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AJR 2003; 180:733-736
© American Roentgen Ray Society


Original Report

Pneumatosis Intestinalis in Patients with Ischemia: Correlation of CT Findings with Viability of the Bowel

Lily Y. Kernagis1, Marc S. Levine1 and Jill E. Jacobs1,2

1 Department of Radiology, Hospital of the University of Pennsylvania, 3400 Spruce St., Philadelphia, PA 19104.
2 Present address: Department of Radiology, New York University School of Medicine, 560 First Ave., New York, NY 10016.

Received May 13, 2002; accepted after revision August 22, 2002.

 
Address correspondence to M. S. Levine.


Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. The purpose of our study was to reassess the CT finding of pneumatosis in intestinal ischemia to determine whether it indicates transmural necrosis versus partial mural ischemia and also to determine whether other CT findings can be used to predict which patients with pneumatosis are likely to have viable bowel.

CONCLUSION. The CT finding of pneumatosis does not always indicate transmural infarction of the bowel in intestinal ischemia. Patients with associated portomesenteric venous gas are more likely to have transmural infarction than those with pneumatosis alone.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Pneumatosis intestinalis may be detected on abdominal radiographs or CT not only in patients with ischemic bowel disease but also in patients with a variety of nonischemic causes, including chronic obstructive pulmonary disease, connective tissue disorders, infectious enteritis, celiac disease, leukemia, organ transplants, steroids, chemotherapy, and AIDS [1, 2]. In ischemia, pneumatosis is considered an ominous radiographic finding, particularly if associated with portomesenteric venous gas. In numerous articles and chapters, pneumatosis has been described as an advanced sign of ischemic bowel disease, usually indicating irreversible injury and transmural necrosis [1, 3,4,5,6,7,8].

The widespread use of abdominal CT in ischemic bowel disease has enabled detection of more subtle pneumatosis at earlier stages of the disease [9,10,11]. This raises the possibility that pneumatosis can be detected in patients with partial ischemic damage of the bowel wall before the development of transmural infarction. Thus, some patients with intestinal ischemia could have viable bowel despite findings of pneumatosis on CT. A recent study by Wiesner et al. [12] supports this hypothesis; pneumatosis was observed on CT in patients with intestinal ischemia in the absence of transmural infarction. The purpose of our study was to reassess the CT finding of pneumatosis in ischemic bowel disease to determine whether it indicates transmural necrosis versus partial mural ischemia and also to determine whether other CT findings can be used to predict which patients with pneumatosis are more likely to have viable bowel.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
A computerized search of radiology files from January 1993 to July 2001 at our hospital revealed 34 patients with pneumatosis intestinalis who had undergone abdominal CT. Medical records were reviewed to determine which patients with pneumatosis had clinical signs or symptoms of ischemic bowel disease and risk factors for intestinal ischemia at the time of CT. To minimize selection bias, the authors had no knowledge of the CT findings at the time of chart review. Twelve patients were excluded because medical records were not available. Another seven patients had no clinical signs of intestinal ischemia; six of these patients had nonischemic risk factors for pneumatosis, including chronic steroid use in four, connective tissue disease in one, and celiac disease in one. These seven patients, therefore, were also excluded because they could have had benign conditions rather than intestinal ischemia as the cause of their pneumatosis.

Our study group comprised the remaining 15 patients with clinical findings of ischemic bowel disease who underwent abdominal CT with a HiSpeed Advantage scanner (General Electric Medical Systems, Milwaukee, WI). Nine patients underwent contrast-enhanced CT with 150 mL of 60% iodinated contrast material (diatrizoate meglumine [Hypaque] or iohexol [Omnipaque 300]; Nycomed, Princeton, NJ) administered IV. The remaining six patients underwent unenhanced CT. All except one patient also received 20 mL of an oral contrast agent (diatrizoate meglumine and diatrizoate sodium [Gastroview]; Mallinckrodt, St. Louis, MO) diluted with 800 mL of water 30-45 min before the study. CT was routinely performed with the patient supine during full inspiration. Images were obtained at 5- and 7-mm slice collimations (pitch, 1.3:1; mAs, 200-220) and reconstructed with a soft-tissue algorithm.

