Eur J Cardiothorac Surg 2005;28:871-876
© 2005 Elsevier Science NL
Perioperative diagnosis of mesenteric ischemia in acute aortic dissection by transesophageal echocardiography
Kazumasa Orihashi
*
,
Taijiro Sueda,
Kenji Okada,
Katsuhiko Imai
Division of Cardiovascular Surgery, Hiroshima University Hospital, Kasumi 1-2-3, Minami-ku, Hiroshima 734-8551, Japan
Received 28 April 2005;
received in revised form 15 September 2005;
accepted 28 September 2005.
* Corresponding author. Tel.: +81 82 257 5216; fax: +81 82 257 5219. (Email: orichan{at}hiroshima-u.ac.jp).
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Abstract
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Objective: Although computed tomography, angiography, or magnetic resonance imaging is most commonly used for diagnosing mesenteric ischemia caused by acute aortic dissection, use of these modalities is often limited in the perioperative period. Thus, we have introduced transesophageal echocardiography to cover this deficit. Purpose of this study is to report the feasibility and accuracy of transesophageal echocardiographic diagnosis on mesenteric ischemia. Methods: The consecutive 24 cases with acute aortic dissection which involved abdominal aorta and underwent surgery were examined. The celiac artery and superior mesenteric artery was visualized with 5 MHz biplane transesophageal echocardiography and was assessed for presence of dissection and blood flow in each of true and false lumen. The transesophageal echocardiographic findings were then correlated to the clinical course, computed tomographic findings, and laboratory data. Results: The celiac artery and superior mesenteric artery was successfully visualized in 24 cases (100%) and 23 cases (95.8%), respectively. Perfusion patterns in superior mesenteric artery were categorized into four patterns: (1) intact artery with adequate perfusion (type A: 14 cases); (2) dissection in the artery but with adequate perfusion in true lumen (type B: 5 cases); (3) dissection in the artery with narrowed true lumen compressed by false lumen without detectable blood flow (type C: 1 case); and (4) obstruction of arterial orifice by the intimal flap with narrowed true lumen in the proximal aorta (type D: 2 cases). One case with immediate postoperative death and another case with unsuccessful visualization of superior mesenteric artery were excluded from the analysis. Clinically apparent intestinal ischemia was present in three cases: one case with type C and two cases with type D, but in none of the remaining 19 cases with type A or type B (both sensitivity and specificity were 100%). The superior mesenteric artery was opacified in all of these three cases with ischemia. Conclusions: The transesophageal echocardiographic assessment is feasible in nearly all patients and potentially provides correct diagnosis on intestinal ischemia in the perioperative period of acute aortic dissection. Types C and D indicate significant mesenteric malperfusion.
Key Words: Aorta • Echocardiography • Ischemia
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1. Introduction
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Although intestinal necrosis is one of the factors that lead to a poor prognosis in cases of aortic dissection [1–3], apparent findings are often absent on physical examination until the intestines become necrotic, when it is too late to avoid resection of a large portion of intestine and multiple organ failure often develops. Computed tomography (CT), angiography, or magnetic resonance imaging (MRI) provides information on the presence and extent of dissection and potentially facilitates an early diagnosis of visceral malperfusion. However, use of these modalities are often hesitated when the patient is anuric or hemodynamically unstable as is often the case in acute aortic dissection. Intraoperatively, progressive or sustained metabolic acidosis often develops, especially during cardiopulmonary bypass, and suggests presence or mesenteric ischemia. However, none of the above modalities is available in the operating room to determine whether ischemia is present or not.
To overcome these limitations, we focused attention on transesophageal echocardiography (TEE), which had been used for monitoring the thoracic aorta during the surgical management of aortic dissection [4–6], and expanded its use to the abdominal aorta and visceral branch arteries that had been considered to be a blind zone for TEE. In 1997, we reported the techniques for visualizing the celiac artery (CEA) and superior mesenteric artery (SMA) in the majority of patients [7,8]. Reversible intestinal ischemia could be diagnosed with TEE in a patient with type IIIb aortic dissection under antihypertensive therapy [9]. However, the TEE criteria on diagnosing mesenteric ischemia in the surgical cases have not been established yet. The purpose of this study is to examine the feasibility of TEE assessment on visceral arteries and to evaluate the accuracy of TEE diagnosis in a series of surgical cases with acute aortic dissection.
