or large intestine were of’ questionable viability in ! hesr Zi patients. The causes of intestinal &hernia were (+)sed locq~ obstruction (nine patients), incarcerated hernia (five). at herosclerosis (three), volvulus (two), trauma (one), low cardiac output (one), mesenteric venous thrombosis Fwm
the Department
lumbus. Reprint Tenth
requests
Avenue.
Presented Al mentary
Volume
of Surgery.
The Ohio
State
University
Hospitals,
Co-
Ohlo should
at the Tract.
139.
be addressed
Columbus. 20th
New
January
Ohlo Annual Orleans.
1980
to Marc
Cooperman,
MD, 410 West
43210. Meeting Louwana,
of the May
Society
for Surgery
22-23.
1979
of the
(one) and metastatic carcinoma (one patient). Vascular compromise involved the small intestine in 18 patients and the colon in 5 patients. At operation, after the cause of intestinal &hernia was corrected when possible, t,he viability of the involved intestine was initially evaluated by the surgeon according to the clinical criteria of bowel color, peristalsis and mesenteric pulsations. On the basis of these observations, the surgeon made a preliminary decision regarding the viability of the ischemic segment. A 9mHz Doppler pencil probe calibrated to a Doppler flowmeter (Parks Electronics, model 806) was passed along the antimrsenteric surface of the ischemic intestine (Figure I ). Before use, probes were gas-sterilized and the tip was coated with sterile water-soluble gel to enhance contact with the bowel wall. The probe was lightly applied to the intestinal wall at a 45’ angle. Final operative decisions were based solely on the results of the Doppler examination. If arterial flow signals were detected throughout the entire segment of ischemic intestine, the segment was considered viable. II’ arterial flow signals were absent in the wall of the ischemic segment of’ howel, it was considered nonviable and was resected. Margins of’ resection were selected according to IIoppler findings; proximal and distal margins were chosen at the last point along the antimesenteric horder at which an arterial flow signal could be detected. Doppler arterial signals were only judged to be either present or absent; no effort was made to evaluate the arterial wave forms. The presence or absence of venous flow signals within the howel wall was not taken into account in the assessment of intestinal viability. Histologic examination of all resected specrmens was performed. Second-look laparotomies were not perf’ormed. Results
Four segments of ischemic intestine were considered viable on the basis of both clinical criteria and the presence of Dofiler arterial signals. None of these segments was resected, and the uncomplicated postoperative course of the patients confirmed the viability of the involved segments of howel.
73
Cooperman
et al
Technique
~
Figure 1. The Doppler probe is lightly applied at a 45O angle to the bowel wall. Arterial flow signals must be present within the wall of the intestine itself.
Figure 3. Small bowel series obtained in the same patient as in Figure 2. A normal mucosalpattern is present. There is no evidence of stricture or fistula formation.
Figure 2. Severely ischemic small intestine after release of a strangulating obstruction due to adhesions after a staging laparotomy. Doppler arterial signals were clearly audible, and the bowel proved viable.
Nine segments of intestine were judged nonviable on the basis of both clinical criteria and absent Doppler arterial flow signals. All nine were resected, and subsequent histologic examination confirmed either severe ischemia or infarction. Ten segments of ischemic bowel were judged, on the basis of examination by the operating surgeon, to be of extremely doubtful viability and would have been resected on the basis of clinical examination alone. However, Doppler arterial signals were readily detected within the bowel wall of these segments, confirming the presence of arterial flow (Figure 2). Accordingly, none of the segments was resected, and the subsequent benign clinical course of the patients demonstrated the viability of the ischemic area of intestine. Two of these patients, in whom ischemic
74
loops of small intestine secondary to strangulating closed loop obstructions were not resected, passed small amounts of blood by rectum in the early postoperative period. However, small bowel barium radiologic examination 2 to 3 months postoperatively demonstrated normal small intestine with no evidence of stricture or fistula formation (Figure 3). Two segments of intestine were judged clinically to be viable, but Doppler arterial signals were absent. Both of these segments were resected despite their clinical appearance. Histologic examination demonstrated severe ischemic changes in both segments, There was one death in this series of 23 patients, for a mortality of 4.3 percent. It occurred in an elderly woman with severe cardiac failure secondary to aortic valvular regurgitation whose preoperative diagnosis was mesenteric vascular insufficiency. Despite palpable pulsations in the superior mesenteric artery, no Doppler arterial signals could be detected in the wall of the small intestine or the ascending or
The American
Journal
of Surgery
Doppler