All CT scans were analyzed by a consensus review of two abdominal radiologists who had no knowledge of the surgical or pathologic findings or eventual clinical outcome for these patients. The CT scans were reviewed at a computer workstation so that window settings could be adjusted to optimize visualization of pneumatosis. As in the study by Wiesner et al. [12], the pneumatosis was classified as curvilinear (if manifested predominantly by arclike bands of gas) or bubbly (if manifested predominantly by tiny circular collections of gas). The images were also reviewed for other CT findings of ischemia, including a mural stratification pattern (i.e., target sign), dilatation of bowel, mural thickening, mesenteric edema, mural or mesenteric hemorrhage, hemorrhagic ascites, visceral infarcts, pneumoperitoneum, mesenteric arterial or venous thrombi, and portomesenteric venous gas [9, 10].

The imaging findings were then correlated with the clinical and pathologic data to determine how often pneumatosis was associated with irreversible transmural infarction of bowel versus partial mural ischemia without full-thickness necrosis and also to determine whether other CT findings could be used to predict which patients with pneumatosis were more likely to have viable bowel. Patients were classified as having nonviable bowel with transmural infarction if the diseased bowel was resected at surgery and if pathologic examination of the resected specimen confirmed the presence of gangrenous bowel or if the patient died from complications of ischemic bowel disease without undergoing surgery. Conversely, patients were classified as having viable bowel with partial mural ischemia if they did not have necrotic bowel at surgery or if they recovered without surgery. A statistical analysis of the data was not performed because such an analysis would have limited value in our small study population.

Our institutional review board approved all aspects of this retrospective study and did not require the informed consent of patients whose records were included in our study.


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Clinical and Pathologic Findings
Our study group included eight men and seven women who were 22-82 years old (average age, 59 years). Fourteen of the 15 patients presented with abdominal pain, distention, or both. Associated laboratory findings included metabolic acidosis in six patients, leukocytosis in five, elevated liver enzymes in three, elevated lactate level in one, and elevated phosphate level in one. Risk factors for intestinal ischemia included age greater than 50 years in 13 patients, atherosclerosis in three, hypotension in three, digitalis or pressor use in two, a thromboembolic history in two, atrial fibrillation in one, and valvular heart disease in one.

Nine (60%) of the 15 patients with pneumatosis had infarcted bowel: three had resection of the gangrenous bowel at surgery (one patient died 3 days later), and six died from complications of bowel infarction without undergoing surgery within a mean interval of 5.8 days from presentation (range, 1-25 days). The other six patients (40%) had viable bowel without transmural infarction: three had partial mural ischemia at surgery and three recovered without surgery. Thus, seven (47%) of 15 patients with pneumatosis died from complications of bowel infarction.

CT Findings
Nine patients (60%) had transmural infarction. CT revealed pneumatosis that was predominantly curvilinear in seven of these patients (Fig. 1) and bubbly in two (Fig. 2A). The small bowel was affected in four patients (Fig. 2A), and the colon, in five (Fig. 1). All nine patients with transmural ischemia had other CT findings of ischemia, including dilatation of bowel in nine (Fig. 2A), mural thickening in eight (Fig. 1), mural stratification in three, mesenteric edema in five, mural or mesenteric hemorrhage in two, hemorrhagic ascites in two, visceral infarcts in two, pneumoperitoneum in three, and portomesenteric venous gas in four [9, 10] (Fig. 2B). The remaining six patients (40%) had partial mural ischemia without transmural infarction. CT depicted pneumatosis that was predominantly curvilinear in four of these patients (Figs. 3 and 4) and bubbly in two. The small bowel was affected in four patients (Fig. 3); the colon, in one (Fig. 4); and the small bowel and colon, in one. Four of the six patients with partial mural ischemia had other CT findings of ischemia, including dilatation of the bowel in three (Fig. 3), mural thickening in three (Fig. 3), and pneumoperitoneum in three; two patients had isolated pneumatosis without other CT findings of ischemia; and none had portomesenteric venous gas.