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2. Materials and methods
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We examined the 24 consecutive patients of acute aortic dissection that involved the abdominal aorta and surgically treated between 1997 and 2004 (Table 1
). A total of 31 cases in the same period were excluded from the study because the abdominal aorta was not involved by the preoperative CT assessment. These 24 cases included 13 males and 11 females, with ages ranging from 38 to 84 years old. The Stanford classification of aortic dissection was type A in 17 cases and type B in 7 cases. There was a retrograde extension of dissection to the aortic arch or ascending aorta in four of the seven cases with type B dissection. Eight of the 24 cases (33.3%) were hemodynamically unstable on admission due to pericardial tamponade, rupture, or acute myocardial infarction. Surgical procedures were replacement of ascending aorta, ascending to arch replacement, total arch replacement and/or transaortic stent graft implantation, replacement of descending aorta, and ilio-SMA bypass in 11, 5, 5, 2, and 1 case(s), respectively. Coronary artery bypass grafting was added in four cases. This study was approved by the institutional ethics committee on human research in our institute and informed consent was obtained from every patient.
A 5 MHz biplane TEE system (EUB-555, Hitachi, Co., Tokyo, Japan) was instituted after induction of anesthesia and was used for visualizing the abdominal aorta as previously reported [7,8]. Starting from the short-axis view of descending thoracic aorta, the TEE probe was advanced into the stomach with a counterclockwise rotation to keep the image of the aorta in view. An upward and leftward flexion of the probe tip was often needed to optimize the contact of TEE transducer to the gastric mucosa and to proximate the transducer to the aorta because the probe tip tends to be directed toward left at the cardia. The CEA appeared first at the 12 to 2 o’clock position relative to the aorta. As the probe was further advanced by a few centimeters, the CEA disappeared and then the SMA appeared instead in a similar direction relative to the aorta. As the probe was further advanced, the renal arteries could be occasionally visualized. When the image quality was inadequate due to attenuation of ultrasound, the frequency of ultrasound was lowered to 3.75 MHz. The abdominal aorta and visceral branch arteries were examined for dissection (presence of intimal flap) in two-dimensional echocardiography and for malperfusion (absence or narrowing of the flow signal) in color Doppler imaging. No echo contrast agents were needed.
Perfusion patterns in the CEA and SMA were categorized into four types (Fig. 1
): (1) type A: no dissection in the CEA/SMA with blood flow detectable in the entire portion of its lumen; (2) type B: dissection extending into the CEA/SMA with patent and dominant true lumen associated with small non-perfused or perfused false lumen; (3) type C: dissection extending into the CEA/SMA with narrowed true lumen (less than half of its lumen) compressed by false lumen without detectable blood flow; and (4) type D: no dissection in the CEA/SMA but the orifice obstructed by the intimal flap in the aorta. The abdominal aorta and visceral arteries were examined routinely at three time points (before, during, and after cardiopulmonary bypass), and whenever visceral malperfusion was suspected.
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Fig. 1. Schematic illustrations demonstrating four perfusion patterns of visceral arteries. Type A: no dissection in the branch artery with detectable blood flow. Type B: dissection extending into the branch artery with patent and dominant true lumen (TL) associated with small non-perfused (type B1) or perfused false lumen (FL) (type B2). Type C: dissection extending into the branch artery with narrowed true lumen compressed by false lumen without detectable blood flow. Type D: no dissection in the branch artery but the orifice obstructed by the intimal flap in the aorta (AO).
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An arterial perfusion route was placed at the ascending aorta, femoral artery, axillary artery, or femoral and axillary arteries in 1, 12, 6, and 2 patients, respectively. The cannulation site was determined by the surgeon (the second author) based on the findings of preoperative CT and intraoperative TEE. Aortic replacement was performed under deep to moderate hypothermia at a rectal temperature between 20 and 25 °C. The blood gas analysis was performed every 60 min during cardiopulmonary bypass and additionally whenever needed with ABL-620 (Radiometer Co., Copenhagen, Norway).
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3. Results
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Among the 24 cases, the CEA and SMA could be visualized with TEE in 24 (100%) and 23 cases (95.8%), respectively (Table 1). No complications related to the manipulation of TEE probe in the stomach were encountered. Four of the 24 patients (16.7%) died within 1 month after surgery: case 2 due to sudden rupture of ascending aorta on the fifth postoperative day despite of an uneventful postoperative course until this event; case 5 on the next day due to uncontrolled bleeding (every cross-clamped portion of aorta was torn); case 16 and 23 on the 15th and 63rd day after surgery due to malperfusion-related multiple organ failure. Case 5 with immediate postoperative death and case 8 with unsuccessful visualization of SMA are excluded from the subsequent analysis. Among the remaining 22 cases, the perfusion pattern of CEA was type A, B, and D in 13, 7, and 2 cases, respectively. The pattern of SMA was type A, B, C, and D in 14, 5, 1, and 2 case(s), respectively. Clinically apparent mesenteric ischemia was present in three cases: 16, 22, and 23. All of these three cases had Stanford type A dissection and perfusion pattern of SMA was either type C or type D. Clinical manifestations related to the intestinal ischemia such as ischemic colitis or paralytic ileus were not encountered in any of the remaining 19 patients, in which SMA/CEA perfusion pattern was type A or type B.
