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Reevaluating the Sonographic Criteria for Acute Appendicitis in Children

Rationale and Objectives

There has been little rigorous evaluation of the sonographic criteria for acute appendicitis in children. Our clinical experience has called the traditional diagnostic criteria into question. We set out to review the literature, evaluate the most commonly applied diagnostic criteria for acute appendicitis, and identify those criteria that best predict the presence of disease.

Materials and Methods

A critical review of the literature concerning the sonographic diagnosis of acute appendicitis was performed. Based on diagnostic criteria identified in that review, two independent, blinded pediatric radiologists retrospectively reviewed 246 right lower quadrant ultrasound examinations in which the appendix was identified with attention to commonly described diagnostic criteria for acute appendicitis. Multivariate and classification and regression tree analysis were performed to identify criteria that predict appendicitis.

Results

In a multivariate analysis, inflammation of the periappendiceal fat is the only finding that statistically significantly predicts acute appendicitis (OR = 68.93, P < .0001). Other criteria such as diameter, noncompressibility, hyperemia, the presence of an appendicolith, and loss of stratification of the appendiceal wall do not independently predict appendicitis.

Conclusion

Periappendiceal fat infiltration is the most important diagnostic criterion for acute appendicitis in children. Strict application of other criteria such as diameter should be avoided.

Sonographic evaluation of the appendix was originally described in 1986 in a population of adults . Since that time, the technique has been adopted in children and due to the lack of ionizing radiation has largely become the technique of choice in this population . In the 25 years since the original article, there have been numerous analyses of the performance of ultrasound in diagnosing acute appendicitis in children. Interestingly, the diagnostic criteria that are applied for acute appendicitis are largely based on the adult population and these criteria, as they apply to children, have received significantly less analytic attention over that same 25-year period. A few studies have evaluated the diagnostic value of specific sonographic findings and a recent analysis has called into question the diagnostic criteria as historically defined in the literature . This recent publication resonated with our clinical experience as we have anecdotally noted the limited value of some of the traditional diagnostic criteria. Specifically, we hypothesized that appendiceal diameter >6 mm and lack of compressibility of the appendix are poor diagnostic criteria for acute appendicitis and that secondary findings such as periappendiceal fat infiltration better predict the presence of appendicitis.

Based on our clinical experience and this hypothesis, we set out to critically review the literature and to evaluate the diagnostic performance of common sonographic criteria for acute appendicitis in children.

Materials and methods

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Table 1

Diagnostic Criteria Assessed by Independent Reviewers and the Specific Definitions of these Criteria

Parameter Definition Maximal appendiceal diameter Maximum anteroposterior dimension of the appendix measured in millimeters from serosal to serosal surface while imaging the appendix in the transverse plane Compressibility ( Figure 6 ) Measurable, reproducible change in the caliber of the lumen of the appendix or noticeable deformation of the adjacent or overlying soft tissues

Appendiceal wall signature ( Figure 7 )

Appendiceal vascularity ( Figure 8 ) Assessed with color or power Doppler, relative to adjacent normal soft tissue

Periappendiceal fat infiltration ( Figures 3 and 4 ) Increased echogenicity of the periappendiceal fat relative to normal intraabdominal fat with associated thickening

Presence of appendicolith ( Figure 9 ) Echogenic, well-defined focus within the appendix with posterior acoustic shadowing

Presence of fluid Simple or complex fluid without a defined wall

Fluid characteristics

Presence of organized fluid collection Loculated fluid collection surrounded by a definable wall with associated mass effect