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Fig. 1. 51-year-old man with transmural infarction. Unenhanced CT scan shows marked degree of curvilinear pneumatosis (large straight arrow) in rectum with asymmetric mural thickening (small straight arrow) and perirectal gas (curved arrow) anterior to sacrum. Additional images of upper abdomen from same study (not shown) also revealed small amount of pneumoperitoneum anterior to liver. Patient was presumed to have transmural infarction because he died from complications of ischemic bowel disease without undergoing surgery.

 


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Fig. 2A. 81-year-old woman with transmural infarction. Unenhanced CT scan shows dilated small bowel with bubbly pneumatosis (arrows) in several loops of ileum.

 


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Fig. 2B. 81-year-old woman with transmural infarction. Unenhanced CT scan of upper abdomen shows portal venous gas (arrow) in liver. Patient was presumed to have transmural infarction because she died from complications of ischemic bowel disease without undergoing surgery. In this study, all four patients with pneumatosis and portomesenteric venous gas had transmural infarction.

 


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Fig. 3. 42-year-old woman with partial mural ischemia. Enhanced CT scan shows dilated small bowel with curvilinear pneumatosis (black arrow) in ileum and associated mural thickening (white arrow). At surgery, ileum was found to be ischemic without evidence of transmural infarction; therefore, no bowel was resected. Patient made full recovery.

 


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Fig. 4. 59-year-old woman with partial mural ischemia. Unenhanced CT scan shows curvilinear pneumatosis (arrow) in pelvic cecum without other CT findings of ischemia. In this study, both patients with intestinal ischemia and isolated pneumatosis had viable bowel and recovered without surgery.

 

Of the 15 patients with pneumatosis on CT, both patients (100%) with isolated pneumatosis and no other CT findings of ischemia had viable bowel and recovered without surgery. Five (56%) of nine with pneumatosis and other CT findings of ischemia but no portomesenteric venous gas, and all four (100%) with pneumatosis and other CT findings of ischemia, including portomesenteric venous gas, had gangrenous bowel. When the CT findings were correlated with clinical outcome, both patients (100%) with isolated pneumatosis survived. Three (33%) of nine patients with pneumatosis and other CT findings of ischemia but no portomesenteric venous gas, and all four (100%) with pneumatosis and other CT findings of ischemia including portomesenteric venous gas, died.


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
In recent years, CT has been used to evaluate more and more patients with clinical signs and symptoms of ischemic bowel disease. Depending on the severity and extent of disease, intestinal ischemia may be manifested on CT by a spectrum of findings, including dilatation of bowel, mural thickening, a mural stratification pattern, mesenteric edema, mural or mesenteric hemorrhage, ascites, pneumoperitoneum, mesenteric arterial or venous thrombi, and portomesenteric venous gas [9, 10]. In the clinical setting of intestinal ischemia, pneumatosis and portomesenteric venous gas have been considered to be signs of advanced disease, usually indicating irreversible injury and transmural necrosis [1, 3,4,5,6,7,8]. However, the use of CT improves our ability to detect even subtle cases of pneumatosis [9,10,11], so this finding can, in theory, be observed in patients with intestinal ischemia before the development of transmural necrosis. This hypothesis was supported by a recent study by Wiesner et al. [12], in which it was found that seven (30%) of 23 patients with ischemic bowel disease and pneumatosis on CT had partial mural ischemia rather than transmural infarction on the basis of the pathologic findings at surgery or at clinical follow-up in patients who did not undergo surgery.

In our study, six (40%) of 15 patients with pneumatosis on CT and clinical findings of intestinal ischemia had viable bowel at surgery or recovered without surgery (Figs. 3 and 4), indicating partial mural ischemia without transmural necrosis. Our findings independently corroborate the findings of Wiesner et al. [12] that pneumatosis on CT does not always indicate transmural necrosis of the bowel in patients with intestinal ischemia. Both of these studies refute the long-held concept that pneumatosis is a specific sign of bowel infarction in ischemic bowel disease. Presumably, gas can enter the ischemic bowel wall via a disrupted mucosa in the absence of transmural infarction. This observation explains our ability to detect pneumatosis on CT in patients with viable bowel in whom surgical resection is not required.

