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Sonography of Acute Right Lower Quadrant Pain: Importance of Increased Intraabdominal Fat Echo

¹ Department of Radiology, Konkuk University Hospital and Konkuk University School of Medicine, Hwayang-dong, Gwangjin-gu, Seoul, 143-729, Korea.

Received October 20, 2007; accepted after revision July 22, 2008.

 
Address correspondence to Y. J. Kim (yjkim{at}kuh.ac.kr).

This paper was supported by Konkuk University in 2005.

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. The purpose of our study was to assess the diagnostic usefulness of increased intraabdominal fat echo during the sonographic evaluation of patients with acute right lower quadrant (RLQ) pain.

SUBJECTS AND METHODS. A total of 328 consecutive patients (132 male and 196 female; mean age, 28 ± 15 [SD] years) with acute RLQ pain prospectively underwent transabdominal sonography by one of three experienced radiologists. The radiologists prospectively graded intraabdominal fat echo using a 3-point scale: 1, normal; 2, slight increase; and 3, marked and diffuse increase. Final diagnoses were made using surgical or pathologic findings or by clinical follow-up. Of the 328 patients, 11 were lost to follow-up and excluded from analysis. Sensitivity, specificity, accuracy, positive predictive value (PPV), and negative predictive value (NPV) of increased intraabdominal fat echo were calculated for a positive final diagnosis.

RESULTS. Final diagnoses were negative (n = 103), acute appendicitis (n = 137), right colonic diverticulitis (n = 18), mesenteric lymphadenitis (n = 13), enteritis (n = 26), and others (n = 20). Grades of intraabdominal fat echo were grade 1 (n = 158), grade 2 (n = 35), and grade 3 (n = 124). Overall, fat echo grades 2 or 3 were more frequently observed in patients with a positive final diagnosis (73% [157/214] vs 2% [2/103], p < 0.001) than in those with a negative final diagnosis. Sensitivity, specificity, accuracy, PPV, and NPV of increased intraabdominal fat echo for a positive final diagnosis were 73%, 98%, 81%, 99%, and 64%. Increased intraabdominal fat echo was documented in 89% (122/137) of cases of acute appendicitis and in 100% (18/18) of cases of right colonic diverticulitis.

CONCLUSION. An increased intraabdominal fat echo on sonography is highly specific for the presence of RLQ inflammatory disease.

Keywords: abdominal pain • appendicitis • diverticulitis • intraabdominal fat • sonography

Introduction

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Sonography has been widely used to evaluate patients with acute right lower quadrant (RLQ) pain. In addition to direct sonographic visualization of various causes, increased intraabdominal fat echo is an important ancillary diagnostic feature. This finding has reportedly been frequently associated with a variety of abdominal inflammatory diseases, such as acute appendicitis [1-3], right colonic diverticulitis [2, 4], epiploic appendagitis [2], omental infarction [2, 5], and Crohn's disease [2, 6, 7].

Although increased intraabdominal fat echo is commonly encountered during sonography of patients with acute RLQ pain, to our knowledge, its diagnostic usefulness has not been verified in a scientific manner. For example, the clinical significance of increased intraabdominal fat echo alone without direct visualization of any specific cause remains unknown. Therefore, the purpose of this study was to prospectively evaluate the diagnostic usefulness of the finding of an increased intraabdominal fat echo during the sonographic evaluation of patients with acute RLQ pain.

Subjects and Methods

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Patients
This prospective study was approved by our institutional review board and written informed consent was obtained from all patients. From July 2006 through March 2007, a total of 328 consecutive patients (132 male and 196 female; mean age, 28 ± 15 [SD] years were referred to our department for the sonographic evaluation of acute RLQ pain. Of these, 11 were excluded because of loss to follow-up that prevented a final definitive diagnosis. Therefore, 317 patients constituted the final study population.

