Pe d i a t r i c I m a g i n g • O r i g i n a l R e s e a r c h Trout et al. Imaging the Pediatric Appendix
FOCUS ON:
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Pediatric Imaging Original Research
JOURNAL CLUB: JOURNA L
CLUB
Andrew T. Trout 1 Alexander J. Towbin1 Bin Zhang2 Trout AT, Towbin AJ, Zhang B
The Pediatric Appendix: Defining Normal OBJECTIVE. The purpose of this study was to characterize the normal pediatric appendix and the variables that affect its diameter. MATERIALS AND METHODS. Imaging and medical records, including CT studies, from 420 unique patients with normal appendixes were reviewed by two pediatric radiologists. Appendiceal diameter was measured on the axial images, and appendiceal content and the presence of enlarged lymph nodes were recorded. RESULTS. The mean appendiceal diameter was 5.6 ± 1.4 and 5.7 ± 1.5 mm for reviewer 1 and reviewer 2, respectively, with 34% and 39% of appendixes measuring larger than 6 mm. Appendiceal diameter was normally distributed across the population and was significantly associated with patient age (p < 0.0001). Diameter increased by 0.4 mm/y until 6–7 years of age, after which, it remained stable. The quantity of pericecal fat (p = 0.03 and p < 0.0001) and type of appendiceal content (p = 0.0002 and p < 0.0001), respectively, were multivariate predictors of diameter. Lymphoid stimulation was a multivariate predictor of diameter for only one reviewer (p = 0.0008). Patient sex and the month or season of imaging were not predictors of diameter. CONCLUSION. Uniform diameter cutoffs for appendiceal diameter should not be applied across the pediatric population because the appendix grows during childhood. Additionally, this study calls into question a 6-mm diameter cutoff for appendicitis. Normal pediatric appendixes measure up to 8.7 mm, with up to 39% measuring more than 6 mm in diameter. Nonpathologic factors, including pericecal fat, appendiceal content, and presence of lymphoid stimulation, influence appendiceal diameter in healthy children.
U
Keywords: appendicitis, appendix, CT, normal DOI:10.2214/AJR.13.11030 Received April 7, 2013; accepted after revision July 1, 2013. 1 Department of Radiology, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Ave, Cincinnati, OH 45229. Address correspondence to A. T. Trout ([email protected]). 2 Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH.
This article is available for credit. AJR 2014; 202:936–945 0361–803X/14/2025–936 © American Roentgen Ray Society
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ltrasound is the imaging modality of choice in the initial evaluation of pediatric patients with suspected acute appendicitis [1, 2]. CT plays a valuable role in problem solving when clinical suspicion is high and ultrasound is unable to definitively diagnose or exclude appendicitis [1]. CT is also readily available throughout the community and abdominopelvic CT examinations are performed for other presumed causes of abdominal pain in pediatric patients. For these reasons, a substantial number of abdominopelvic CT studies are performed in children. The CT criteria for diagnosis of acute appendicitis have been debated in the literature [3–8]. These criteria form the basis of what is considered an “abnormal” appendix and by inference what is a “normal” appendix. There are little data specifically concerning the normal CT appearance of the pediatric appendix, with most information coming from control
subjects in studies of appendicitis [4, 5, 9, 10]. To date, we know of only three studies that have specifically evaluated the normal pediatric appendix by CT, all of which focused on factors influencing visibility [11–13]. A more detailed understanding of the normal CT appearance of the appendix in children is needed to inform diagnostic criteria and interpretation of pediatric abdominopelvic CT. In this study, we address this need by systematically assessing the normal appendiceal diameter in a large population of pediatric patients. We hypothesized that the normal appendix would vary in diameter across the population and that diameter would depend on nonpathologic variables, including age, appendiceal content, and degree of lymphoid stimulation. Materials and Methods This study is a component of a larger study of CT of the appendix in children for which institu-
AJR:202, May 2014
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Imaging the Pediatric Appendix TABLE 1: Patients Excluded From Study Population According to Exclusion Criteria
tional review board approval with a waiver of informed consent was obtained. All reviews of patient records were HIPAA compliant. Imaging records at our tertiary children’s hospital were searched for abdominopelvic CT studies interpreted between January 1 and December 31, 2010. CT studies in patients 18 years old or younger were included in the analysis. Examinations were subdivided by the month in which the CT was performed and were randomly ordered using Microsoft Office Excel 2007. Sufficient examinations were reviewed to identify 35 unique patient CT studies per calendar month in patients with normal appendixes. Examinations were ex-
cluded from analysis according to the following criteria: examination performed at an outside institution, images not available, coronal reformatted images not available, repeat examination in a patient, prior appendectomy, documented histories, or imaging findings of processes that might alter appendiceal diameter (e.g., appendicitis, lymphoid hyperplasia, inflammatory bowel disease, active colitis, Henoch-Schönlein purpura, cystic fibrosis, and hematologic malignancies). Lymphoma and hematologic malignancies were considered exclusion criteria because of the potential for abdominopelvic lymph node enlargement and involvement of appendiceal and periappendiceal lymphoid tissue and lymphatics. Examinations performed for a clinical indication of “rule out appendicitis” or for symptoms of appendicitis were not excluded unless appendicitis was ultimately diagnosed. Because of the potential effect of missed or self-resolving mild appendicitis on appendiceal diameter, the subgroup of patients who underwent CT for an indication of trauma without right lower quadrant symptoms was compared with the remainder of the population [14]. CT studies were independently reviewed by two board-certified pediatric radiologists (R1 and R2). Appendiceal diameter was measured in the axial plane at 400% magnification from the serosal-toserosal surface at the location of greatest transverse dimension (Fig. 1). The quantity of pericecal fat, appendiceal content, and presence of lymph nodes increased in size or number in the right lower quadrant or mesentery were recorded. The quantity of pericecal fat was scored 0–2 according to the system described by Nikolaidis et al. [15] (Fig. 2). Ap-
pendiceal contents recorded included nothing, air, fluid, contrast material, stool, appendicolith, or oth-
A
B
C
Fig. 1—Cropped axial CT image shows measurement of appendix in 11-year-old boy imaged for right-sided abdominal pain, fever, and vomiting. Appendix measures 6.9 mm in greatest transverse dimension in axial plane. There is no stranding in periappendiceal fat and appendix contains both contrast material and stool.
Reason for Exclusion Technical exclusions
No. of Excluded Patients Cases (%) 249
66.9
Examination performed at outside hospital
113
30.4
Repeat examination
82
22.0
Appendix not identified by both reviewers
34
9.1
No consensus
11
3.0
No coronal reformats
5
1.3
No images
3
0.8
Abdomen only Appendicitis Absent appendix
1
0.3
59
15.9
27
7.3
History of appendectomy
23
6.2
History of colectomy
3
0.8
History of enteric transplant
1
0.3
Inflammatory bowel disease
13
3.5
Colitis
9
2.4
Hematologic malignancy
9
2.4
Cystic fibrosis
3
0.8
Lymphoid hyperplasia
2
0.5
Henoch-Schönlein purpura
1
0.3
Fig. 2—Axial CT images show each of three grades (0–2) of pericecal fat quantity described by Nikolaidis et al. [15]. In each figure, appendix is indicated by arrow. A, Grade 0 shown in this 16-year-old boy is defined as fat surrounding less than half of circumference of cecum and measuring less than 1 cm in maximal thickness. B, Grade 1 shown in this 14-year-old boy is defined as fat surrounding more than half of circumference of cecum but measuring less than 1 cm in maximal thickness. C, Grade 2 shown in this 9-year-old girl is defined as fat surrounding more than half of circumference of cecum and measuring greater than 1 cm in maximal thickness.
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Trout et al. er (not easily classified) (Fig. 3). Lymph nodes were considered enlarged if they measured greater than 0.5 cm in the short axis [8]. After independent review, examinations in which the appendix was visualized by only one reviewer or in which the appendix was measured on images separated by more than 5 slices were reviewed in consensus. Examinations in which the appendix was not identified by both reviewers or in which consensus on identification of the appendix could not be achieved were excluded. Patient medical records were reviewed for demographic data and clinical histories relevant to the exclusion criteria. A diagnosis of appendicitis was assigned to patients who underwent appendectomy with pathologic proof of appendicitis and in
patients with symptoms clinically suggestive of appendicitis who were managed conservatively.
A
B
C
D
E
F
Statistics Descriptive analysis was performed for exclusion criteria and patient demographics. Appendiceal diameter was compared with a two-sample Student t test or one factor analysis of variance to detect differences on the basis of categoric variables. Pairwise comparison was used when appendiceal diameter was significantly different for a given variable with three or more categories. The association between appendiceal diameter and continuous variables was assessed by simple linear regression and multiple linear regression when controlling for covariates. Interobserver agree-
ment was assessed with the kappa test. All analyses were performed with SAS, version 9.3 (SAS Institute) and the level of significance for all analyses was set at 0.05. For seasonal analysis, the vernal and autumnal equinoxes and summer and winter solstices were used to define the seasons.
Results At our institution, 1648 abdominopelvic CT examinations were interpreted during the study period; 222 of the 1648 (13.5%) studies that were performed in patients more than 18 years old were excluded. Of the remaining 1426 examinations, 792 (55.5%) were reviewed to identify 35 unique patient examinations per month (total 420 examinations).
