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Presence or Absence of Gas in the Appendix: Additional Criteria to Rule Out or Confirm Acute Appendicitis-Evaluation with US¹

¹ From the Departments of Radiology and Nuclear Medicine (T.R., A.H., P.M., N.G.) and Surgery (R.F.), Hospital Barmherzige Brueder, Kajetanerplatz 1, A-5010 Salzburg, Austria; the Department of Nuclear Medicine, State Hospital of Salzburg, Austria (L.R.); and the Institute of Medical Statistics, University of Vienna, Wien, Austria (B.S.). From the 1998 RSNA scientific assembly. Received September 18, 1998; revision requested November 4; final revision received May 17, 1999; accepted August 4. Address reprint requests to T.R.

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To investigate whether the presence or absence of gas in the appendix may be considered as additional ultrasonographic (US) criteria to rule out or confirm acute appendicitis.

MATERIALS AND METHODS: The appendices in 239 control subjects, 138 patients with lower right quadrant pain without acute appendicitis, and 80 patients with acute appendicitis were prospectively evaluated for intraluminal gas with US.

RESULTS: The appendices in 206 (86%) control subjects showed gas at US, and those in 33 (14%) did not. The appendices in 109 (79%) symptomatic patients without acute appendicitis showed gas, and those in 29 (21%) did not. The appendices in 12 (15%) patients with acutely inflamed appendices showed gas, and those in 68 (85%) did not. The absence of gas as a criterion for acute appendicitis had a sensitivity of 85%; specificity, 79%; positive and negative predictive values, 57% and 94%, respectively; and accuracy, 81%. Gas was useful to exclude acute appendicitis in 64 (46%) symptomatic patients because the established criteria were misleading. In 19 (24%) patients, the absence of gas was useful for diagnosis of acute appendicitis because the other criteria were not convincing.

CONCLUSION: US-based detection of gas in the appendiceal lumen helps to rule out acute appendicitis, whereas the absence of gas further confirms its presence, especially in cases where established US criteria are either insufficiently present or misleading.

Index terms: Appendicitis, 751.291 • Appendix, US, 751.12981

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Ultrasonography (US) is an established imaging method to confirm or rule out acute appendicitis in patients with lower right quadrant pain (1). In 1986, an important study (2), in which the only criterion for acute appendicitis was the detectability of the appendix at US, was published. In that study, the normal appendix could not be detected in any of the 50 control subjects. Soon after, other investigators (3–6) sometimes could detect the normal appendix; therefore, in addition to detectability of the appendix at US, other criteria for acute appendicitis, such as outer diameter of the appendix, compressibility of the appendix, and echogenic inflammatory periappendiceal fat change, had to be established.

Advanced US equipment and accumulated experience enable the US depiction of normal appendices more often. The rates of detecting noninflamed appendices in more recent US studies (7–9) range from 60% to 82%. Therefore, the US-based detectability of the appendix cannot be further used as a criterion. Federle (10) emphasized that the key to diagnosing appendicitis today is the recognition of the appendix as normal or abnormal. Although the established criteria for recognition of appendicitis are important, they have limited sensitivity or specificity. The outer diameter of the appendix (6 mm in acute appendicitis) has high sensitivity—about 100%—but relatively low specificity—about 64% (9). In addition, we have found the compressibility of the appendix to have poor specificity. The echogenic inflammatory periappendiceal fat change has poor sensitivity—about 50%—but high specificity—about 95% (11). In addition, color Doppler US has diagnostic weaknesses when the appendix is located deep within the abdomen or has gangrene (8).

Additional criteria to improve the accuracy of differentiating normal from abnormal appendices would be welcome. In the radiology department at the Hospital Barmherzige Brueder, we successfully use additional criteria, such as the presence or absence of gas in the appendix and the shape of the transverse section of the appendix, in our diagnosis of acute appendicitis. Gas in the appendix is controversially discussed in the literature (12–15). We initiated this prospective study to gain statistically significant data concerning the presence of gas in normal and acutely inflamed appendices and to determine the usefulness of this finding as a US criterion for appendicitis.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
To detect vermiform appendices ultrasonographically, the graded compression technique introduced and described by Puylaert (2) was used. For this study, 457 US-depicted appendices were prospectively evaluated as positive or negative for the presence of intraluminal appendiceal gas. We used 2–4-MHz curved-array and 5–10-MHz linear-array transducers (HDI 3000; Advanced Technology Laboratories, Bothell, Wash) as well as 3.5-MHz curved-array and 7.5–10.0-MHz linear-array transducers (AU4; Esaote, Florence, Italy).