Sonographic Examinations
All sonographic examinations were performed using an HDI 5000 system (Philips Healthcare) or an IU-22 system (Philips Healthcare) by one of three radiologists with 8, 13, and 21 years of abdominal sonographic experience. Radiologists initially evaluated the RLQ of the abdomen using a curved 5- to 8-MHz transducer. The appendix, cecum, ascending colon, and terminal ileum were carefully examined. For appendix evaluations, the graded compression technique described by Puylaert was used [8]. The diagnostic criteria for acute appendicitis were an enlarged appendix (> 6 mm outer diameter) and lack of compressibility [9, 10]. Diagnostic criteria for right colonic diverticulitis were visualization of diverticula as outpouching structures from the colon, thickening of the colonic wall, and local tenderness induced by graded compression [11]. Enteritis was diagnosed when diffuse mural thickening of the small bowel or colon was present with or without mesenteric lymphadenopathy [11]. A diagnosis of mesenteric lymphadenitis was made when clustered lymphadenopathies (each measuring 5 mm) in the RLQ were found in the absence of an identifiable underlying inflammatory process [2, 12].

View larger version (88K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1 —34-year-old man with negative diagnosis: grade 1 intraabdominal fat echo. Transverse sonogram of right lower quadrant shows compressible ovoid structure (arrow and calipers) surrounded by normal noninflamed fat, suggestive of normal appendix.

View larger version (90K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2 —14-year-old boy with acute appendicitis and grade 2 intraabdominal fat echo. Transverse sonogram of right lower quadrant shows enlarged round appendix (arrow) surrounded by slightly increased intraabdominal fat echo (arrowheads), indicating inflamed fat.

View larger version (115K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3 —44-year-old man with acute appendicitis and grade 3 intraabdominal fat echo. Longitudinal sonogram of right lower quadrant shows enlarged appendix (arrowheads) surrounded by definitely increased intraabdominal fat echo.

Negative sonography referred to the lack of an identifiable cause and the presence of a normal intraabdominal fat echo. In cases with increased intraabdominal fat echo (defined as intraabdominal fat echo grade 2 or 3) without a visualized specific cause, contrast-enhanced abdominal CT was performed. Subsequently, the whole abdomen was examined using a curved 2- to 5-MHz transducer. Immediately after imaging, specific sonographic diagnoses were prospectively recorded on a data sheet.

Assessment of Outcomes
Final diagnoses, which were used as the reference standards, were established by surgery or pathologic examinations for 142 (45%) patients and by clinical follow-up for the other 175 (55%) patients.

Statistical Analysis
Cases with normal or increased intraabdominal fat echo were compared with final diagnoses. Sensitivity, specificity, accuracy, positive predictive value (PPV), and negative predictive value (NPV) of increased intraabdominal fat echo for a positive final diagnosis were calculated. Association of final diagnoses with normal and increased intraabdominal fat echo grades was evaluated using the chisquare test. Cases with increased intraabdominal fat echo as an isolated sonographic finding were also compared with final diagnoses. Statistical analyses were performed using SPSS 11.0 software (SPSS), and statistical significance was accepted at the p < 0.05 level. For statistical analyses involving three pairwise comparisons of the three radiologists' performances, a p value of less than 0.017 for each pairwise comparison (i.e., Bonferroni adjustment) was used to account for an increase in error in determining statistical significance.

Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Sonographic results and final diagnoses are summarized in Table 1. Diagnoses were negative (n = 103, 32%), acute appendicitis (n = 137, 43%), right colonic diverticulitis (n = 18, 6%), mesenteric lymphadenitis (n = 13, 4%), enteritis (n = 26, 8%), and others (n = 20, 6%). The sensitivity, specificity, accuracy, PPV, and NPV of sonographic examinations were 95% (130/137), 99% (178/180), 97% (308/317), 98% (130/132), and 96% (178/185) for acute appendicitis and 89% (16/18), 100% (298/299), 99% (314/317), 94% (16/17), and 99% (298/300) for right colonic diverticulitis, respectively.

Final diagnoses according to RLQ fat echogenicity are summarized in Table 2. Intraabdominal fat echo was graded grade 1 in 158 patients (50%), grade 2 in 35 patients (11%), and grade 3 in 124 patients (39%). For the 35 patients with grade 2 intraabdominal fat echo, 33 (94%) were found to have a positive final diagnosis; for the 124 patients with grade 3 intraabdominal fat echo, all (100%) had a positive final diagnosis (Table 3). Most (150 patients, 94%) of the patients (n = 159) with increased intraabdominal fat echo (grade 2 or 3) were accounted for in one of three disease groups: acute appendicitis (n = 122, 77%), right colonic diverticulitis (n = 18, 11%), and enteritis (n = 10, 6%).