Fig. 3—Example CT images for subtypes of appendiceal content assessed in this study. A, Coronal reformatted image in 10-year-old female trauma victim shows appendix (arrow) folded back on itself containing nothing. B, CT image in 8-year-old male trauma victim shows appendix (arrow) containing air. C, CT image in 7-year-old boy with abdominal pain shows appendix (arrows) containing fluid. Note how appendiceal content is low in attenuation, similar to expected attenuation of fluid. D, CT image in 6-month-old girl with leukemia shows appendix (arrow) containing contrast material. E, CT image in 4-year-old boy with trauma shows appendix (arrow) containing stool. F, CT image in 11-year-old boy with trauma shows appendix containing appendicolith (arrow). Appendicolith appears as ovoid focus of high attenuation within otherwise collapsed appendix.
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Imaging the Pediatric Appendix TABLE 2: Normal Appendiceal Diameter Measured by Both Reviewers on Axial Images
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Parameter
95% CI Mean (mm) Median (mm) Mode (mm) SD (mm) (mean ± 2 SD)
All patients (including trauma) Reviewer 1
5.57
5.60
5.00
1.35
2.87–8.27
Reviewer 2
5.68
5.70
6.30
1.50
2.68–8.68
Reviewer 1
5.49
5.40
4.40
1.34
2.81–8.17
Reviewer 2
5.55
5.50
5.00
1.42
2.71–8.39
Reviewer 1
4.65
4.45
4.50
1.44
Reviewer 2
4.76
4.60
3.10
1.58
Reviewer 1
5.78
5.70
5.00
1.24
Reviewer 2
5.89
5.80
6.00
1.40
Trauma patients
Patients < 6.5 years old (n = 78)
Patients ≥ 6.5 years old (n = 342)
Note—The distribution and frequency of appendiceal diameters for the entire patient population are shown in Figure 4.
Table 1 details the reason for exclusion of 372 of 792 examinations (46.9%). The 45 patients in whom the appendix was not identified (34 not seen by either reviewer, no consensus in 11) were significantly younger than patients in whom the appendix was identified (8.8 ± 5.8 years, p = 0.0044). The mean age for the 420 patients included in this analysis was 11.0 ± 4.8 years (range, < 0.1–18 years); 51.4% (216/420) were girls. Descriptive statistics for appendiceal diameter are shown in Table 2 and graphically in Figure 4. Of note, 34.3% (144/420 for R1) and 39.3% (165/420 for R2) of appendixes measured larger than 6 mm. Table 3 details the results of univariate analysis of the association between appendiceal diameter and the assessed variables. We will discuss some specific variables of interest. Patient Age Age was significantly associated with appendiceal diameter (p < 0.0001 for both reviewers) with a mean increase of 0.1 mm in diameter per year of age between birth and 18 years. Stratifying patients by age at 1-year intervals, however, did not show a linear increase in diameter. Instead, there are two components to the diameter-age curve. The first part of the curve shows appendiceal diameter increasing until the child is 6–7 years old. After 6–7 years, the curve is relatively flat through 18 years old (Fig. 5). Regression lines fitted to the two portions of the diameter-age curve are significantly different in slope with a slope of 0.37
(R1) and 0.41 (R2) for 0–6.49 years old and 0.05 (R1) and 0.04 (R2) for ≥ 6.5 years old (p < 0.0001 for both reviewers). When the population was subdivided on the basis of this 6.5-year-old transition, appendiceal diameters were significantly different between the two groups (Table 2 and Fig. 6) with children younger than 6.5 years old having smaller appendixes than those 6.5 years old or older (p < 0.0001 for both reviewers). Pericecal Fat Grading Between reviewers there was moderate (к = 0.49) but significant (p < 0.0001) agreement in grading of pericecal fat. For both reviewers, the quantity of pericecal fat was significantly (p < 0.0001 for both reviewers) associated with appendiceal diameter, with the diameter increasing by 1.03 mm (R1) and 1.14 mm (R2) between grades 0 and 2. Time of Year Season of imaging was significantly associated with appendiceal diameter for R2 only (p = 0.037). Pairwise comparisons of appendiceal diameter by season showed that diameter was significantly greater in summer than in spring (mean difference, 0.5 mm) without significant differences between other seasons. Lymphoid Stimulation Between reviewers there was fair (к = 0.3517) but significant (p < 0.0001) agreement on the presence of lymph nodes increased in size or number. For both review-
ers, lymphoid stimulation was significantly (p = 0.0001 [R1], p = 0.0003 [R2]) associated with appendiceal diameter. In the presence of lymphoid stimulation, the appendix measured 0.51 mm (R1) and 0.56 mm (R2) larger. Appendiceal Content Appendiceal content at the location of measurement was significantly associated with appendiceal diameter (p < 0.0001 for both reviewers) (Table 3). Common themes between reviewers were that appendixes filled with contrast material were smallest, whereas those containing stool and fluid measured the largest (Table 3). On multivariate analysis including only variables that reached univariate statistical significance for both reviewers, patient age, appendiceal content, and pericecal fat grade remained statistically significant independent predictors of appendiceal diameter for both reviewers (Table 3). The presence of lymphoid stimulation remained a significant predictor of appendiceal diameter for reviewer 1 but only approached significance for reviewer 2 (Table 3). Analysis of Trauma Subpopulation CT was performed for trauma in 156 of 420 (37.1%) patients. Patients in this subgroup were significantly younger (10.1 ± 4.8 years, p = 0.0018) and significantly less likely to be girls (33.3%, p < 0.0001) than the rest of the population. Appendiceal diameter in this subgroup is detailed in Table 2. There was no significant difference in mean diameter in trauma patients compared with the remainder of the population (p = 0.241 [R1], p = 0.121 [R2]). Discussion Appendiceal diameter is considered an important criterion for the diagnosis of acute appendicitis in children [3, 5, 7, 10, 16, 17]. A diameter greater than 6 mm is frequently cited as the diagnostic cutoff for an abnormally enlarged or distended appendix [6, 7, 10, 18]. Studies have supported the use of this cutoff [6, 7], but its derivation and application are problematic for several reasons. First, the use of a 6-mm cutoff for diagnosing acute appendicitis originated in the ultrasound literature as a “guideline” but not an “absolute” [19]. Despite this, the 6-mm cutoff gained substantial traction and was later extrapolated to CT even though the appendix is compressed during sonography but not during CT.
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Trout et al. TABLE 3: Appendiceal Diameter on the Basis of Assessed Variables Variable
R1 (mean± SD) R2 (mean± SD) (mm) (mm)
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Sex
0.569/0.928
M
5.54 ± 1.42
5.69 ± 1.62
F
5.61 ± 1.28
5.68 ± 1.38
Age
NAa
NAa
Pericecal fat grading 0
5.18 ± 1.34
5.27 ± 1.47
1
5.74 ± 1.22
6.01 ± 1.35
2
6.21 ± 1.33
6.41 ± 1.39
5.71 ± 1.47
5.46 ± 1.39
Month of imaging January
< 0.0001
< 0.0001
< 0.0001
0.0283/< 0.0001
0.603/0.088
February
5.63 ± 1.42
5.45 ± 1.46
March
5.62 ± 1.33
5.60 ± 1.44
April
5.42 ± 1.20
5.56 ± 1.61
May
5.31 ± 1.26
5.39 ± 1.14
June
5.35 ± 1.27
5.28 ± 1.07
July
5.79 ± 1.07
5.99 ± 1.10
August
5.85 ± 1.34
6.12 ± 1.68
September
5.87 ± 1.63
6.33 ± 2.09
October
5.36 ± 1.35
5.53 ± 1.52
November
5.63 ± 1.38
5.87 ± 1.61
December
5.34 ± 1.43
5.63 ± 1.44
5.44 ± 1.16
5.46 ± 1.28
Time of year Spring
Univariate p Value Multivariate p Value (R1/R2) (R1/R2)
0.302/0.037
Summer
5.74 ± 1.35
6.01 ± 1.61
Fall
5.46 ± 1.38
5.70 ± 1.57
Winter
5.64 ± 1.48
5.54 ± 1.43
Present
5.84 ± 1.35
6.19 ± 1.56
Absent
5.33 ± 1.31
5.53 ± 1.45
Enlarged lymph nodes
Appendiceal content at location of measurement Air
5.32 ± 1.35
5.45 ± 1.31
Stool
6.96 ± 1.09
7.90 ± 1.49
Appendicolith
6.30 ± 1.83
6.14 ± 1.52
Contrast material
4.75 ± 1.62
4.58 ± 1.61
Fluid
6.12 ± 1.08
6.45 ± 1.71
Other
6.12 ± 1.22
Not assigned
Nothing
5.74 ± 1.18
5.89 ± 1.38
0.0001/0.0003
0.0008/0.0694
< 0.0001
0.0002/< 0.0001
Note—Both univariate and multivariate results are shown in this table; p values apply to comparisons within reviewers. When a single p value is given, it applies to both reviewers. Values for p that meet statistical significance (< 0.05) are indicated in bold. R1 = reviewer 1, R2 = reviewer 2, NA = not applicable. aContinuous variable.