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Statistical Analysis

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Results

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Table 2

Summary of Diagnostic Parameters as Recorded by Both Readers

Parameter_n_ (%) Pathology Conclusion Normal Appendicitis Perforated Appendicitis Mean maximal diameter Reader 1: 5.9 ± 1.8 mm 10.2 ± 3.1 mm 10.1 ± 4.1 mm Reader 2: 5.7 ± 1.6 mm 10 ± 2.9 mm 10.3 ± 3.1 mm Compressibility Yes Reader 1: 40 (18.2%) 26 9 5 Reader 2: 42 (19%) 36 6 0 No Reader 1: 17 (7.7%) 1 11 5 Reader 2: 58 (26.2%) 6 17 35 Inadequate compression Reader 1: 163 (74.1%) 90 56 17 Reader 2: 121 (54.8%) 76 35 10 Appendiceal wall signature 3 rings (normal) Reader 1: 155 (70.5%) 108 38 9 Reader 2: 154 (69.7%) 112 34 8 2 rings Reader 1: 59 (26.8%) 9 34 16 Reader 2: 58 (26.2%) 6 36 16 1 ring Reader 1: 6 (2.7%) 0 4 2 Reader 2: 9 (4.1%) 0 6 3 Appendiceal vascularity Normal Reader 1: 78 (53.4%) 59 14 5 Reader 2: 61 (41.8%) 49 9 3 Increased Reader 1: 55 (37.7%) 7 38 10 Reader 2: 67 (45.9%) 12 43 12 Decreased/absent Reader 1: 13 (8.9%) 0 10 3 Reader 2: 18 (12.3%) 2 12 4 Periappendiceal fat infiltration Absent Reader 1: 120 (52.4%) 110 10 0 Reader 2: 119 (51.5%) 110 9 0 Present Reader 1: 109 (47.6%) 15 66 28 Reader 2: 112 (48.5%) 18 67 27 Presence of appendicolith Yes Reader 1: 38 (17.3%) 3 25 10 Reader 2: 32 (14.5%) 3 21 8 No Reader 1: 182 (82.7%) 114 51 17 Reader 2: 189 (85.5%) 115 55 19 Presence of fluid Yes Reader 1: 135 (58.7%) 67 46 22 Reader 2: 104 (45.2%) 49 38 19 No Reader 1: 95 (41.3%) 59 30 6 Reader 2: 124 (53.9%) 77 38 9 Fluid characteristics Simple Reader 1: 105 (78.4%) 65 34 6 Reader 2: 80 (75.5%) 44 26 10 Complex Reader 1: 29 (21.6%) 1 12 16 Reader 2: 26 (24.5%) 5 12 9 Presence of organized fluid collection Yes Reader 1: 8 (3.4%) 0 2 6 Reader 2: 5 (2.1%) 0 1 4 No Reader 1: 225 (96.6%) 129 74 22 Reader 2: 228 (97.9%) 129 75 24

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Appendiceal Diameter

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Table 3

Frequency of Acute Appendicitis (Perforated and Nonperforated) Based on Maximal Appendiceal Diameter

Diameter_n_ Appendicitis (Perforated, Nonperforated) Normal Sensitivity Specificity PPV NPV Accuracy 2–4 mm R1: 22 (10%) 2 (1, 1) 20 R2: 25 (11.3%) 1 (0, 1) 24 5 mm R1: 32 (14.5%) 3 (3, 0) 29 95.1% 41.9% 59% 90.7% 66.8% R2: 36 (16.3%) 2 (1, 1) 34 97.1% 49.2% 62.5% 95.1% 71.5% 6 mm R1: 45 (20.5%) 10 (3, 7) 35 85.4% 71.8% 72.7% 84.8% 78.2% R2: 43 (19.5%) 7 (2, 5) 36 90.3% 79.7% 79.5% 90.4% 84.6% 7 mm R1: 23 (10.5%) 11 (1, 10) 12 74.8% 82.1% 78.6% 78.7% 78.6% R2: 21 (9.5%) 12 (2, 10) 9 78.6% 87.3% 84.4% 82.4% 83.3% 8 mm R1: 16 (7.3%) 5 (2, 3) 11 69.9% 91.5% 87.8% 77.5% 81.4% R2: 14 (6.3%) 7 (2, 5) 7 71.8% 93.2% 90.2% 79.1% 83.3% ≥9 mm R1: 82 (37.3%) 72 (17, 55) 10 R2: 82 (37.1%) 74 (20, 54) 8

NPV, negative predictive value; PPV, positive predictive value; R1, reader 1; R2, reader 2.