In case 16, preoperative CT showed that the SMA was patent without apparent dissection in the SMA (Fig. 2A and B). Intraoperative TEE demonstrated that dissection extended into the SMA but with detectable blood flow in both true and false lumen. The perfusion pattern was categorized as type B. As the systemic perfusion was started through the femoral and axillary arteries, the true lumen in the aortic arch was found to be collapsed by means of TEE, but no unusual data were noted in other monitoring. The femoral arterial perfusion was terminated immediately. TEE confirmed that the true lumen was restored under axillary arterial perfusion. However, there were no signs of SMA malperfusion in the TEE findings. Marked metabolic acidosis (base excess below –10 mEq/L) developed during the rewarming period but was normalized toward the end of surgery without administration of sodium bicarbonate. There was no change in the perfusion pattern of SMA during this period. Thus, the surgeon did not make a decision of laparotomy. Within a few days after surgery, however, urinary output decreased and abdominal distention appeared with sustained acidosis, and continuous hemodilution filtration was started. At this time, TEE revealed that the true lumen in the SMA was segmentally narrowed at a few centimeters from its orifice (Fig. 2C and D). The perfusion pattern of SMA was diagnosed as pattern C. Although laparotomy was recommended, subsequent surgery was not performed due to multiple organ damages, and the patient died 2 weeks later. The autopsy revealed: (1) stenosis in the proximal portion of SMA caused by dissection and (2) diffuse and scattered necrosis of the intestine.
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Fig. 2. (A and B) Preoperative computed tomogram showing opacified superior mesenteric artery (SMA) in case 16. The true lumen (TL) in the aorta (AO) is not collapsed. (C and D) Postoperative transesophageal echocardiogram in the same case showing type C of perfusion pattern. True lumen is compressed in the SMA. FL: false lumen.
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Case 22 had Stanford type A dissection which occurred at 7 months after coronary artery bypass grafting. He complained of severe pain with paresthesia in the upper extremities associated with metabolic acidosis (BE = –6.3 mEq/L), but had no abdominal pain. The blood flow was obliterated in the bilateral axillary arteries. The preoperative CT showed collapsed true lumen in the aorta with opacified SMA (Fig. 3A and B). Abdominal ultrasonography showed that the blood flow in the SMA was detectable only in the narrowed true lumen at the proximal portion (Fig. 3C), whereas the blood flow in the aorta in the far field was clearly detected. The perfusion pattern was diagnosed as type D (or type C). Abdominal ultrasonography showed that peristaltic movement of intestines was attenuated and metabolic acidosis gradually progressed. Therefore, we performed ilio-SMA bypass with a saphenous vein graft concomitant with fenestration of bilateral axillary arteries. Intraoperative TEE also showed absence of flow in the SMA (Fig. 3D). On laparotomy, the intestine was pale but not necrotic. As soon as the SMA was revascularized through the vein graft, the color and peristaltic movements of the intestine improved.
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Fig. 3. (A and B) Preoperative computed tomogram showing opacified superior mesenteric artery (SMA) in case 22. The true lumen in the aorta (AO) is collapsed. (C and D) Abdominal ultrasonogram and intraoperative transesophageal echocardiogram in the same case showing compressed true lumen with non-perfused false lumen in the SMA. IVC: inferior vena cava.
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Case 23 had acute Stanford type A dissection complicated with broad infarction of right ventricle and underwent repair of ascending aorta and coronary revascularization. CT on admission and intraoperative TEE showed that the true lumen in the abdominal aorta was narrow and the intimal flap in the aorta was close to the orifice of SMA and CEA (type D), but the blood flow was clearly detectable in both arteries (Fig. 4
). Although fenestration of abdominal aorta was also indicated, we decided to perform central repair to salvage the heart. The base excess dropped below –10 mEq/L and lactate level was elevated to 20.8 mmol/L during cardiopulmonary bypass, but these data improved by the end of surgery. There was no apparent changes of TEE findings in the abdominal aorta and visceral branches. However, transaminase elevated to over 4000 IU/L and total bilirubin level was elevated to 13 mg/dL. She had abdominal pain at this time and the intestines remained paralytic. Although the blood exam data gradually improved after 40 days, she had sudden hypotension and the CT revealed massive gas embolism in the portal veins (Fig. 5
) without significant changes in the aorta and visceral arteries in the CT and TEE findings. Multiple organ failure gradually progressed and she died 63 days after surgery.
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Fig. 4. (A–C) Preoperative computed tomogram in case 23 showing intact celiac and superior mesenteric artery (SMA) with collapsed true lumen (TL) in the aorta. (D–F) Intraoperative transesophageal echocardiogram in the same case showing the similar findings as computed tomogram. FL: false lumen, AO: aorta.