Second, the 6-mm cutoff was described for adult patients but has been applied to pediatric patients without discussion of the va-
940
lidity of this direct translation. The lack of discussion around this point may reflect prior studies showing no association between
appendiceal diameter and age [20–22] and is bolstered by the reasonable diagnostic performance of a 6-mm cutoff in children [6, 7]. Lastly, the 6-mm cutoff has been used despite the lack of a systematic assessment of the normal pediatric appendix. In the 420 children evaluated in this study, appendiceal diameter is relatively normally distributed across the population (Fig. 4), a finding that has not been previously shown. Among these patients, the mean diameter of the normal appendix was 5.6–5.7 mm, with a normal range (95% CI) encompassing 2.7–8.7 mm and 34–39% of normal appendixes measuring greater than 6 mm in diameter. Although this represents a much larger sample than prior studies, the mean normal appendiceal diameter is concordant with diameters described in published pediatric studies (Table 4). The most informative finding of this study is that the appendix increases in diameter during childhood. This increase is not linear over time. Instead, the appendix increases in diameter by 0.4 mm per year until approximately 6.5 years of age after which point it changes little. Previous studies have not shown an association between appendiceal diameter and age or other patient-specific factors [20–22]. Studies by Ozel et al. [20] and Wiersma et al. [22] included 142 and 120 children, respectively, but were based on ultrasound measurements. Although those authors measured appendiceal diameter with and without compression, some degree of compression was likely always present. This supposition is supported by smaller mean diameters reported in these studies relative to diameters in the CT literature (4.2 ± 0.9 mm for the study by Ozel et al. and 3.9 ± 0.8 mm for the study by Wiersma et al.). A study of a mixed population of children and adults by Tamburinni et al. [21] was based on CT, but patients were subdivided into broad age categories (e.g., 0–30 years) likely masking increasing appendiceal diameter in younger patients. It should not be surprising that the appendix increases in diameter with age given what is known about the embryology and development of the appendix. Development of the appendix is characterized by a transition from a conical cecal base with a gradual transition to the appendix to a rounded cecal base with an abrupt transition to a uniformly narrow appendix [23–25]. During this process, the appendix migrates from the cecal tip to the left posterior wall of the cecum [23, 24]. The appendix also elongates during fetal life and is believed to continue to elongate after birth because the
AJR:202, May 2014
Imaging the Pediatric Appendix 25
Population (no.)
15
10
5
10.0
9.6
9.2
8.8
8.0
8.4
7.6
7.2
6.8
6.4
6.0
5.6
5.2
4.4
4.8
4.0
3.6
3.2
2.8
2.4
2.0
0 Appendiceal Diameter (mm)
A 25
20
Population (no.)
15
10
5
10.4
9.2 9.5 9.8 10.1
2.6 2.9 3.2 3.5 3.8 4.1 4.4 4.7 5.0 5.3 5.6 5.9 6.2 6.5 6.8 7.1 7.4 7.7 8.0 8.3 8.6 8.9
0 2.0 2.3
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20
Appendiceal Diameter (mm)
B Fig. 4—Population distribution of normal appendiceal diameters in 420 patients. A and B, Graphs show results measured by reviewer 1 (A) and reviewer 2 (B).
mean appendiceal length at birth is 4.5 cm whereas that in adults is 9.1–10 cm [24, 26]. In addition to the relationship between patient age and appendiceal diameter, we have identified other factors that influence appendiceal diameter independent of pathology, including quantity of pericecal fat and type of appendiceal content. As the quantity of pericecal fat increased, so did appendiceal diameter, with a slightly greater than 1-mm difference between patients with little to no pericecal fat and those with abundant pericecal fat. This finding is difficult to explain. It may be that the quantity of pericecal fat is a reflection of patient size, with higher rates of obesity in older children. Prior studies, however, have not shown an association between patient size (body mass index) and appendiceal diameter [20, 22]. Other possible (but unsupported) explanations include dietary differences or the presence of increased fat in the appendiceal wall. As for appendiceal content, the association between specific content and diameter has been previously shown in adults [27, 28]. In this study, there was some difference between reviewers regarding which contents were associated with larger appendiceal diameters, but general themes did emerge. Appendixes opacified by contrast material were generally smallest in diameter and those filled with stool or fluid were generally largest. Differences in diameter between appendixes with different contents were as great as 2 mm. Our finding of increased appendiceal diameter in the presence of fecal content is concordant with results previously reported by ultrasound [29]. Our results also suggest that appendixes may be larger in diameter in the setting of lymphoid stimulation. Univariate analysis showed a significant association between lymphoid stimulation and diameter for both reviewers. On multivariate analysis, howev-
TABLE 4: Summary of Published Values of Normal Appendiceal Diameter in Children No. of Patients
Patient Age (y) Mean Appendiceal (mean ± SD) Diameter (mm) (SD)
Reference
Year
Applegate et al. [4]
2001
32
Friedland and Siegel [5]
1997
25
9.8 10
Grayson et al. [12]
2001
120
Kaiser et al. [10]
2004
177
Ozturkmen et al. [11]
2007
72
Victoria and Mahboubi [33]
2010
13 (V) and 13 (G)
Hörmann et al. [34]
2002
15
Kovanlikaya et al. [35]
2012
28
Diameter Range (mm)
Notes
2–10 6 6
3–10
5.5
2–9
7.3
5 (1.34)
2.8–10
12 and 13
5 (1.3) and 5.1 (1.5)
14.3 ± 3.2
2.8–6.9 and 2.8–7.3 Comparison between V and G
4.5
3–5
5
2.5–7
MRE MRE; IBD patients without active symptoms
Note—V = barium preparation (VoLumen, Bracco Diagnostics), G = meglumine diatrizoate (Gastrografin, Bristol-Myers Squibb), MRE = MR enterography, IBD = inflammatory bowel disease.
AJR:202, May 2014 941
Trout et al.
Mean Appendiceal Diameter (mm)
7.0
6.0
5.0
4.0
3.0
17–18
16–16.9
15–15.9
14–14.9
13–13.9
12–12.9
11–11.9
10–10.9
9–9.9
8–8.9
7–7.9
6–6.9
5–5.9
4–4.9
3–3.9
2–2.9
1–1.9
0–0.9
2.0
Age (y)
A 9.0
Mean Appendiceal Diameter (mm)
8.0 7.0 6.0 5.0 4.0 3.0
17–18
16–16.9
15–15.9
14–14.9
13–13.9
12–12.9
11–11.9
10–10.9
9–9.9
8–8.9
7–7.9
6–6.9
5–5.9
4–4.9
3–3.9
2–2.9
1–1.9
2.0 0–0.9
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8.0
Age (y)
B Fig. 5—Mean normal appendiceal diameter as stratified by patient age. A and B, Graphs show data from reviewer 1 (A) and reviewer 2 (B). Error bars represent 1 SD of mean and trend lines reflect best-fit regression lines.
er, this persisted only for R1. For R2, there was a trend toward statistical significance (p = 0.069), which might have been reached with a larger population. Lymphoid hyperplasia of the appendix has been previously shown to result in increased mural thickness and appendiceal diameter to the point of mimicking acute appendicitis [30, 31]. If overall lymphoid activation in the abdomen is reflected in lymphoid stimulation in the appendix, this
942
would explain the observed association between mesenteric and right lower quadrant lymph nodes increased in size or number and increased appendiceal diameter. Factors that were not associated with appendiceal diameter included patient sex and season or month of imaging. To our knowledge, the association of these variables with appendiceal diameter has not been previously investigated. With regard to seasonal
variation, we had hypothesized that seasonal variance in the incidence of viral gastroenteritis would be reflected in the degree of gastrointestinal lymphoid stimulation and in appendiceal diameter. This was not the case because there was only a univariate association between appendiceal diameter and season for one reviewer. Moreover, for this reviewer, appendiceal diameter was largest in summer and was only significantly different when compared with appendiceal diameter for patients imaged in the spring. This distribution of diameters is not concordant with the seasonal rates of gastroenteritis, which is observed with greatest frequency from October to April [32]. Although our analysis represents the largest normal pediatric population reported in the literature, this study has potential limitations to the broad application of the reported findings. The findings of this study relate to a patient population at a single institution. Populations at other institutions may differ in some way relevant to the diameter of the appendix. For example, the immune stimulatory milieu might differ across geographic regions, possibly resulting in differences in appendiceal diameter. A second limitation of this study is the inclusion of patients who underwent CT for indications possibly reflecting underlying appendicitis. Although no patients had imaging findings of appendicitis or were clinically or surgically diagnosed with appendicitis, it is possible that some patients may have had missed or spontaneously resolving appendicitis, which might influence appendiceal diameter [14]. The fact that appendiceal diameters were not significantly different between the population as a whole and the subgroup of patients who underwent CT for trauma suggests, however, that if cases of missed appendicitis were included in the patient group, their effect on assessed diameter would be minimal. Finally, it is possible that the mean normal diameter for the described population might be skewed higher than the actual mean for pediatric patients because patients in whom the appendix was not identified were younger and likely had smaller appendixes. This study also has technical limitations. Measurements are limited to the resolution of the image pixel size and the appendix was measured on the axial images, which may not be an accurate reflection of the true transverse diameter of the appendix. However, because images are reviewed as axial
AJR:202, May 2014
Imaging the Pediatric Appendix Fig. 6—Population distribution of normal appendiceal diameters measured by reviewer 1, separating patients into subgroups on basis of age. Patients younger than 6.5 years old are shown in gray, and those 6.5 years old or older are shown in black.
20 18
Population (no.)