Sensitivity, specificity, PPV and NPV results are based on using that diameter as a diagnostic cutoff.

Figure 1, Receiver operating characteristic curve for appendiceal diameter for reader 1.

Figure 2, Receiver operating characteristic curve for appendiceal diameter for reader 2.

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Other Diagnostic Parameters

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Table 4

Statistical Significance of Individual Diagnostic Parameters for a Diagnosis of Acute Appendicitis Based upon Univariate Analysis of Findings Recorded by Readers 1 and 2

Parameter Reader 1 Reader 2 Interrater Agreement (95% Confidence Interval) Odds Ratio_P_ Value Odds Ratio_P_ Value Sex (male) 1.99 .0120 – Age 1.03 .0914 – Body mass index 2.43 .0262 – Appendiceal diameter Continuous variable 1.02 .1286 1.02 .0933 0.9* 6-mm cutoff 14.12 <.0001 32.22 <.0001 7-mm cutoff 14.93 <.0001 36.43 <.0001 8-mm cutoff 13.54 <.0001 25.28 <.0001 Compressibility (no) 0.03 <.0001 0.02 <.0001 0.675 (0.469–0.882) Appendiceal wall signature 0.741 (0.645–0.836) 1 ring vs. 3 rings NA .0010 NA <.0001 2 rings vs. 3 rings 12.77 <.0001 23.09 <.0001 Vascularity 0.755 (0.653–0.857) Decreased vs. normal NA <.0001 NA <.0001 Increased vs. normal 21.29 <.0001 18.72 <.0001 Periappendiceal fat infiltration (yes) 68.93 <.0001 63.83 <.0001 0.886 (0.825–0.946) Appendicolith (yes) 19.56 <.0001 15.02 <.0001 0.898 (0.818–0.979) Free fluid (yes) 1.66 .0801 1.91 .0173 0.674 (0.579–0.769) Fluid characteristics (complex vs. anechoic) 45.5 <.0001 5.13 .0015 0.713 (0.552–0.873) Organized fluid collection NA .0014 NA .0168 0.763 (0.497–1)

Interrater agreement for each parameter is also provided expressed as kappa statistics with Pearson correlation (*) reported for appendiceal diameter as a continuous variable. Odds ratios indicated as “NA” are a result of inability to calculate the odds ratio in situations in which there is a frequency of zero in any one of the diagnostic categories.

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Figure 3, Periappendiceal fat infiltration. (a) A 2 year old with abdominal pain. Ultrasound shows a normal appendix with normal periappendiceal fat. The fat is intermediate in echogenicity and without mass effect. (b) A 10 year old with right lower quadrant pain. Ultrasound shows circumferential echogenic fat ( asterisks ) around a distended, abnormal appendix in a patient with acute appendicitis. Note the increased thickness and poor definition of the fat in addition to the altered echogenicity.

Figure 4, A 10 year old with right lower quadrant pain and periappendiceal fat infiltration resulting from acute appendicitis. In this image, the appendix is oriented longitudinally. Note the echogenic, thickened periappendiceal fat ( asterisks ) surrounding the abnormal appendix (A). The signature of the appendiceal wall is abnormal with only a single echogenic layer visible.

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Figure 5, Classification and Regression Tree (CART) analysis based on reader 1. Each decision point in the tree is the result of application of one of the diagnostic criteria. Criteria with the greatest discriminatory efficacy are placed earlier in the tree. Percentages indicated in parentheses are the rate of appendicitis in that subgroup. Note that periappendiceal fat stranding most effectively classifies patients (highest percentage of appendicitis in the positive group and lowest percentage in the negative group). Application of additional diagnostic criteria change the diagnostic probability as indicated but do not substantially change the classification of patients to “appendicitis” or “not appendicitis.”