Among the 317 patients included in this study, increased intraabdominal fat echo was more frequently observed in those with a positive final diagnosis (73% [157/214] vs 2% [2/103], p < 0.001) (Table 3). Sensitivity, specificity, accuracy, PPV, and NPV of an increased intraabdominal fat echo for a positive final diagnosis were 73%, 98%, 81%, 99%, and 64%. No significant differences in these diagnostic performance measures were seen among the three radiologists involved in this study (range of p values, 0.59-0.99) (Table 4).

When considering only inflammatory diseases (acute appendicitis, right colonic diverticulitis, mesenteric lymphadenitis, enteritis, pelvic inflammatory disease, pericecal abscess, appendiceal cancer with perforation, and acute pyelonephritis), the sensitivity, specificity, accuracy, PPV, and NPV of an increased intraabdominal fat echo were 76% (155/205), 98% (101/103), 83% (256/308), 99% (155/157), and 67% (101/151), respectively. Increased intraabdominal fat echo was documented in 89% (122/137) of patients with acute appendicitis, in 100% (18/18) with right colonic diverticulitis, and in 38% (10/26) with enteritis. Of 15 subjects with acute appendicitis and a normal intraabdominal fat echo, four were found to have deep appendicitis (retrocecal appendicitis, n = 2; tip appendicitis, n = 2). In distinction to the other inflammatory diseases, none of cases of mesenteric lymphadenitis revealed increased intraabdominal fat echo.

Seven patients had only an increased intraabdominal fat echo in the RLQ without a visualized cause. Of these, six (86%) cases eventually received a positive final diagnosis—specifically, acute appendicitis (n = 1, grade 3) (Figs. 4A, and 4B), pelvic inflammatory disease (n = 2, grade 2; n = 1, grade 3) (Figs. 5A, and 5B), and right colonic diverticulitis (n = 2, grade 3) (Figs. 6A, and 6B).

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A —17-year-old boy who presented with fever and right lower quadrant (RLQ) pain with increased intraabdominal fat echo in RLQ without a visible cause at sonographic examination. Transverse sonogram of RLQ shows increased intraabdominal fat echo, grade 3 (arrowheads).

View larger version (113K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B —17-year-old boy who presented with fever and right lower quadrant (RLQ) pain with increased intraabdominal fat echo in RLQ without a visible cause at sonographic examination. Contrast-enhanced CT scan shows enlarged appendix and appendiceal wall thickening (arrow) surrounded by fat stranding (arrowheads), suggestive of acute appendicitis. Note deep position of inflamed appendix.

View larger version (114K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A —27-year-old woman with right lower quadrant (RLQ) pain and increased intraabdominal fat echo in RLQ without a visible cause on sonography. Transverse sonogram of RLQ shows increased intraabdominal fat echo, grade 3 (arrowheads).

View larger version (137K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B —27-year-old woman with right lower quadrant (RLQ) pain and increased intraabdominal fat echo in RLQ without a visible cause on sonography. Contrast-enhanced CT scan shows diffuse intraabdominal stranding of fat in tissue (white arrowheads) of RLQ. Note thickened salpinx (black arrowheads), suggestive of presence of pelvic inflammatory disease. Laparoscopy revealed tubal congestion of right salpinx, indicating pelvic inflammatory disease.

View larger version (114K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6A —36-year-old man with fever, right lower quadrant (RLQ) pain, and increased intraabdominal fat echo in RLQ without a visible cause on sonography. Transverse sonogram of RLQ shows diffuse increased intraabdominal fat echo, grade 3 (arrowheads).

View larger version (137K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6B —36-year-old man with fever, right lower quadrant (RLQ) pain, and increased intraabdominal fat echo in RLQ without a visible cause on sonography. Contrast-enhanced CT scan shows inflamed right colonic diverticulum (arrow) and surrounding extensive stranding of fat in tissue (arrowheads) along colonic wall and mesocolon.