14 12 10 8 6 4 2 0
2.0 2.3 2.6 2.9 3.2 3.5 3.8 4.1 4.4 4.7 5.0 5.3 5.6 5.9 6.2 6.5 6.8 7.1 7.4 7.7 8.0 8.3 8.6 8.9 9.2 9.5 9.8
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16
Appendiceal Diameter (mm)
(with or without coronal) reconstructions in clinical practice, the reported diameters are more relevant. Finally, not every appendix was reviewed in consensus. It is possible that measurements are skewed by misidentification of the appendix by one or both reviewers. We do not believe this to be the case because in most of the consensus cases, despite slice differences both reviewers were found to have evaluated the same structure. This study represents the first large-scale systematic assessment of the normal pediatric appendix. The findings increase our understanding of the normal range and should influence interpretation of pediatric abdominopelvic CT. Specifically, our results suggest that uniform diameter cutoffs should not be applied across the pediatric population because the appendix grows during childhood. Moreover, our findings call into question the use of a 6-mm cutoff for appendicitis because the range of normal appendiceal diameters in children extends as high as 8.7 mm and up to 39% of pediatric patients have an appendix larger than 6 mm in diameter. Additionally, multiple nonpathologic factors, including pericecal fat, appendiceal content, and the presence of lymphoid stimulation, influence appendiceal diameter in healthy children. References 1. Strouse PJ. Pediatric appendicitis: an argument for US. Radiology 2010; 255:8–13 2. Rosen MP, Ding A, Blake MA, et al. ACR Appropriateness Criteria: right lower quadrant pain—suspected appendicitis. J Am Coll Radiol 2011; 8:749–755 3. Sivit CJ, Siegel MJ, Applegate KE, Newman KD. When appendicitis is suspected in children. RadioGraphics 2001; 21:247–262
4. Applegate KE, Sivit CJ, Myers MT, Pschesang B. Using helical CT to diagnose acute appendicitis in children: spectrum of findings. AJR 2001; 176:501–505 5. Friedland JA, Siegel MJ. CT appearance of acute appendicitis in childhood. AJR 1997; 168:439– 442 6. Lowe LH, Penney MW, Scheker LE, et al. Appendicolith revealed on CT in children with suspected appendicitis: how specific is it in the diagnosis of appendicitis? AJR 2000; 175:981–984 7. Mullins ME, Kircher MF, Ryan DP, et al. Evaluation of suspected appendicitis in children using limited helical CT and colonic contrast material. AJR 2001; 176:37–41 8. Rao PM, Rhea JT, Novelline RA. CT diagnosis of mesenteric adenitis. Radiology 1997; 202:145–149 9. Andre JB, Sebastian VA, Ruchman RM, Saad SA. CT and appendicitis: evaluation of correlation between CT diagnosis and pathological diagnosis. Postgrad Med J 2008; 84:321–324 10. Kaiser S, Finnbogason T, Jorulf HK, Soderman E, Frenckner B. Suspected appendicitis in children: diagnosis with contrast-enhanced versus nonenhanced helical CT. Radiology 2004; 231:427–433 11. Ozturkmen Akay H, Akpinar E, Akgul Ozmen C, Ergun O, Haliloglu M. Visualization of the normal appendix in children by non-contrast MDCT. Acta Chir Belg 2007; 107:531–534 12. Grayson DE, Wettlaufer JR, Dalrymple NC, Keesling CA. Appendiceal CT in pediatric patients: relationship of visualization to amount of peritoneal fat. AJR 2001; 176:497–500 13. Garcia K, Hernanz-Schulman M, Bennett DL, Morrow SE, Yu C, Kan JH. Suspected appendicitis in children: diagnostic importance of normal abdominopelvic CT findings with nonvisualized appendix. Radiology 2009; 250:531–537 14. Migraine S, Atri M, Bret PM, Lough JO, Hinchey
JE. Spontaneously resolving acute appendicitis: clinical and sonographic documentation. Radiology 1997; 205:55–58 15. Nikolaidis P, Hwang CM, Miller FH, Papanicolaou N. The nonvisualized appendix: incidence of acute appendicitis when secondary inflammatory changes are absent. AJR 2004; 183:889– 892 16. Garcia Peña BM, Mandl KD, Kraus SJ, et al. Ultrasonography and limited computed tomography in the diagnosis and management of appendicitis in children. JAMA 1999; 282:1041–1046 17. Kharbanda AB, Taylor GA, Bachur RG. Suspected appendicitis in children: rectal and intravenous contrast-enhanced versus intravenous contrast-enhanced CT. Radiology 2007; 243:520–526 18. Hoecker CC, Billman GF. The utility of unenhanced computed tomography in appendicitis in children. J Emerg Med 2005; 28:415–421 19. Jeffrey RB Jr, Laing FC, Townsend RR. Acute appendicitis: sonographic criteria based on 250 cases. Radiology 1988; 167:327–329 20. Ozel A, Orhan UP, Akdana B, et al. Sonographic appearance of the normal appendix in children. J Clin Ultrasound 2011; 39:183–186 21. Tamburrini S, Brunetti A, Brown M, Sirlin CB, Casola G. CT appearance of the normal appendix in adults. Eur Radiol 2005; 15:2096–2103 22. Wiersma F, Sramek A, Holscher HC. US features of the normal appendix and surrounding area in children. Radiology 2005; 235:1018–1022 23. Balthazar EJ, Gade M. The normal and abnormal development of the appendix: a radiographic assessment. Radiology 1976; 121:599–604 24. Buschard K, Kjaeldgaard A. Investigation and analysis of the position, fixation, length and embryology of the vermiform appendix. Acta Chir Scand 1973; 139:293–298 25. Wakeley CP. The position of the vermiform appendix as ascertained by an analysis of 10,000 cases. J Anat 1933; 67:277–283 26. Malas MA, Gokcimen A, Sulak O. Growing of caecum and vermiform appendix during the fetal period. Fetal Diagn Ther 2001; 16:173–177 27. Johnson PT, Eng J, Moore CJ, Horton KM, Fishman EK. Multidetector-row CT of the appendix in healthy adults. Emerg Radiol 2006; 12:248– 253 28. Webb EM, Wang ZJ, Coakley FV, Poder L, Westphalen AC, Yeh BM. The equivocal appendix at CT: prevalence in a control population. Emerg Radiol 2010; 17:57–61 29. Park NH, Park CS, Lee EJ, et al. Ultrasonographic findings identifying the faecal-impacted appendix: differential findings with acute appendicitis. Br J Radiol 2007; 80:872–877 30. Hahn HB, Hoepner FU, Kalle T, et al. Sonography of acute appendicitis in children: 7 years
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Trout et al. experience. Pediatr Radiol 1998; 28:147–151 31. Spear R, Kimmey MB, Wang KY, Sillery JK, Benjamin DR, Sawin RS. Appendiceal US scans: histologic correlation. Radiology 1992; 183:831–834 32. National Center for Immunization and Respiratory Diseases Division of Viral Diseases web-
site. Viral gastroenteritis. www.cdc.gov/ncidod/ dvrd/revb/gastro/faq.htm. Revised February 11, 2011. Accessed January 16, 2014 33. Victoria T, Mahboubi S. Normal appendiceal diameter in children: does choice of CT oral contrast (VoLumen versus Gastrografin) make a difference? Emerg Radiol 2010; 17:397–401
34. Hörmann M, Puig S, Prokesch SR, Partik B, Helbich TH. MR imaging of the normal appendix in children. Eur Radiol 2002; 12:2313–2316 35. Kovanlikaya A, Rosenbaum D, Mazumdar M, Dunning A, Brill PW. Visualization of the normal appendix with MR enterography in children. Pediatr Radiol 2012; 42:959–964
F O R YO U R I N F O R M AT I O N
This article is available for CME and Self-Assessment (SA-CME) credit that satisfies Part II requirements for maintenance of certification (MOC). To access the examination for this article, follow the prompts associated with the online version of the article. This article has been selected for AJR Journal Club activity. The accompanying Journal Club study guide can be found on the following page. For more information on Journal Clubs, see “Evidence-Based Radiology: A Primer in Reading Scientific Articles” in the July 2010 AJR at www.ajronline.org/cgi/content/full/195/1/w1.
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Imaging the Pediatric Appendix APPENDIX 1: AJR JOURNAL CLUB
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Study Guide The Pediatric Appendix: Defining Normal Alan Mautz1* Margaret Mulligan2 , Joseph J. Budovec2 1The Aroostook Medical Center, Presque Isle, ME 2 Medical College of Wisconsin, Milwaukee, WI [email protected], [email protected], [email protected] Introduction 1. What is the research question being asked with this study? How timely and relevant is the characterization of a normal pediatric appendix and diameter variables? Based on this, does the study attempt to answer a clinically important question? 2. What is the null hypothesis of this study? How would you state the alternative hypothesis? Methods 3. How were CT examinations selected for inclusion in this study? What were the exclusion criteria? How do the inclusion and exclusion criteria compare with similar studies? 4. What variables were considered as possible causes of variation in appendiceal diameter? 5. What are the limitations of this study? Are these limitations adequately discussed? Results 6. Was the research question answered? 7. How do the results compare with other studies of appendiceal measurement, both by ultrasound and CT? Medical Knowledge 8. How does this study advance the art and science of pediatric imaging? Discussion 9. What impact on clinical practice does this study have? 10. The study hypothesizes several possible causes of variation of appendiceal diameter. Should radiologists report the presence or absence of these when reviewing CT studies for appendicitis? 11. Does the study possess adequate statistical power to alter clinical practice? 12. What explanations does the study cite as possible regarding the differences between normal appendiceal diameters on ultrasound and the current study? Are these explanations satisfactory? Background Reading 1. Ozturkmen Akay H, Akpinar E, Akgul Ozmen C, Ergun O, Haliloglu M. Visualization of the normal appendix in children by non-contrast MDCT. Acta Chir Belg 2007; 107:531–534 2. Tamburrini S, Brunetti A, Brown M, Sirlin CB, Casola G. CT appearance of the normal appendix in adults. Eur Radiol 2005; 15:2096–2103
*Please note that the authors of the Study Guide are distinct from those of the companion article.