The US appearance of gas is characterized by a sharp, complete reflection that is caused by a very high acoustic impedance at the entrance to the gas bubble, with either reverberation artifacts or acoustic shadowing behind it (Fig 1) (16). In addition, the gas surface often is linear (Fig 1). The appearance of calculi (ie, appendicoliths) can be similar to this, but these have a more convex formed surface (Fig 2), and the entrance echo is usually not as intense as the entrance echo of gas. The appendix may also contain a small amount of feces, which usually appears echogenic but does not have such intense entrance echos and acoustic shadowing as gas or calculi.

View larger version (159K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. (a) Longitudinal and (b) transverse US images show a normal appendix (black arrows) with intraluminal gas (short white arrows). The gas has a linear surface and a very intense entrance echo (short white arrows) with reverberation artifacts (long white arrows) behind it.

View larger version (161K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. (a) Longitudinal and (b) transverse US images show a normal appendix (black arrows) with intraluminal gas (short white arrows). The gas has a linear surface and a very intense entrance echo (short white arrows) with reverberation artifacts (long white arrows) behind it.

View larger version (181K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Longitudinal US image shows an acutely inflamed appendix (short black and white arrows). An intraluminal appendicolith (curved arrow) with a curved surface and acoustic shadowing (long arrows) behind it is seen.

Control Group
For approximately 15 weeks, we tried to visualize the appendix with US in 380 consecutive adult individuals. In 239 (63%) (112 men, 127 women; mean age, 55 years; age range, 25–82 years) of them, the appendix could be seen clearly; this was the control group. The 380 patients were part of our abdominal US screening program, which has been offered to almost all of our inpatients as a common practice since 1988, even in those patients without clinical abdominal symptoms. Informed consent was obtained from each patient, and the study was approved by the ethical committee at the Hospital Barmherzige Brueder. The only selection criterion for this group was that the patient could not exhibit any sign of abdominal disease or have undergone appendectomy previously. Patients had an overnight period of fasting, as they would in preparation for the general screening investigation, but they were not specially prepared. At the end of the screening investigation, we attempted to detect the appendix ultrasonographically within an examination time of 5–15 minutes. The depicted appendices were prospectively interpreted by one of four experienced gastrointestinal radiologists (T.R., A.H., P.M., N.G.) as positive or negative for the presence of intraluminal appendiceal gas.

Patients Clinically Suspected of Having Acute Appendicitis
For approximately 2 years, 263 consecutive patients (age range, 7–97 years; mean age, 34 years) who were clinically suspected of having acute appendicitis were referred for US in our department. We were able to detect the appendix with US in 218 (113 male patients, 105 female patients; mean age, 32 years; age range, 7–97 years) of them; these individuals made up our sample population of patients with lower right quadrant pain who had appendices that were acutely inflamed and who had appendices that were not. The US criteria we used to differentiate an acutely inflamed appendix from a normal one are as follows: proof that the point of maximal tenderness was indeed located at the appendix, outer diameter of the appendix greater than or equal to 6 mm, noncompressibility of the appendix, rounded transverse section of the appendix, increased blood flow in the appendiceal wall detected by using color Doppler US, and echogenic periappendiceal inflammatory fat change. All of these depicted appendices also were prospectively interpreted by one of four experienced gastrointestinal radiologists (T.R., A.H., P.M., N.G.) as positive or negative for the presence of intraluminal appendiceal gas.

For statistical analysis, we calculated the estimated probabilities for the absence of intraluminal gas at US in predicting an acutely inflamed appendix. These probabilities included sensitivity, specificity, positive and negative predictive values, and accuracy.

	RESULTS

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One hundred seventy-seven (67%) of the 263 patients clinically suspected of having acute appendicitis were found not to have acute appendicitis. The definite diagnosis was established either surgically and histologically in 56 patients or at clinical follow-up in 121 patients. In 138 (78%) of these 177 patients, we were able to detect the appendix ultrasonographically. These 138 patients were the subgroup of patients who were clinically suspected of having acute appendicitis but did not have acutely inflamed appendices.

Eighty-six (33%) of the 263 patients with clinically suspected acute appendicitis had acute appendicitis. All 86 patients were treated surgically after US investigation, and the definite diagnosis was confirmed histologically. US depicted the appendix in 80 of the 86 patients. These 80 patients were the subgroup of patients clinically suspected of having acute appendicitis who had acutely inflamed appendices. In four patients, US could not depict the appendix, but its findings suggested a perforating appendicitis because an inflammation process with abscess formation was seen near the cecum. Two patients had acute appendicitis without US depiction of the appendix or a periappendiceal inflammatory process.