1r;t.Isverse colon. The bowel appeared slight,lv dusky itt (olor hut viable. The patient died during the earl!: I)~~~tc)perafi\:e period because of’ cardiac f’ailure. l’()stm()rtem examination confirmed patchy necrosis t tlroughotit the small intestine and the ascending and t r;tns~~erse (melon. Comments ‘I’hr gross appearance ot’ ischemic intestine may he tllisle:tdirq to the surgeon. As clinical experience and exl)eritnental studies have shown, subjective criteria 01’intestinal viability after release of a st,rangulating oh:,tructiort or emholectomy of’ the superior mesenteric. artery tnay he quite inaccurate. Bowel that is tlrtsky in color tnay still have suf’ficient blood flow to he \,inl)le. i\I’ter blood flow is restored, improvement it1 : he grist appearance of’ viable hut severely ischtarnit- howe may he so slow that unnecessary resection k ~)erI’orrnc~d. (‘onversely, bowel in which irreversible vascular thrombosis has occurred may not yet have hacl srtf’t’icirnt time to exhibit the gross appearance ot’ j’rank ittf’arction. !\Jurnerous techniques have been devised to determine ot).jectively the viability of ischemic intestine 11.i.571. However, none has gained wide clinical ;rpl,lic.atiort owing either to the complexity of’ the eytlipmenf or time required or to the lack of’absolute prchdic,t i1.e accuracy. i)opplt~r ultrasound examination is established as an acc~~r~~l.r, rapid technique for assessing arterial :rncl \‘enouh Mood flow. It is widely used in peripheral va~ular disease and, consequently, the necessary +q~tipntent is available in most major hospitals. The I )c’pglrr prohe is gas-st,erilizahle f’or intraoperative I~s(‘. ‘I’he tip should be coated with a st,erile watersoluble gel. It’ it is lightly applied at a 45” angle to the intrst inal wall, arterial and venous flow signals are re;ldily cletected. (:wre tnust be taken not to exert cbxc,es
Volume
139,
January
1980
Ultrasound in Intestinal lschemia
order to avoid anastomotic stricture or disruption secondary to incorporation of’ devitalized tissue into the suture line. The applicability of’ this technique in selecting margins of’ resection of’ ischemic colon has also heen demonstrat,ed experimentally 1III 1,showing that a Doppler arterial signal must he present within 1 cm ot’ the margins of resection to avoid a high incidence of’ anastomot,ic disruption or st rictllre. Our study demonstrat,ed the clinical usefulness of this technique. The return of’ arterial f’l(18wsignals within the ischetnic bowel wall was an a(‘(~ rate index of’ intestinal viability. (‘onversely, t hr absence of’ arterial flow signals was an objective measure of’ irreversible ischemia or infarction. Of’ the 25 segments of ischemic intestine observed in 23 patients, the clinical judgment oft he surgeon based on the gross appearance of’ the howel differed from the 1)oppler ultrasound findings in I :! segments (48 percent ). In each case, the Doppler findings were proved accurate either by the suhseyuent clinical course of’ the patient or by histologic examination of’ the resected specimen. Ten unnecessary resect ions of’viahle intestine were avoided hy the use of’ Doppler ultrasound, and two segments of’irreversihl:\r ischemic int.estine that would otherwise ha\:e heen lef’t within the ahdotnen were resected. In addition, Doppler ultrasound proved accurate in all l:i segments in which the Doppler findings were in agreement with the surgeon’s subjective assessment of’ the viahilit,y of’ the bowel. A second-look laparotomy was not necessary in any patient in this series. FVith this technique, the critical criterion predicting vi,ability of’ischetnic intestine after restoration of blood flow is the presence of’audihle arterial flow signals in the bowel wall itself throughout the ischemic :iegment of’ intestine. \:enous flow signals are easily dift’erentiated f’rom arterial signals and should not he considered decisive. Arterial flow within the mesenteric vessels alone is also not adequate evidence. No ef’f’o’rtwas made in our study to analyze I)oppler arterial wave forms, although such analysis has been usef’ul in peripheral vascular disease. As a predictor of’ intestinal viability. on1y the presence or absence of’ audible arterial flow signals needs 10 he considered. The m;tjor advantages of’ I)oppler ultrasound examination as an objective technique t’or drtermining intestinal viability include its great predic?ive accuracy, its, simplicity and its rapidity ot’ perf’ormance. The use c,f I)oppler ultrasound of’ten reduces operating titne. When arterial flow signals are present,, it. is unnecessary to wait f’or improvement irt i he gross
75
Cooperman
et al
appearance of the bowel. Similarly, when irreversible &hernia is present, the Doppler probe can be used to select viable margins of resection. Our study demonstrated that Doppler ultrasound examination is far more accurate than subjective appraisal of intestinal viability based on the gross appearance of the bowel. We hope that application of this technique in operations for intestinal ischemia will diminish morbidity and mortality. The need for second-look laparotomy should be eliminated. Summary Intraoperative Doppler ultrasound examination of ischemic intestine was used to determine viability and to establish margins of resection, even when the findings differed from the surgeon’s clinical appraisal. Ten of 25 segments in 23 patients were clinically judged nonviable, but because arterial flow within the segments was detected by Doppler ultrasound, none was resected. The subsequent benign clinical courses of the patients demonstrated the viability of the segments. Two segments were judged clinically viable, but because Doppler signals were absent, both were resected. Histologic examination demonstrated severe ischemic changes in both segments. Nine segments were judged both by clinical criteria and by Doppler ultrasound examination to be nonviable, and all nine were resected. Histologic examination confirmed ischemia or infarction in all. Doppler ultrasound was a more reliable intraoperative predictor of viability of ischemic intestine than clinical assessment alone, and its use averted postoperative complications and unnecessary second-look procedures. References 1. Bussemaker JB, Lindeman J. Comparison of methods to determine viability of small intestine. Ann Surg 1972; 176: 97. 