AJR:202, May 2014 945
FOCUS ON:
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Pediatric Imaging Original Research
JOURNAL CLUB: JOURNA L
CLUB
Andrew T. Trout 1 Alexander J. Towbin1 Bin Zhang2 Trout AT, Towbin AJ, Zhang B
The Pediatric Appendix: Defining Normal OBJECTIVE. The purpose of this study was to characterize the normal pediatric appendix and the variables that affect its diameter. MATERIALS AND METHODS. Imaging and medical records, including CT studies, from 420 unique patients with normal appendixes were reviewed by two pediatric radiologists. Appendiceal diameter was measured on the axial images, and appendiceal content and the presence of enlarged lymph nodes were recorded. RESULTS. The mean appendiceal diameter was 5.6 ± 1.4 and 5.7 ± 1.5 mm for reviewer 1 and reviewer 2, respectively, with 34% and 39% of appendixes measuring larger than 6 mm. Appendiceal diameter was normally distributed across the population and was significantly associated with patient age (p < 0.0001). Diameter increased by 0.4 mm/y until 6–7 years of age, after which, it remained stable. The quantity of pericecal fat (p = 0.03 and p < 0.0001) and type of appendiceal content (p = 0.0002 and p < 0.0001), respectively, were multivariate predictors of diameter. Lymphoid stimulation was a multivariate predictor of diameter for only one reviewer (p = 0.0008). Patient sex and the month or season of imaging were not predictors of diameter. CONCLUSION. Uniform diameter cutoffs for appendiceal diameter should not be applied across the pediatric population because the appendix grows during childhood. Additionally, this study calls into question a 6-mm diameter cutoff for appendicitis. Normal pediatric appendixes measure up to 8.7 mm, with up to 39% measuring more than 6 mm in diameter. Nonpathologic factors, including pericecal fat, appendiceal content, and presence of lymphoid stimulation, influence appendiceal diameter in healthy children.
U
Keywords: appendicitis, appendix, CT, normal DOI:10.2214/AJR.13.11030 Received April 7, 2013; accepted after revision July 1, 2013. 1 Department of Radiology, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Ave, Cincinnati, OH 45229. Address correspondence to A. T. Trout ([email protected]). 2 Division of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH.
This article is available for credit. AJR 2014; 202:936–945 0361–803X/14/2025–936 © American Roentgen Ray Society
936
ltrasound is the imaging modality of choice in the initial evaluation of pediatric patients with suspected acute appendicitis [1, 2]. CT plays a valuable role in problem solving when clinical suspicion is high and ultrasound is unable to definitively diagnose or exclude appendicitis [1]. CT is also readily available throughout the community and abdominopelvic CT examinations are performed for other presumed causes of abdominal pain in pediatric patients. For these reasons, a substantial number of abdominopelvic CT studies are performed in children. The CT criteria for diagnosis of acute appendicitis have been debated in the literature [3–8]. These criteria form the basis of what is considered an “abnormal” appendix and by inference what is a “normal” appendix. There are little data specifically concerning the normal CT appearance of the pediatric appendix, with most information coming from control
subjects in studies of appendicitis [4, 5, 9, 10]. To date, we know of only three studies that have specifically evaluated the normal pediatric appendix by CT, all of which focused on factors influencing visibility [11–13]. A more detailed understanding of the normal CT appearance of the appendix in children is needed to inform diagnostic criteria and interpretation of pediatric abdominopelvic CT. In this study, we address this need by systematically assessing the normal appendiceal diameter in a large population of pediatric patients. We hypothesized that the normal appendix would vary in diameter across the population and that diameter would depend on nonpathologic variables, including age, appendiceal content, and degree of lymphoid stimulation. Materials and Methods This study is a component of a larger study of CT of the appendix in children for which institu-
AJR:202, May 2014
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Imaging the Pediatric Appendix TABLE 1: Patients Excluded From Study Population According to Exclusion Criteria
tional review board approval with a waiver of informed consent was obtained. All reviews of patient records were HIPAA compliant. Imaging records at our tertiary children’s hospital were searched for abdominopelvic CT studies interpreted between January 1 and December 31, 2010. CT studies in patients 18 years old or younger were included in the analysis. Examinations were subdivided by the month in which the CT was performed and were randomly ordered using Microsoft Office Excel 2007. Sufficient examinations were reviewed to identify 35 unique patient CT studies per calendar month in patients with normal appendixes. Examinations were ex-
cluded from analysis according to the following criteria: examination performed at an outside institution, images not available, coronal reformatted images not available, repeat examination in a patient, prior appendectomy, documented histories, or imaging findings of processes that might alter appendiceal diameter (e.g., appendicitis, lymphoid hyperplasia, inflammatory bowel disease, active colitis, Henoch-Schönlein purpura, cystic fibrosis, and hematologic malignancies). Lymphoma and hematologic malignancies were considered exclusion criteria because of the potential for abdominopelvic lymph node enlargement and involvement of appendiceal and periappendiceal lymphoid tissue and lymphatics. Examinations performed for a clinical indication of “rule out appendicitis” or for symptoms of appendicitis were not excluded unless appendicitis was ultimately diagnosed. Because of the potential effect of missed or self-resolving mild appendicitis on appendiceal diameter, the subgroup of patients who underwent CT for an indication of trauma without right lower quadrant symptoms was compared with the remainder of the population [14]. CT studies were independently reviewed by two board-certified pediatric radiologists (R1 and R2). Appendiceal diameter was measured in the axial plane at 400% magnification from the serosal-toserosal surface at the location of greatest transverse dimension (Fig. 1). The quantity of pericecal fat, appendiceal content, and presence of lymph nodes increased in size or number in the right lower quadrant or mesentery were recorded. The quantity of pericecal fat was scored 0–2 according to the system described by Nikolaidis et al. [15] (Fig. 2). Ap-
pendiceal contents recorded included nothing, air, fluid, contrast material, stool, appendicolith, or oth-
A
B
C
Fig. 1—Cropped axial CT image shows measurement of appendix in 11-year-old boy imaged for right-sided abdominal pain, fever, and vomiting. Appendix measures 6.9 mm in greatest transverse dimension in axial plane. There is no stranding in periappendiceal fat and appendix contains both contrast material and stool.
Reason for Exclusion Technical exclusions
No. of Excluded Patients Cases (%) 249
66.9
Examination performed at outside hospital
113
30.4
Repeat examination
82
22.0
Appendix not identified by both reviewers
34
9.1
No consensus
11
3.0
No coronal reformats
5
1.3
No images
3
0.8
Abdomen only Appendicitis Absent appendix
1
0.3
59
15.9
27
7.3
History of appendectomy
23
6.2
History of colectomy
3
0.8
History of enteric transplant
1
0.3
Inflammatory bowel disease
13
3.5
Colitis
9
2.4
Hematologic malignancy
9
2.4
Cystic fibrosis
3
0.8
Lymphoid hyperplasia
2
0.5
Henoch-Schönlein purpura
1
0.3
Fig. 2—Axial CT images show each of three grades (0–2) of pericecal fat quantity described by Nikolaidis et al. [15]. In each figure, appendix is indicated by arrow. A, Grade 0 shown in this 16-year-old boy is defined as fat surrounding less than half of circumference of cecum and measuring less than 1 cm in maximal thickness. B, Grade 1 shown in this 14-year-old boy is defined as fat surrounding more than half of circumference of cecum but measuring less than 1 cm in maximal thickness. C, Grade 2 shown in this 9-year-old girl is defined as fat surrounding more than half of circumference of cecum and measuring greater than 1 cm in maximal thickness.
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Trout et al. er (not easily classified) (Fig. 3). Lymph nodes were considered enlarged if they measured greater than 0.5 cm in the short axis [8]. After independent review, examinations in which the appendix was visualized by only one reviewer or in which the appendix was measured on images separated by more than 5 slices were reviewed in consensus. Examinations in which the appendix was not identified by both reviewers or in which consensus on identification of the appendix could not be achieved were excluded. Patient medical records were reviewed for demographic data and clinical histories relevant to the exclusion criteria. A diagnosis of appendicitis was assigned to patients who underwent appendectomy with pathologic proof of appendicitis and in
patients with symptoms clinically suggestive of appendicitis who were managed conservatively.
A
B
C
D
E
F
Statistics Descriptive analysis was performed for exclusion criteria and patient demographics. Appendiceal diameter was compared with a two-sample Student t test or one factor analysis of variance to detect differences on the basis of categoric variables. Pairwise comparison was used when appendiceal diameter was significantly different for a given variable with three or more categories. The association between appendiceal diameter and continuous variables was assessed by simple linear regression and multiple linear regression when controlling for covariates. Interobserver agree-
ment was assessed with the kappa test. All analyses were performed with SAS, version 9.3 (SAS Institute) and the level of significance for all analyses was set at 0.05. For seasonal analysis, the vernal and autumnal equinoxes and summer and winter solstices were used to define the seasons.
Results At our institution, 1648 abdominopelvic CT examinations were interpreted during the study period; 222 of the 1648 (13.5%) studies that were performed in patients more than 18 years old were excluded. Of the remaining 1426 examinations, 792 (55.5%) were reviewed to identify 35 unique patient examinations per month (total 420 examinations).