In 206 (86%) of the 239 appendices depicted in the control group, there was intraluminal gas visible during the US examination. There was no gas detectable in 33 (14%) of the 239 appendices (Fig 3). In the 138 appendices depicted in the group with symptoms but without acute appendicitis, intraluminal gas was visible in 109 (79%) and not visible in 29 (21%) (Fig 3). In the 80 acutely inflamed appendices, intraluminal gas could be detected in 12 (15%) (Figs 3, 4), and it could not be detected in 68 (85%) (Figs 3, 5). The percentage of gas-containing inflamed appendices was lower in the patients with severe (ie, phlegmonous or gangrenous) appendicitis (in eight [12%] of 64 patients) than that in those with mild or moderate (ie, catarrhal, erosive, or ulcerous) appendicitis (five [31%] of 16 patients).

View larger version (75K): [in this window] [in a new window] [Download PPT slide]   Figure 3. Graph illustrates the presence (striped area) or absence (white area) of intraluminal appendiceal gas detected by using US in 457 patients. Column a represents the 239 asymptomatic control subjects, 206 (86%) of whom had appendiceal gas and 33 (14%) of whom did not. Column b represents the 138 symptomatic patients without evidence of acute appendicitis, 109 (79%) of whom had appendiceal gas and 29 (21%) of whom did not. Column c represents the 80 symptomatic patients with acute appendicitis, 12 (15%) of whom had intraluminal gas and 68 (85%) of whom did not.

View larger version (176K): [in this window] [in a new window] [Download PPT slide]   Figure 4. Longitudinal US image shows an acutely inflamed appendix (black arrows). Intraluminal gas (short white arrow) with reverberation artifacts (long white arrows) behind it is seen.

View larger version (175K): [in this window] [in a new window] [Download PPT slide]   Figure 5a. (a) Longitudinal and (b) transverse abdominal US images show an acutely inflamed appendix (arrows) without intraluminal gas.

View larger version (177K): [in this window] [in a new window] [Download PPT slide]   Figure 5b. (a) Longitudinal and (b) transverse abdominal US images show an acutely inflamed appendix (arrows) without intraluminal gas.

In the 138 symptomatic patients, gas in the appendix was useful to rule out acute appendicitis because the outer diameter of the appendix was greater than or equal to 6 mm in 30 (22%), the appendix was not compressible in 34 (25%), or because both conditions were present and misleading in 20 (14%) patients.

In 19 (24%) of the 80 patients with acute appendicitis, the absence of gas in the appendix was useful to confirm the diagnosis because other established criteria were not present in a convincing manner.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
To our knowledge, this is the first study in which percentages of the occurrence of gas in both situations—that is, in the normal appendix and in the acutely inflamed appendix—were obtained by using US in a substantial patient population.

Why should the normal appendix contain gas—and the acutely inflamed appendix not contain gas—in a high percentage of cases? The lumen of the normal appendix is connected to the usually gas-filled cecum and contains small amounts of gas in a high percentage of cases, probably as a consequence of regurgitation from the cecum (12,14,17). Obstruction of the appendiceal lumen is the most important cause of acute appendicitis (16,18,19).

The results of our study showed that gas disappears after obstruction in most cases. Resorption of intraluminal gas after obstruction could be a possible explanation for this disappearance. With regard to this subject, it is of interest that in the appendices with mild or moderate (ie, catarrhal, erosive, or ulcerous at histology) acute inflammation, we found a remarkably higher percentage of intraluminal gas (31%) than that in the appendices with severe (ie, phlegmonous or gangrenous at histology) acute inflammation (12%). Provided that the appendices with mild or moderate acute inflammation at histologic analysis are those with beginning inflammation, it could be assumed that the disappearance of intraluminal gas after obstruction will take time, possibly depending on the amount of intraluminal gas. If patients are examined before this time has passed, a residual amount of intraluminal appendiceal gas will be detected despite acute appendicitis.

Another explanation for intraluminal gas in acutely inflamed appendices might be the presence of gas-producing microorganisms (13,20). A third explanation for some cases of acutely inflamed appendices with intraluminal gas might be that acute inflammation sometimes develops without appendiceal obstruction (17,19) or that the appendiceal obstruction that is responsible for the appendicitis may sometimes resolve spontaneously, in which case, gas could regurgitate from the cecum again (21,22).

Intraluminal gas in the appendix can also occur in the proximal normal portion of the appendix, if the inflammatory process is confined to the distal portion (18,23). This was the case in five (6%) of 80 patients with acute appendicitis in our study.