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Fig. 5. Computed tomogram showing gas embolism of portal vein in case 23. It suddenly occurred 40 days after surgery. AO: aorta.
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4. Discussion
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The abdominal aorta and visceral arteries are no longer a blind zone for TEE. The TEE probe can be safely manipulated in the stomach in the anesthetized patients. The quality of TEE images is comparable to that of CT images as shown in the figures, although the ultrasound can be attenuated by surrounding structures or by inappropriate manipulations of the TEE probe. Although the intimal flap is not always visualized clearly, use of color Doppler imaging is helpful for recognizing the presence of dissection and malperfusion in the visceral branches.
While CT, MRI, and angiography are accurate and considered to be a standard method for assessing mesenteric ischemia, TEE assessment has several advantages. First, it enables an assessment in the operating room or intensive care unit and provides real-time information. Because the use of contrast media is not needed, the blood flow can be assessed repeatedly or even continuously. Compared with angiography, it is less invasive. Second, TEE assessment does not interrupt the surgical procedures. It saves time for central repair.
However, there are also disadvantages and limitations. First, benefit of TEE depends much on the TEE examiner's skill of visualizing visceral branches and ability to decide when and what to examine. Second, it is hardly possible to visualize the inferior mesenteric and iliac arteries. Although transcolonic echocardiography [10] may solve this problem, it is unlikely to be feasible during surgery. Third, TEE is not capable of detecting segmental ischemia of SMA that can be caused by thromboembolism. It is rather suitable for detecting global malperfusion of SMA. Fourth, TEE can be invasive in awake patients. Discomfort during insertion and manipulation of the TEE probe may cause hemodynamic instability, possibly leading to rupture of the aorta [11].
The SMA was opacified in the CT assessment even in presence of mesenteric ischemia. Intestinal ischemia without occlusion of mesenteric artery has been reported as non-occlusive mesenteric ischemia, which can be associated with aortic dissection [2], cardiac failure [12], or other pathologies [13,14], probably caused by insufficient amount of blood flow in the SMA. The TEE assessment provides information of blood flow velocity by using pulsed-wave Doppler mode, possibly facilitating to make a diagnosis of non-occlusive mesenteric ischemia in type D malperfusion. It is a fact that SMA perfusion can be assessed by means of dynamic CT or MRI as well, and these modalities should be the first choice as long as the situation permits. However, it is also a fact that the CT data provided by the previous hospital are often inadequate for making definite diagnosis. In such an instance, it would be arguable whether the patient should be transferred to the Radiology Division for re-exploration with a risk of circulatory derangement during the process of assessment. Our results show that TEE is a promising tool that can compensate this deficiency.
Results in case 23 has posed another question to us. The true lumen was not completely collapsed as in case 22 and blood flow velocity in the SMA was not markedly reduced. Since she had not complained of abdominal pain on admission, malperfusion of both CEA and SMA could have occurred at some timing during surgery, resulting in liver damage and mesenteric ischemia postoperatively. In case 16, intestinal ischemia might have been caused by false lumen perfusion following femoral arterial perfusion. Regretfully, TEE was mainly used to examine the aortic arch and cervical branches during the period of this event and there may have been some delay in the TEE assessment of mesenteric perfusion. However, it is practically difficult to monitor multiple organs at the same time. Such frustrating situation may be reduced by avoiding femoral arterial perfusion. Or it might be desirable if a continuous monitoring of mesenteric malperfusion were available. Near-infrared spectroscopy that is used for detecting the cerebral malperfusion may be a candidate for this purpose, as we previously experienced a case in which reversible mesenteric ischemia was associated with reduced regional oxygen saturation in the intestinal region [8]. Reduced oxygen saturation was also recognized in case 22. Further investigation is needed.
Limitations in this study should be mentioned. The number of cases complicated with mesenteric ischemia is as small as three, still inadequate for evaluating TEE diagnosis on mesenteric ischemia. Further investigations in a larger series are necessary. Second, only surgical cases were examined in this study, in spite that diagnosis of mesenteric ischemia is often needed in the cases with antihypertensive therapy as well. However, patients in this group are often treated without sedation or intubation and TEE is not the first choice for assessing mesenteric ischemia.
In conclusion, TEE was feasible for examining the SMA perfusion in nearly all patients undergoing surgery for acute aortic dissection. TEE findings that indicate significant SMA malperfusion were (1) narrowed true lumen in the SMA, compressed by expanded false lumen without blood flow; or (2) orifice of SMA obstructed by the intimal flap with compressed true lumen in the proximal aorta. Although there are technical challenges, TEE may be a promising tool for early detection of intestinal ischemia in acute aortic dissection.
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Abstract
1. Introduction