Fig. 3—Example CT images for subtypes of appendiceal content assessed in this study. A, Coronal reformatted image in 10-year-old female trauma victim shows appendix (arrow) folded back on itself containing nothing. B, CT image in 8-year-old male trauma victim shows appendix (arrow) containing air. C, CT image in 7-year-old boy with abdominal pain shows appendix (arrows) containing fluid. Note how appendiceal content is low in attenuation, similar to expected attenuation of fluid. D, CT image in 6-month-old girl with leukemia shows appendix (arrow) containing contrast material. E, CT image in 4-year-old boy with trauma shows appendix (arrow) containing stool. F, CT image in 11-year-old boy with trauma shows appendix containing appendicolith (arrow). Appendicolith appears as ovoid focus of high attenuation within otherwise collapsed appendix.
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Imaging the Pediatric Appendix TABLE 2: Normal Appendiceal Diameter Measured by Both Reviewers on Axial Images
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Parameter
95% CI Mean (mm) Median (mm) Mode (mm) SD (mm) (mean ± 2 SD)
All patients (including trauma) Reviewer 1
5.57
5.60
5.00
1.35
2.87–8.27
Reviewer 2
5.68
5.70
6.30
1.50
2.68–8.68
Reviewer 1
5.49
5.40
4.40
1.34
2.81–8.17
Reviewer 2
5.55
5.50
5.00
1.42
2.71–8.39
Reviewer 1
4.65
4.45
4.50
1.44
Reviewer 2
4.76
4.60
3.10
1.58
Reviewer 1
5.78
5.70
5.00
1.24
Reviewer 2
5.89
5.80
6.00
1.40
Trauma patients
Patients < 6.5 years old (n = 78)
Patients ≥ 6.5 years old (n = 342)
Note—The distribution and frequency of appendiceal diameters for the entire patient population are shown in Figure 4.
Table 1 details the reason for exclusion of 372 of 792 examinations (46.9%). The 45 patients in whom the appendix was not identified (34 not seen by either reviewer, no consensus in 11) were significantly younger than patients in whom the appendix was identified (8.8 ± 5.8 years, p = 0.0044). The mean age for the 420 patients included in this analysis was 11.0 ± 4.8 years (range, < 0.1–18 years); 51.4% (216/420) were girls. Descriptive statistics for appendiceal diameter are shown in Table 2 and graphically in Figure 4. Of note, 34.3% (144/420 for R1) and 39.3% (165/420 for R2) of appendixes measured larger than 6 mm. Table 3 details the results of univariate analysis of the association between appendiceal diameter and the assessed variables. We will discuss some specific variables of interest. Patient Age Age was significantly associated with appendiceal diameter (p < 0.0001 for both reviewers) with a mean increase of 0.1 mm in diameter per year of age between birth and 18 years. Stratifying patients by age at 1-year intervals, however, did not show a linear increase in diameter. Instead, there are two components to the diameter-age curve. The first part of the curve shows appendiceal diameter increasing until the child is 6–7 years old. After 6–7 years, the curve is relatively flat through 18 years old (Fig. 5). Regression lines fitted to the two portions of the diameter-age curve are significantly different in slope with a slope of 0.37
(R1) and 0.41 (R2) for 0–6.49 years old and 0.05 (R1) and 0.04 (R2) for ≥ 6.5 years old (p < 0.0001 for both reviewers). When the population was subdivided on the basis of this 6.5-year-old transition, appendiceal diameters were significantly different between the two groups (Table 2 and Fig. 6) with children younger than 6.5 years old having smaller appendixes than those 6.5 years old or older (p < 0.0001 for both reviewers). Pericecal Fat Grading Between reviewers there was moderate (к = 0.49) but significant (p < 0.0001) agreement in grading of pericecal fat. For both reviewers, the quantity of pericecal fat was significantly (p < 0.0001 for both reviewers) associated with appendiceal diameter, with the diameter increasing by 1.03 mm (R1) and 1.14 mm (R2) between grades 0 and 2. Time of Year Season of imaging was significantly associated with appendiceal diameter for R2 only (p = 0.037). Pairwise comparisons of appendiceal diameter by season showed that diameter was significantly greater in summer than in spring (mean difference, 0.5 mm) without significant differences between other seasons. Lymphoid Stimulation Between reviewers there was fair (к = 0.3517) but significant (p < 0.0001) agreement on the presence of lymph nodes increased in size or number. For both review-
ers, lymphoid stimulation was significantly (p = 0.0001 [R1], p = 0.0003 [R2]) associated with appendiceal diameter. In the presence of lymphoid stimulation, the appendix measured 0.51 mm (R1) and 0.56 mm (R2) larger. Appendiceal Content Appendiceal content at the location of measurement was significantly associated with appendiceal diameter (p < 0.0001 for both reviewers) (Table 3). Common themes between reviewers were that appendixes filled with contrast material were smallest, whereas those containing stool and fluid measured the largest (Table 3). On multivariate analysis including only variables that reached univariate statistical significance for both reviewers, patient age, appendiceal content, and pericecal fat grade remained statistically significant independent predictors of appendiceal diameter for both reviewers (Table 3). The presence of lymphoid stimulation remained a significant predictor of appendiceal diameter for reviewer 1 but only approached significance for reviewer 2 (Table 3). Analysis of Trauma Subpopulation CT was performed for trauma in 156 of 420 (37.1%) patients. Patients in this subgroup were significantly younger (10.1 ± 4.8 years, p = 0.0018) and significantly less likely to be girls (33.3%, p < 0.0001) than the rest of the population. Appendiceal diameter in this subgroup is detailed in Table 2. There was no significant difference in mean diameter in trauma patients compared with the remainder of the population (p = 0.241 [R1], p = 0.121 [R2]). Discussion Appendiceal diameter is considered an important criterion for the diagnosis of acute appendicitis in children [3, 5, 7, 10, 16, 17]. A diameter greater than 6 mm is frequently cited as the diagnostic cutoff for an abnormally enlarged or distended appendix [6, 7, 10, 18]. Studies have supported the use of this cutoff [6, 7], but its derivation and application are problematic for several reasons. First, the use of a 6-mm cutoff for diagnosing acute appendicitis originated in the ultrasound literature as a “guideline” but not an “absolute” [19]. Despite this, the 6-mm cutoff gained substantial traction and was later extrapolated to CT even though the appendix is compressed during sonography but not during CT.
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Trout et al. TABLE 3: Appendiceal Diameter on the Basis of Assessed Variables Variable
R1 (mean± SD) R2 (mean± SD) (mm) (mm)
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Sex
0.569/0.928
M
5.54 ± 1.42
5.69 ± 1.62
F
5.61 ± 1.28
5.68 ± 1.38
Age
NAa
NAa
Pericecal fat grading 0
5.18 ± 1.34
5.27 ± 1.47
1
5.74 ± 1.22
6.01 ± 1.35
2
6.21 ± 1.33
6.41 ± 1.39
5.71 ± 1.47
5.46 ± 1.39
Month of imaging January
< 0.0001
< 0.0001
< 0.0001
0.0283/< 0.0001
0.603/0.088
February
5.63 ± 1.42
5.45 ± 1.46
March
5.62 ± 1.33
5.60 ± 1.44
April
5.42 ± 1.20
5.56 ± 1.61
May
5.31 ± 1.26
5.39 ± 1.14
June
5.35 ± 1.27
5.28 ± 1.07
July
5.79 ± 1.07
5.99 ± 1.10
August
5.85 ± 1.34
6.12 ± 1.68
September
5.87 ± 1.63
6.33 ± 2.09
October
5.36 ± 1.35
5.53 ± 1.52
November
5.63 ± 1.38
5.87 ± 1.61
December
5.34 ± 1.43
5.63 ± 1.44
5.44 ± 1.16
5.46 ± 1.28
Time of year Spring
Univariate p Value Multivariate p Value (R1/R2) (R1/R2)
0.302/0.037
Summer
5.74 ± 1.35
6.01 ± 1.61
Fall
5.46 ± 1.38
5.70 ± 1.57
Winter
5.64 ± 1.48
5.54 ± 1.43
Present
5.84 ± 1.35
6.19 ± 1.56
Absent
5.33 ± 1.31
5.53 ± 1.45
Enlarged lymph nodes
Appendiceal content at location of measurement Air
5.32 ± 1.35
5.45 ± 1.31
Stool
6.96 ± 1.09
7.90 ± 1.49
Appendicolith
6.30 ± 1.83
6.14 ± 1.52
Contrast material
4.75 ± 1.62
4.58 ± 1.61
Fluid
6.12 ± 1.08
6.45 ± 1.71
Other
6.12 ± 1.22
Not assigned
Nothing
5.74 ± 1.18
5.89 ± 1.38
0.0001/0.0003
0.0008/0.0694
< 0.0001
0.0002/< 0.0001
Note—Both univariate and multivariate results are shown in this table; p values apply to comparisons within reviewers. When a single p value is given, it applies to both reviewers. Values for p that meet statistical significance (< 0.05) are indicated in bold. R1 = reviewer 1, R2 = reviewer 2, NA = not applicable. aContinuous variable.