Our study consisted of both a healthy control group and patients with right lower quadrant pain without evidence of acute appendicitis at either surgery and histologic analysis or clinical follow-up. The results showed that the percentage of cases with appendiceal gas in the control group (86%) was somewhat higher than the percentage of cases with gas in the symptomatic patients without evidence of acute appendicitis (79%). One explanation could be that the group of symptomatic patients without evidence of acute appendicitis at clinical follow-up may have consisted of some patients who had spontaneously resolving acute appendicitis (21,22). Another explanation could be that inflammatory processes near the appendix may affect the appendix and influence its filling with gas. For instance, we observed some cases of acute ileocolitis and ulcerative colitis in which the appendix did not have gas in the acute phase of disease, but it refilled with gas after improvement. For statistical analysis, we analyzed the findings in the symptomatic patient groups (Fig 3, groups b and c), because a comparison with healthy individuals is less relevant.

Before cross-sectional imaging techniques were established, gas detected in the appendix on conventional radiographs was used as a criterion for acute appendicitis (12,14,15). This sign, however, was relatively rare and nonspecific (12,13,16). The results of several reports (12–15,24) indicate that the normal appendix may contain gas that is demonstrable on conventional abdominal radiographs. The amount of gas must be relatively large compared with that detected at US or computed tomography (CT) if it is to be demonstrated at conventional radiography (12,16,18,23). This explains why conventional abdominal radiographs cannot depict gas in a high percentage of normal appendices.

By using US, Poljak et al (16) and Jeffrey et al (20) studied some cases of acutely inflamed appendices that contained air, and a percentage of occurrence of 3% was observed in the retrospective study of Poljak et al. In our prospective study, we observed gas in 12% of the cases of severe appendicitis and in 31% of the cases of mild or moderate appendicitis.

In some CT and US studies (7,25–27) it has been reported that the normal appendix may contain gas, but in these studies, gas was not used as a diagnostic criterion and the percentages of occurrence were not given.

Only Rao et al (18,23), in CT studies, used air in the normal appendix as a diagnostic criterion, in addition to various other criteria, to rule out acute appendicitis. Rao et al detected this finding in 18 (44%) of 41 patients with a normal appendix and did not report cases of air in acutely inflamed appendices (23). An explanation for the lower (44%) percentage of cases with gas in the normal appendix in the study by Rao et al compared with the percentage in our study (79%) could be that 5–10-MHz US is able to depict a small gas bubble surface by using acoustic impedance, whereas in CT, the partial volume effect may impede the detection of punctiform gas bubbles.

Because the US appearance of calculi can resemble that of gas, the differentiation cannot be guaranteed in all situations. In most cases, however, US differentiation is easily possible.

Our study results showed that if a patient with lower right quadrant pain does not have intraluminal gas in the appendix at US, there is a 57% probability (ie, positive predictive value) that he or she has acute appendicitis. If the patient has appendiceal gas at US, then there is a 94% probability (ie, negative predictive value) that he or she has an appendix without acute inflammation. We can therefore conclude that the presence of gas is a more reliable sign to exclude acute appendicitis than is the absence of gas to confirm acute appendicitis.

None of the established US criteria has both high sensitivity and high specificity. Therefore, the US-based diagnosis of appendicitis is based on several features such as point of maximal tenderness, outer diameter of the appendix, compressibility of the appendix, echogenic inflammatory periappendiceal fat change, and blood flow in the appendiceal wall. Nevertheless, the established criteria often are either misleading or not present in a convincing manner. The presence of gas was the most prominent diagnostic sign to exclude acute appendicitis in 64 (46%) of the 138 symptomatic patients without acute appendicitis in our study, and the absence of gas was the most prominent diagnostic finding in 19 (24%) of 80 patients with acute appendicitis. In these cases, the presence or absence of gas in the appendix helped to increase diagnostic accuracy. In summary, the presence of intraluminal gas in the appendix is a useful additional US finding to exclude acute appendicitis, whereas the absence of gas helps to confirm acute appendicitis.

	Footnotes

 
Author contributions: Guarantors of integrity of entire study, T.R., A.H., L.R., N.G.; study concepts and design, T.R., A.H., L.R.; definition of intellectual content, T.R., A.H., L.R., N.G.; literature research, T.R., L.R.; clinical studies, T.R., A.H., P.M., R.F., N.G.; experimental studies, T.R., A.H.; data acquisition, T.R., A.H., P.M., R.F.; data analysis, T.R., A.H., L.R., B.S.; statistical analysis, T.R., B.S.; manuscript preparation and editing, T.R.; manuscript review, A.H., L.R., R.F., B.S., N.G.

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