Top Abstract Introduction Subjects and Methods Results Discussion References

In our study, we analyzed the diagnostic usefulness of increased intraabdominal fat echo in patients with acute RLQ pain and found that it is more frequently observed in patients with RLQ inflammatory diseases. Our results were consistent with the results of previous studies [2, 4, 9]. Kessler et al. [9] reported that inflammatory fat changes were present in 91% (52/57) of the patients with appendicitis, which is nearly identical to our result of 89% (122/137). Noguchi et al. [1] also reported that the presence of a periappendiceal hyperechoic structure may indicate advanced inflammation and associated complications in acute appendicitis, such as perforation, purulent exudates or abscess, and prominent adhesion to the periappendiceal tissue. Oudenhoven et al. [4] reported that hyperechoic, noncompressible fatty tissue representing inflamed mesentery and omentum was present in 100% (44/44) of patients with right colonic diverticulitis, which coincides with our result of 100% (18/18).

However, not all patients with RLQ inflammatory disease showed increased intraabdominal fat echo on sonography. In our study, 57 of 158 subjects with a normal intraabdominal fat echo received a positive final diagnosis (Table 2). A normal intraabdominal fat echo in 11% (15/137) of patients with acute appendicitis concurs with the findings of an earlier study in which 9% of such patients failed to show increased abdominal fat echo [9]. Presumably, subtle inflammatory changes of periappendiceal fat were responsible for these false-negative cases. Deep appendicitis, such as retrocecal or tip appendicitis, may also account for some misses. In our series, four of the 15 patients with acute appendicitis and a normal intraabdominal fat echo were found to have deep appendicitis. The paucity of intraabdominal fat in slim patients presents another obstacle to the evaluation of inflammatory fatty changes [16]. Interestingly, increased intraabdominal fat echo was not found in any of the 13 patients with mesenteric lymphadenitis in our series, which again is in close agreement with a previous report [2]. This may reflect the confinement of inflammation to the mesenteric lymph nodes and little extranodal infiltration.

In our series, seven patients had increased intraabdominal fat echo in the RLQ as an isolated finding without a visible cause on initial sonography. Among these, six (86%) patients were proven to have an active inflammatory disease—namely, acute appendicitis, pelvic inflammatory disease, or right colonic diverticulitis. Although increased intraabdominal fat echo may aid the localization and characterization of disease in most circumstances, it might paradoxically obscure the primary lesion by significantly attenuating sonic transmission. Given our finding that increased intraabdominal fat echo is a highly specific sign of an active inflammatory process, cases with increased intraabdominal fat echo without a visible cause should warrant further imaging study—for example, contrast-enhanced abdominal CT—or careful follow-up.

Some limitations of our study should be mentioned. First, given the inherently subjective nature of sonographic examinations, some degree of interobserver variability might be expected in the grading of intraabdominal fat echo. Intraabdominal fat echo was prospectively evaluated in each patient by the one radiologist performing the examination on the basis of real-time sonographic findings, rather than on retrospective review of captured still sonograms. Therefore, the evaluation of interobserver agreement among the radiologists was not possible in this study. However, the similar diagnostic performance measures obtained among the three radiologists (sensitivity, 67-79%; specificity, 97-100%; accuracy, 76-85%; PPV, 98-100%; NPV, 55-69%) argue that increased intraabdominal fat echo in patients with RLQ pain is a clinically useful and reproducible finding. Second, we did not take into account the still-debated effect of body mass index on the visualization of intraabdominal structures such as the appendix [17-19]. Third, laboratory tests, such as WBCs, erythrocyte sedimentation rates, and C-reactive protein, were not routinely included in the evaluation of acute RLQ pain because the focus of this study was to evaluate the diagnostic usefulness of increased intraabdominal fat echo. However, it might be interesting to compare the sonographic findings and laboratory data in patients with acute RLQ pain. Finally, cases of self-limiting or spontaneously resolving inflammatory diseases with negative sonographic results would have caused underestimation of false-negatives because no fully reliable method was available to confirm a diagnosis in those patients without histopathologic results. This limitation, however, is inevitable because not all patients with acute RLQ pain undergo surgery [9, 20].

In conclusion, increased intraabdominal fat echo on sonography in patients with acute RLQ pain was found to be highly specific for the presence of an inflammatory disease. Therefore, increased intraabdominal fat echo alone without a visible cause on sonographic examination should prompt further complimentary studies such as CT.

References

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This Article Abstract Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Lee, M. W. Articles by Yi, J. G. Search for Related Content PubMed PubMed Citation Articles by Lee, M. W. Articles by Yi, J. G. Social Bookmarking                      What's this? Hotlight (NEW!) What's Hotlight?