Second, the 6-mm cutoff was described for adult patients but has been applied to pediatric patients without discussion of the va-
940
lidity of this direct translation. The lack of discussion around this point may reflect prior studies showing no association between
appendiceal diameter and age [20–22] and is bolstered by the reasonable diagnostic performance of a 6-mm cutoff in children [6, 7]. Lastly, the 6-mm cutoff has been used despite the lack of a systematic assessment of the normal pediatric appendix. In the 420 children evaluated in this study, appendiceal diameter is relatively normally distributed across the population (Fig. 4), a finding that has not been previously shown. Among these patients, the mean diameter of the normal appendix was 5.6–5.7 mm, with a normal range (95% CI) encompassing 2.7–8.7 mm and 34–39% of normal appendixes measuring greater than 6 mm in diameter. Although this represents a much larger sample than prior studies, the mean normal appendiceal diameter is concordant with diameters described in published pediatric studies (Table 4). The most informative finding of this study is that the appendix increases in diameter during childhood. This increase is not linear over time. Instead, the appendix increases in diameter by 0.4 mm per year until approximately 6.5 years of age after which point it changes little. Previous studies have not shown an association between appendiceal diameter and age or other patient-specific factors [20–22]. Studies by Ozel et al. [20] and Wiersma et al. [22] included 142 and 120 children, respectively, but were based on ultrasound measurements. Although those authors measured appendiceal diameter with and without compression, some degree of compression was likely always present. This supposition is supported by smaller mean diameters reported in these studies relative to diameters in the CT literature (4.2 ± 0.9 mm for the study by Ozel et al. and 3.9 ± 0.8 mm for the study by Wiersma et al.). A study of a mixed population of children and adults by Tamburinni et al. [21] was based on CT, but patients were subdivided into broad age categories (e.g., 0–30 years) likely masking increasing appendiceal diameter in younger patients. It should not be surprising that the appendix increases in diameter with age given what is known about the embryology and development of the appendix. Development of the appendix is characterized by a transition from a conical cecal base with a gradual transition to the appendix to a rounded cecal base with an abrupt transition to a uniformly narrow appendix [23–25]. During this process, the appendix migrates from the cecal tip to the left posterior wall of the cecum [23, 24]. The appendix also elongates during fetal life and is believed to continue to elongate after birth because the
AJR:202, May 2014
Imaging the Pediatric Appendix 25
Population (no.)
15
10
5
10.0
9.6
9.2
8.8
8.0
8.4
7.6
7.2
6.8
6.4
6.0
5.6
5.2
4.4
4.8
4.0
3.6
3.2
2.8
2.4
2.0
0 Appendiceal Diameter (mm)
A 25
20
Population (no.)
15
10
5
10.4
9.2 9.5 9.8 10.1
2.6 2.9 3.2 3.5 3.8 4.1 4.4 4.7 5.0 5.3 5.6 5.9 6.2 6.5 6.8 7.1 7.4 7.7 8.0 8.3 8.6 8.9
0 2.0 2.3
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20
Appendiceal Diameter (mm)
B Fig. 4—Population distribution of normal appendiceal diameters in 420 patients. A and B, Graphs show results measured by reviewer 1 (A) and reviewer 2 (B).
mean appendiceal length at birth is 4.5 cm whereas that in adults is 9.1–10 cm [24, 26]. In addition to the relationship between patient age and appendiceal diameter, we have identified other factors that influence appendiceal diameter independent of pathology, including quantity of pericecal fat and type of appendiceal content. As the quantity of pericecal fat increased, so did appendiceal diameter, with a slightly greater than 1-mm difference between patients with little to no pericecal fat and those with abundant pericecal fat. This finding is difficult to explain. It may be that the quantity of pericecal fat is a reflection of patient size, with higher rates of obesity in older children. Prior studies, however, have not shown an association between patient size (body mass index) and appendiceal diameter [20, 22]. Other possible (but unsupported) explanations include dietary differences or the presence of increased fat in the appendiceal wall. As for appendiceal content, the association between specific content and diameter has been previously shown in adults [27, 28]. In this study, there was some difference between reviewers regarding which contents were associated with larger appendiceal diameters, but general themes did emerge. Appendixes opacified by contrast material were generally smallest in diameter and those filled with stool or fluid were generally largest. Differences in diameter between appendixes with different contents were as great as 2 mm. Our finding of increased appendiceal diameter in the presence of fecal content is concordant with results previously reported by ultrasound [29]. Our results also suggest that appendixes may be larger in diameter in the setting of lymphoid stimulation. Univariate analysis showed a significant association between lymphoid stimulation and diameter for both reviewers. On multivariate analysis, howev-
TABLE 4: Summary of Published Values of Normal Appendiceal Diameter in Children No. of Patients
Patient Age (y) Mean Appendiceal (mean ± SD) Diameter (mm) (SD)
Reference
Year
Applegate et al. [4]
2001
32
Friedland and Siegel [5]
1997
25
9.8 10
Grayson et al. [12]
2001
120
Kaiser et al. [10]
2004
177
Ozturkmen et al. [11]
2007
72
Victoria and Mahboubi [33]
2010
13 (V) and 13 (G)
Hörmann et al. [34]
2002
15
Kovanlikaya et al. [35]
2012
28
Diameter Range (mm)
Notes
2–10 6 6
3–10
5.5
2–9
7.3
5 (1.34)
2.8–10
12 and 13
5 (1.3) and 5.1 (1.5)
14.3 ± 3.2
2.8–6.9 and 2.8–7.3 Comparison between V and G
4.5
3–5
5
2.5–7
MRE MRE; IBD patients without active symptoms
Note—V = barium preparation (VoLumen, Bracco Diagnostics), G = meglumine diatrizoate (Gastrografin, Bristol-Myers Squibb), MRE = MR enterography, IBD = inflammatory bowel disease.
AJR:202, May 2014 941
Trout et al.
Mean Appendiceal Diameter (mm)
7.0
6.0
5.0
4.0
3.0
17–18
16–16.9
15–15.9
14–14.9
13–13.9
12–12.9
11–11.9
10–10.9
9–9.9
8–8.9
7–7.9
6–6.9
5–5.9
4–4.9
3–3.9
2–2.9
1–1.9
0–0.9
2.0
Age (y)
A 9.0
Mean Appendiceal Diameter (mm)
8.0 7.0 6.0 5.0 4.0 3.0
17–18
16–16.9
15–15.9
14–14.9
13–13.9
12–12.9
11–11.9
10–10.9
9–9.9
8–8.9
7–7.9
6–6.9
5–5.9
4–4.9
3–3.9
2–2.9
1–1.9
2.0 0–0.9
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8.0
Age (y)
B Fig. 5—Mean normal appendiceal diameter as stratified by patient age. A and B, Graphs show data from reviewer 1 (A) and reviewer 2 (B). Error bars represent 1 SD of mean and trend lines reflect best-fit regression lines.
er, this persisted only for R1. For R2, there was a trend toward statistical significance (p = 0.069), which might have been reached with a larger population. Lymphoid hyperplasia of the appendix has been previously shown to result in increased mural thickness and appendiceal diameter to the point of mimicking acute appendicitis [30, 31]. If overall lymphoid activation in the abdomen is reflected in lymphoid stimulation in the appendix, this
942
would explain the observed association between mesenteric and right lower quadrant lymph nodes increased in size or number and increased appendiceal diameter. Factors that were not associated with appendiceal diameter included patient sex and season or month of imaging. To our knowledge, the association of these variables with appendiceal diameter has not been previously investigated. With regard to seasonal
variation, we had hypothesized that seasonal variance in the incidence of viral gastroenteritis would be reflected in the degree of gastrointestinal lymphoid stimulation and in appendiceal diameter. This was not the case because there was only a univariate association between appendiceal diameter and season for one reviewer. Moreover, for this reviewer, appendiceal diameter was largest in summer and was only significantly different when compared with appendiceal diameter for patients imaged in the spring. This distribution of diameters is not concordant with the seasonal rates of gastroenteritis, which is observed with greatest frequency from October to April [32]. Although our analysis represents the largest normal pediatric population reported in the literature, this study has potential limitations to the broad application of the reported findings. The findings of this study relate to a patient population at a single institution. Populations at other institutions may differ in some way relevant to the diameter of the appendix. For example, the immune stimulatory milieu might differ across geographic regions, possibly resulting in differences in appendiceal diameter. A second limitation of this study is the inclusion of patients who underwent CT for indications possibly reflecting underlying appendicitis. Although no patients had imaging findings of appendicitis or were clinically or surgically diagnosed with appendicitis, it is possible that some patients may have had missed or spontaneously resolving appendicitis, which might influence appendiceal diameter [14]. The fact that appendiceal diameters were not significantly different between the population as a whole and the subgroup of patients who underwent CT for trauma suggests, however, that if cases of missed appendicitis were included in the patient group, their effect on assessed diameter would be minimal. Finally, it is possible that the mean normal diameter for the described population might be skewed higher than the actual mean for pediatric patients because patients in whom the appendix was not identified were younger and likely had smaller appendixes. This study also has technical limitations. Measurements are limited to the resolution of the image pixel size and the appendix was measured on the axial images, which may not be an accurate reflection of the true transverse diameter of the appendix. However, because images are reviewed as axial
AJR:202, May 2014
Imaging the Pediatric Appendix Fig. 6—Population distribution of normal appendiceal diameters measured by reviewer 1, separating patients into subgroups on basis of age. Patients younger than 6.5 years old are shown in gray, and those 6.5 years old or older are shown in black.
20 18
Population (no.)