2. Glotzer DJ, Villegas AH, Anekamaya S, Shaw RS. Healing of the intestine in experimental bowel infarction. Ann Surg 1962; 155:183. 3. Jensen CB, Smith GA. Clinical study of 51 cases of mesenteric infarction. Surgery 1956; 40:930. 4. Katz S. Wahab A, Murray W, Williams L. New parameters of viability in ischemic bowel disease. Am J Surg 1974; 127: 136. 5. Moosa AR, Skinner DB, Stark U, Hoffer P. Assessment of bowel viability using technetium-tagged albumin microspheres. J Surg Res 1974; 16:466. 6. Wright CB. Hobson RW. Prediction of intestinal viability using Doppler ultrasound technics. Am J Surg 1975; 129:642. 7. Zarins CK, Skinner DB, Rhodes BA, Janes AE. Prediction of the viability of revascularized intestine with radioactive microspheres. Surg Gynecol Obstet 1974; 138:676. 8. Boley SJ. Schwartz SS, Williams LF. Vascular disorders of the
76
intestine. New York: Appleton-Century-Crofts, 197 1:5 16. 9. Cooperman M, Pace WG, Martin EW Jr, Pflug B, Keith LM, Evans WE, Carey LC. Determination of viability of ischemic intestine by Doppler ultrasound. Surgery 1978; 83:705. 10. Cooperman M, Martin EW Jr, Evans WE, Carey LC. Assessment of anastomotic blood supply by Doppler ultrasound in operations upon the colon. Surg Gynecol Obstet 1979; 149: 15.
Discussion Abdool R. Moossa (Chicago, IL): The problem of the potentially ischemic bowel can be divided into three sections. The obviously gangrenous bowel segment or the obviously viable one presents no difficulty to the operating surgeon. It is the “doubtful” segment which is edematous and hemorrhagic after revascularization that creates a dilemma; clinical assessment in this situation may be erroneous. The authors had only 12 patients in this third category. They resected 2 bowel segments and left 10 behind; fortunately all the patients had an uneventful recovery. I disagree somewhat with their experimental design. I would rather that they had assessed these bowel segments clinically, looked at the Doppler “results” and put everything back in all cases. Then they should have performed a second-look laparotomy in all 12 patients. We would then have known for certain the relative merits of the Doppler versus clinical assessment. At the moment their data are highly suggestive but by no means conclusive. If the thesis proves true, they have given us a quick and simple solution to a difficult problem in the operating room and the Doppler will become a valuable addition to the general surgeon’s operative armamentarium. One other word of caution. Some of Dr. Cooperman’s patients have been followed up for only a short time, especially those who had bloody diarrhea postoperatively; they may still present with stenotic bowel at a later date. I have three questions for Dr. Cooperman: First, how does he manage patients with mesenteric venous thrombosis? Second, has he looked at the Doppler pattern of a routine bowel anastomosis? Third, what does a “flattening” in the Doppler wave form signify clinically?
M. Michael Eisenberg (Minneapolis, MN): I congratulate Drs. Cooperman, Martin and Carey on their innovative approach to the use of the Doppler in the evaluation of potentially morbid bowel. I have some reservations concerning this technique. Ischemic bowel is notoriously progressive; one potential problem in this regard includes the possibility that while during operation the Doppler may give a positive flow finding, within a matter of hours or a day or two progression of the underlying disorder may cause infarction and may require a second-look operation. The second reservation I have concerns a rather large group of patients with ischemic bowel with whom we come in contact but who were not on your list: those patients who have cardiac arrhythmia, those who are taking digitalis preparations or vasopressors, and those who infarct their
The American Journal of Surgery
Doppler Ultrasound
t)owel. These
patients’ bowel tissues, when examined by show no evidence of large or even medillm-sized arterial involvement, but only end-artery and cazillary involvement. I would appreciate knowing whether you think the Doppler flow that you measure provides any re.ll insight as to the level of small vessel disease. Yinally. in the patient with 4 or 6 feet of questionable t)( wel, is it possible to use the Doppler to effectively examine every area of bowel? Patchy necrosis, for example, is Jways a possibility in these patients, as is mucosal slough without serosal and muscularis involvement.. I wonder if’the risk in using the Doppler technique in a la ‘ge number of patients will be significantly different t,han that of resection and primary anastomosis on questionable t)owrl of a short length. I realize that it is another situation if there is a midgut volvulus with involvement of everything l’rt)rn the ligament of’ Treitz to the ileocecal valve, but with sl-art segments of bowel are you saving the patient signific.mt risk? Alternatively, is the risk of reoperation for a second look (which I do not particularly endorse) significantly worse than t,he risk one takes using a really indirect technique?