Further analysis of our cases revealed that both patients (100%) with isolated pneumatosis had viable bowel (Fig. 4). Five (56%) of nine with pneumatosis and other CT findings of ischemia but no portomesenteric venous gas (Fig. 1), and all four (100%) with pneumatosis and other CT findings of ischemia including portomesenteric venous gas (Fig. 2A,2B), had transmural infarction. Our data suggest that patients with isolated pneumatosis are more likely to have partial mural ischemia, whereas patients with pneumatosis and portomesenteric venous gas are more likely to have transmural infarction. Similarly, Wiesner et al. [12] found that patients with findings of pneumatosis and portomesenteric venous gas on CT were more likely to have transmural infarction than those with pneumatosis alone. Thus, preliminary data from both studies indicate that the presence of portomesenteric venous gas can be used to predict which patients with pneumatosis are more likely to have transmural infarction necessitating emergency surgical intervention.

Our study has limitations. Because ours was a retrospective investigation, the need for strict inclusion criteria limited the total number of cases in our study population, precluding a meaningful statistical analysis of the data. Small sample sizes could also have magnified the effect of selection bias on our study population. In addition, we cannot exclude the possibility that one or more patients with clinically suspected intestinal ischemia may have had coincidental pneumatosis from a nonischemic cause. We also cannot totally exclude the possibility that the two patients with isolated pneumatosis had false-positive findings on CT resulting from an unusual configuration of trapped intraluminal gas, nor can we exclude the possibility that one or more of the three patients who recovered without surgery might have had a tiny segment of transmural infarction. Conversely, some patients excluded from the analysis because of a benign clinical presentation may actually have had ischemic bowel disease, so we could have underestimated the frequency of pneumatosis in patients with intestinal ischemia who had viable bowel. Finally, some patients in our study underwent unenhanced CT, limiting our ability to detect other CT findings of ischemia, such as a mural stratification pattern.

In conclusion, our data suggest that the CT finding of pneumatosis does not always indicate transmural infarction of the bowel in intestinal ischemia. Patients with associated portomesenteric venous gas are more likely to have transmural infarction than those with pneumatosis alone. Thus, some patients with intestinal ischemia may have partial mural ischemia with viable bowel despite the presence of pneumatosis on CT.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Kelvin FM, Korobkin M, Rauch RF, Rice RP, Silverman PM. Computed tomography of pneumatosis intestinalis. J Comput Assist Tomogr 1984;8:276 -280[Medline]
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  7. Brandt LJ, Boley SJ. AGA technical review on intestinal ischemia. Gastroenterology 2000;118:954 -968[Medline]
  8. Nolan DJ, Herlinger H. Vascular disorders of the small bowel. In: Gore RM, Levine MS, eds. Textbook of gastrointestinal radiology, 2nd ed. Philadelphia: Saunders, 2000: 402-409
  9. Clark RA. Computed tomography of bowel infarction. J Comput Assist Tomogr 1987;11:757 -762[Medline]
  10. Perez C, Llauger J, Puig J, Palmer J. Computed tomographic findings in bowel ischemia. Gastrointest Radiol 1989;14:241 -245[Medline]
  11. Smerud MJ, Johnson CD, Stephens DH. Diagnosis of bowel infarction: a comparison of plain films and CT scans in 23 cases. AJR 1990;154:99 -103[Abstract/Free Full Text]
  12. Wiesner W, Mortele KJ, Glickman JN, Ji H, Ros PR. Pneumatosis intestinalis and portomesenteric venous gas in intestinal ischemia: correlation of CT findings with severity of ischemia and clinical outcome. AJR 2001;177:1319 -1323[Abstract/Free Full Text]

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