14 12 10 8 6 4 2 0
2.0 2.3 2.6 2.9 3.2 3.5 3.8 4.1 4.4 4.7 5.0 5.3 5.6 5.9 6.2 6.5 6.8 7.1 7.4 7.7 8.0 8.3 8.6 8.9 9.2 9.5 9.8
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16
Appendiceal Diameter (mm)
(with or without coronal) reconstructions in clinical practice, the reported diameters are more relevant. Finally, not every appendix was reviewed in consensus. It is possible that measurements are skewed by misidentification of the appendix by one or both reviewers. We do not believe this to be the case because in most of the consensus cases, despite slice differences both reviewers were found to have evaluated the same structure. This study represents the first large-scale systematic assessment of the normal pediatric appendix. The findings increase our understanding of the normal range and should influence interpretation of pediatric abdominopelvic CT. Specifically, our results suggest that uniform diameter cutoffs should not be applied across the pediatric population because the appendix grows during childhood. Moreover, our findings call into question the use of a 6-mm cutoff for appendicitis because the range of normal appendiceal diameters in children extends as high as 8.7 mm and up to 39% of pediatric patients have an appendix larger than 6 mm in diameter. Additionally, multiple nonpathologic factors, including pericecal fat, appendiceal content, and the presence of lymphoid stimulation, influence appendiceal diameter in healthy children. References 1. Strouse PJ. Pediatric appendicitis: an argument for US. Radiology 2010; 255:8–13 2. Rosen MP, Ding A, Blake MA, et al. ACR Appropriateness Criteria: right lower quadrant pain—suspected appendicitis. J Am Coll Radiol 2011; 8:749–755 3. Sivit CJ, Siegel MJ, Applegate KE, Newman KD. When appendicitis is suspected in children. RadioGraphics 2001; 21:247–262
4. Applegate KE, Sivit CJ, Myers MT, Pschesang B. Using helical CT to diagnose acute appendicitis in children: spectrum of findings. AJR 2001; 176:501–505 5. Friedland JA, Siegel MJ. CT appearance of acute appendicitis in childhood. AJR 1997; 168:439– 442 6. Lowe LH, Penney MW, Scheker LE, et al. Appendicolith revealed on CT in children with suspected appendicitis: how specific is it in the diagnosis of appendicitis? AJR 2000; 175:981–984 7. Mullins ME, Kircher MF, Ryan DP, et al. Evaluation of suspected appendicitis in children using limited helical CT and colonic contrast material. AJR 2001; 176:37–41 8. Rao PM, Rhea JT, Novelline RA. CT diagnosis of mesenteric adenitis. Radiology 1997; 202:145–149 9. Andre JB, Sebastian VA, Ruchman RM, Saad SA. CT and appendicitis: evaluation of correlation between CT diagnosis and pathological diagnosis. Postgrad Med J 2008; 84:321–324 10. Kaiser S, Finnbogason T, Jorulf HK, Soderman E, Frenckner B. Suspected appendicitis in children: diagnosis with contrast-enhanced versus nonenhanced helical CT. Radiology 2004; 231:427–433 11. Ozturkmen Akay H, Akpinar E, Akgul Ozmen C, Ergun O, Haliloglu M. Visualization of the normal appendix in children by non-contrast MDCT. Acta Chir Belg 2007; 107:531–534 12. Grayson DE, Wettlaufer JR, Dalrymple NC, Keesling CA. Appendiceal CT in pediatric patients: relationship of visualization to amount of peritoneal fat. AJR 2001; 176:497–500 13. Garcia K, Hernanz-Schulman M, Bennett DL, Morrow SE, Yu C, Kan JH. Suspected appendicitis in children: diagnostic importance of normal abdominopelvic CT findings with nonvisualized appendix. Radiology 2009; 250:531–537 14. Migraine S, Atri M, Bret PM, Lough JO, Hinchey
JE. Spontaneously resolving acute appendicitis: clinical and sonographic documentation. Radiology 1997; 205:55–58 15. Nikolaidis P, Hwang CM, Miller FH, Papanicolaou N. The nonvisualized appendix: incidence of acute appendicitis when secondary inflammatory changes are absent. AJR 2004; 183:889– 892 16. Garcia Peña BM, Mandl KD, Kraus SJ, et al. Ultrasonography and limited computed tomography in the diagnosis and management of appendicitis in children. JAMA 1999; 282:1041–1046 17. Kharbanda AB, Taylor GA, Bachur RG. Suspected appendicitis in children: rectal and intravenous contrast-enhanced versus intravenous contrast-enhanced CT. Radiology 2007; 243:520–526 18. Hoecker CC, Billman GF. The utility of unenhanced computed tomography in appendicitis in children. J Emerg Med 2005; 28:415–421 19. Jeffrey RB Jr, Laing FC, Townsend RR. Acute appendicitis: sonographic criteria based on 250 cases. Radiology 1988; 167:327–329 20. Ozel A, Orhan UP, Akdana B, et al. Sonographic appearance of the normal appendix in children. J Clin Ultrasound 2011; 39:183–186 21. Tamburrini S, Brunetti A, Brown M, Sirlin CB, Casola G. CT appearance of the normal appendix in adults. Eur Radiol 2005; 15:2096–2103 22. Wiersma F, Sramek A, Holscher HC. US features of the normal appendix and surrounding area in children. Radiology 2005; 235:1018–1022 23. Balthazar EJ, Gade M. The normal and abnormal development of the appendix: a radiographic assessment. Radiology 1976; 121:599–604 24. Buschard K, Kjaeldgaard A. Investigation and analysis of the position, fixation, length and embryology of the vermiform appendix. Acta Chir Scand 1973; 139:293–298 25. Wakeley CP. The position of the vermiform appendix as ascertained by an analysis of 10,000 cases. J Anat 1933; 67:277–283 26. Malas MA, Gokcimen A, Sulak O. Growing of caecum and vermiform appendix during the fetal period. Fetal Diagn Ther 2001; 16:173–177 27. Johnson PT, Eng J, Moore CJ, Horton KM, Fishman EK. Multidetector-row CT of the appendix in healthy adults. Emerg Radiol 2006; 12:248– 253 28. Webb EM, Wang ZJ, Coakley FV, Poder L, Westphalen AC, Yeh BM. The equivocal appendix at CT: prevalence in a control population. Emerg Radiol 2010; 17:57–61 29. Park NH, Park CS, Lee EJ, et al. Ultrasonographic findings identifying the faecal-impacted appendix: differential findings with acute appendicitis. Br J Radiol 2007; 80:872–877 30. Hahn HB, Hoepner FU, Kalle T, et al. Sonography of acute appendicitis in children: 7 years
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Trout et al. experience. Pediatr Radiol 1998; 28:147–151 31. Spear R, Kimmey MB, Wang KY, Sillery JK, Benjamin DR, Sawin RS. Appendiceal US scans: histologic correlation. Radiology 1992; 183:831–834 32. National Center for Immunization and Respiratory Diseases Division of Viral Diseases web-
site. Viral gastroenteritis. www.cdc.gov/ncidod/ dvrd/revb/gastro/faq.htm. Revised February 11, 2011. Accessed January 16, 2014 33. Victoria T, Mahboubi S. Normal appendiceal diameter in children: does choice of CT oral contrast (VoLumen versus Gastrografin) make a difference? Emerg Radiol 2010; 17:397–401
34. Hörmann M, Puig S, Prokesch SR, Partik B, Helbich TH. MR imaging of the normal appendix in children. Eur Radiol 2002; 12:2313–2316 35. Kovanlikaya A, Rosenbaum D, Mazumdar M, Dunning A, Brill PW. Visualization of the normal appendix with MR enterography in children. Pediatr Radiol 2012; 42:959–964
F O R YO U R I N F O R M AT I O N
This article is available for CME and Self-Assessment (SA-CME) credit that satisfies Part II requirements for maintenance of certification (MOC). To access the examination for this article, follow the prompts associated with the online version of the article. This article has been selected for AJR Journal Club activity. The accompanying Journal Club study guide can be found on the following page. For more information on Journal Clubs, see “Evidence-Based Radiology: A Primer in Reading Scientific Articles” in the July 2010 AJR at www.ajronline.org/cgi/content/full/195/1/w1.
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AJR:202, May 2014
Imaging the Pediatric Appendix APPENDIX 1: AJR JOURNAL CLUB
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Study Guide The Pediatric Appendix: Defining Normal Alan Mautz1* Margaret Mulligan2 , Joseph J. Budovec2 1The Aroostook Medical Center, Presque Isle, ME 2 Medical College of Wisconsin, Milwaukee, WI [email protected], [email protected], [email protected] Introduction 1. What is the research question being asked with this study? How timely and relevant is the characterization of a normal pediatric appendix and diameter variables? Based on this, does the study attempt to answer a clinically important question? 2. What is the null hypothesis of this study? How would you state the alternative hypothesis? Methods 3. How were CT examinations selected for inclusion in this study? What were the exclusion criteria? How do the inclusion and exclusion criteria compare with similar studies? 4. What variables were considered as possible causes of variation in appendiceal diameter? 5. What are the limitations of this study? Are these limitations adequately discussed? Results 6. Was the research question answered? 7. How do the results compare with other studies of appendiceal measurement, both by ultrasound and CT? Medical Knowledge 8. How does this study advance the art and science of pediatric imaging? Discussion 9. What impact on clinical practice does this study have? 10. The study hypothesizes several possible causes of variation of appendiceal diameter. Should radiologists report the presence or absence of these when reviewing CT studies for appendicitis? 11. Does the study possess adequate statistical power to alter clinical practice? 12. What explanations does the study cite as possible regarding the differences between normal appendiceal diameters on ultrasound and the current study? Are these explanations satisfactory? Background Reading 1. Ozturkmen Akay H, Akpinar E, Akgul Ozmen C, Ergun O, Haliloglu M. Visualization of the normal appendix in children by non-contrast MDCT. Acta Chir Belg 2007; 107:531–534 2. Tamburrini S, Brunetti A, Brown M, Sirlin CB, Casola G. CT appearance of the normal appendix in adults. Eur Radiol 2005; 15:2096–2103
*Please note that the authors of the Study Guide are distinct from those of the companion article.
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