t h.2 pathologist,
Nathaniel M. Matolo (Davis, CA): Are you using this technique in patients undergoing resection of an abdominal aortic aneurysm to determine whether the blood flow is adequate after ligation of the inferior mesenteric artery? Paul H. Jordan, Jr. (Houston, TX): In peripheral vascular disease Doppler ultrasound seems to play its most important role when the pressure is known. Is the Doppler an effective measurement when the pressure in the gut is n4)t knowll? Dr. Cabot (Denver, CO): I agree with Dr. Eisenberg about the problem of incomplete mesenteric insufficiency and the problem it poses to the surgeon intraoperatively. I ,Nould like to ask Dr. Cooperman to comment further on the exact nature of his method: are audible pulsatile sounds 1,:; the Doppler sufficient evidence of viability? Marc Cooperman (closing): Two patients in our study d d pass some gross blood by rectum postoperatively. Roth of’ these patients had large areas of ischemic small intestine ir which LQpler signals were present. A small bowel series was obtained in these patients 3 and 6 months postoperatively. and both were entirely normal. In answer to Dr. Moossa’s questions about whether this is useful in venous infarction, we feel it is. We have done an experimental study in which the venous drainage of’ a I(~op of intestine was occluded, and we found that in a relal ivcly short time Doppler arterial signals disappeared within the bowel wall. On release of the occluding clamp o 1 t.he venous drainage in those loops of bowel that subsequently proved viable, L)oppler arterial signals within the h )WPI WillI itself returned.
Volume
139, January
1980
in Intestinal
lschemia
We have used this technique in routine screening of intestinal anastomoses. We have a series 01’ 1% small and large bowel resections in which the operating surgeon chose the initial points of resection based on the appearance of the bowel and then checked the margins with the Doppler hoth before and after completion of t,he anastomo,sis. In this study 8 of the 1% patients were found to have absent Doppler arterial signals on one side of the anast omosis. and these anas omoses were immediately revised. An additional ;i to 1‘Linches of bowel were resected in order tg) go hack to an easily alldible arterial flow signal. In one patient, despite the absence of arterial signals, the operating surgeon felt the howrl looked sufficiently viable to leave it in place. Seven days later the patient underwent rrexploration for peritonitis and leakage from the anastomosis was found. In answer to the question of whether the wave form is important. we have found that it is not. The I)oppler findings predictive of viability appear to be an all-or-none phenomenon. The presence 01’arterial flow signals. even if they are reduced in caliber, indicates sufficient flow for subsequent intestinal viability. In regard to Dr. Eisenberg’s questions, I am certain that in some disease processes there is underlying progression of the intestinal ischemia. The majority of’patients we dealt with had I.,losed loop obstructions from adhesions or superior mesenteric artery emboli which, once corrected, should not be progressive. (“ertainly a I)opplrr arterial reading of the bowel wall at one point in time I:ould not he assumed t#r)be equally predictive in a patient. with ischemia hased on low flow. 1l:e feel we are measuring extremely small vessels in this study because these are the vessels present within the bowel wall itself’, and readings are taken (In the antimesentrric, surface where the vascular supply is the most precarious. We do not pay any attention to finl:iings within the mesenteric arcade itself, but depend on flow within the bowel wall. 1 think t,he second-look procedure does hold some risk; one sul)jrcts a critically ill patient to a majln- operative procedure. Certainly if any of the patients in whom we left ischemic: intestine within the abdominal cavity had deteriorated clinically, we would have performed a second look to reassess bowel viability. Fortunately. all of these patients did so well that this was unnecessary. Yes. we have used this technique in patients undergoing resection of abdominal aneurysms. I)rs. M’right and Hobson have used this as well, and found that if t Ihere is loss of’ arterial si;:nals within the sigmoid colon when the inferior mesentrric. artery is ligated, the inf’erior mesenteric, Lressel should be reimplanted. The I)oppler appears to be eff’ect ivri without pressure measurements or wave forms. As I said, it appears to be an all-or-norle phenomenon, and the only thing ncJcessary to know is njhether arterial flow is present.
77