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Discussion

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Appendiceal Diameter

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Table 5

Diameters of Normal and Acutely Inflamed Appendices Reported in the Pediatric Literature

Study Study Type_n_ Mean Normal Diameter Mean Appendicitis Diameter Goldin, 2011 Retrospective 204 5.0 mm (range 2.0–11.0) ∗ 9.0 (range 1.3–20.0 mm) ∗ Hahn, 1998 Prospective 542 suspected appendicitis

54 healthy 3.9 (±1.2) mm 10.9 (±3.1) mm Ozel, 2011 Prospective 142 4.2 (±0.9) mm – Park, 2007 Prospective 51 – 9.7 mm (range 6.7–21.2 mm) Wiersma, 2005 Prospective 118 3.9 mm (range 2.1–6.4 mm) – Our data Retrospective 216 5.9 (±1.7) mm 10.5 (±3.1) mm

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Table 6

Performance of Specific Diameter Cutoffs in the Diagnosis of Acute Appendicitis as Reported in the Literature

Study Study Type Population Total n__n Used for Analysis Diameter Cutoff Sens Spec Acc OR Je, 2009 Retrospective Pediatric 160 160 >5.7 mm 89.6 93.2 Peletti, 2006 Prospective Pediatric 107 100 >6 mm 100 98 Goldin, 2011 Retrospective Pediatric 304 204 >7 mm 89.7 95.4 93.2 Kessler, 2004 Prospective Adult 125 104 >6 mm 98 98 97 Rettenbacher, 2001 Prospective Adult 710 518 >6 mm 100 68 79 van Randen, 2010 Prospective Adult 942 528 >6 mm 9.4 Worrel, 1990 Prospective Adult 200 200 >6 mm 66 93

Sens, sensitivity; spec, specificity; acc, accuracy; OR, odds ratio.

Although diameter is commonly used as a diagnostic criterion, these were among the few studies that looked at diameter as an independent predictor in the sonographic evaluation of appendicitis.

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Compressibility

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Figure 6, Compression of a normal appendix. In this 15 year old with right lower quadrant pain, the normal appendix is indicated by the arrows . (a) With gentle pressure the appendix is more round in configuration. During compression (b) , there is a notable change in diameter of the appendix which is now more ovoid in configuration.

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Altered Appendiceal Wall Signature

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Figure 7, Appendiceal wall signature. In this 4 year old with right lower quadrant pain, the normal appendix (a) has three concentric hyperechoic rings formed by the serosa, submucosa, and mucosa. Progressive inflammation results in loss of these concentric rings beginning with the mucosa. (b) In this 15 year old with right lower quadrant pain, the appendix has a two-ring appearance with the echogenic submucosal and serosa still visible. (c) In this 10 year old with acute appendicitis, ultrasound shows loss of all but the outer serosal echogenic ring.

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Vascularity

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Figure 8, Hypervascularity in acute appendicitis. Normally, flow greater than that of normal adjacent soft tissue should not be detectable within the wall of the appendix. In this 10 year old with right lower quadrant pain, there is increased blood flow in the wall ( arrowheads ) and within the echogenic periappendiceal fat.

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Periappendiceal Fat Infiltration

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Appendicolith

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Figure 9, Longitudinal (a) and transverse (b) images of appendicoliths. In this 11 year old with right lower quadrant pain, appendicoliths appear as echogenic foci ( arrows ) with associated posterior acoustic shadowing ( arrowheads ) within the appendiceal lumen. Note the normal appendiceal wall in (a) with three discrete echogenic layers.

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Presence of Fluid

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Approach to Ultrasound in Suspected Acute Appendicitis

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Acknowledgment

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