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Clinical Observations |
1 Department of Radiology, Children's Hospital Boston and Harvard Medical
School, 300 Longwood Ave., Boston, MA 02115.
2 Department of Orthopaedic Surgery, Children's Hospital Boston and Harvard
Medical School, Boston, MA 02115.
Received January 11, 2005;
accepted after revision March 7, 2005.
Address correspondence to G. A. Taylor
(george.taylor{at}childrens.harvard.edu).
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CONCLUSION. Appendicitis is not rare in young children and imaging findings reflect the high frequency of perforation in this population.
Keywords: abdominal imaging • CT • pediatric imaging • sonography
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Sonography and CT criteria for appendicitis have been largely defined in adults and in children without further stratification of patients by age [8-10]. Imaging findings in the high-risk group of young children have not received much attention and are not well described. This study was undertaken to compare the imaging characteristics of younger children (< 5 years old) to those of older children and to determine the impact of a younger age on sonography and CT diagnoses and the clinical outcomes of appendiceal perforation and negative appendectomy rate.
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The diagnosis of appendicitis was confirmed pathologically in all cases. However, some patients with a perforated appendix and periappendiceal abscess were first treated medically with antibiotics or by catheter drainage before an interval appendectomy at a later time after the acute process had resolved. In some of these cases, pathology showed that the appendix had already returned to normal. Therefore, in this small group of patients, the diagnosis of appendicitis was based on clinical course, classical CT findings for appendicitis, and clinical outcome (6-month follow-up postdischarge).
Based on a retrospective review of electronic medical records by two of the authors, the following data were obtained: demographic information, types of imaging studies performed, imaging findings on sonography and CT, CT technique used, imaging interpretation, surgical and pathologic findings, and clinical course of those who underwent an interval appendectomy. Only initial interpretations by a board-certified pediatric radiologist or a second-year pediatric radiology fellow were used for this study.
Imaging was considered after initial evaluation by emergency department physicians and subsequent examination by a fourth- or fifth-year surgical resident. Sonography or CT was used as the initial imaging study depending on an institutional clinical practice guideline developed jointly by the departments of emergency medicine, surgery, and radiology. Patients who were imaged with both techniques typically underwent sonography first followed by CT if the initial study was indeterminate or negative for appendicitis. All CT studies were performed on a helical Hi-Speed Advantage single-detector scanner (GE Healthcare). Images were acquired from the iliac crests (bottom of the L3 vertebral body) through the pubic rami using helical mode at a pitch of 1.5:1, with 5-mm collimation, reconstructed at a 3-mm interval. The study was extended to the entire abdomen if any abnormality was detected on the most cephalad images.
During the study, one of three helical CT techniques was used to evaluate clinically suspected appendicitis depending on the patient's characteristics: rectal contrast material only, rectal and IV contrast material, and oral and IV contrast material. The first imaging protocol implemented in our department consisted of a limited abdominal helical CT with rectal contrast material only and was in effect from November 1999 to May 2000 [11]. Our standard protocol was modified to include the use of both rectal and IV contrast material and was in effect from June 1, 2000, to February 1, 2004 [12]. Patients unable to tolerate or retain rectal contrast material were imaged using oral and IV contrast material.
Exclusionary criteria for administration of rectal contrast material were patient age less than 4 years, developmental delay, inability to tolerate or retain rectal contrast material, presence of bloody stools, or preexisting conditions that placed patients at a high risk for intestinal perforation (inflammatory bowel disease, transplant recipients, oncology patients, or children with collagen vascular disorders). These children received oral contrast material 1 or 2 hours before imaging. All eligible patients were given IV contrast material. Patients with a contraindication to IV contrast material administration were imaged with rectal contrast material only.
Pelvic sonograms were performed using a Sequoia sonography unit (Siemens Medical Solutions) equipped with 5.0- and 7.5-MHz linear array transducers and the graded-compression technique.
Imaging Diagnostic Criteria
Criteria for the diagnosis of appendicitis by CT included the presence of
direct signs such as an enlarged appendix (> 6 mm), a nonopacified
appendiceal lumen, and significant wall enhancement with IV contrast material.
Indirect CT signs included periappendiceal fat stranding, appendicolith, free
fluid or abscess in the right lower quadrant or pelvis, or focal cecal wall
thickening [10,
13].
The criterion for the diagnosis of appendicitis by sonography was the
detection of a fluid-filled, noncompressible, distended tubular structure
(
6 mm in diameter) with or without an appendicolith that showed no
peristaltic activity, appeared constant in shape and position, and was located
either anterior to the psoas muscle or in a retrocecal position. The presence
of pericecal inflammatory changes in the absence of visualizing an abnormal
appendix was considered suggestive but not specific for acute appendicitis
[14,
15].
Statistical Analysis
The cohort was divided into two subgroups: children less than 5 years old
and children 5 years old or above. All results were calculated for each age
group, and comparisons were performed between them.
Using standard formulas, diagnostic parameters were calculated separately for each imaging technique—sonography, CT, and CT/sonography—including sensitivity, specificity, and false-positive and false-negative ratios [16]. The population evaluated in this study included only patients who had surgical and pathologic confirmation of appendicitis, not all patients imaged for suspected appendicitis. Therefore, diagnostic parameters such as specificity and accuracy were not evaluated. True-negative refers to patients with imaging studies interpreted as negative who were taken to surgery for clinical suspicion of appendicitis and were proven by pathologic examination not to have the disease. False-negative refers to patients with imaging studies interpreted as negative for appendicitis who were taken to surgery and proven to have the disease by pathologic examination.
Continuous variables were expressed in terms of the mean and SD and compared using Student's t tests. Proportions were compared using Fisher's exact tests or Pearson chi-square tests as appropriate. Logistic regression analysis was performed to describe the relationship between the age of the patient and the likelihood of perforation of the appendix with probability based on maximum likelihood estimation and the resulting exponential equation fitted using the regression coefficients (slope and y-intercept) based on the final logistic model [17]. Statistical analysis was conducted using the SPSS Statistical Package, Version 12.0 (SPSS). A two-tailed value of p < 0.05 was considered statistically significant.
An imaging study interpreted by the radiologist as positive for appendicitis was categorized as true-positive when appendicitis was proven by pathology or by clinical course (in those patients who underwent an interval appendectomy) and as false-positive when the pathologic examination was negative for appendicitis. A sonography or CT study interpreted as negative for appendicitis by the radiologist was categorized as true-negative when the pathology was negative, and it was categorized as false-negative when the pathology was positive for appendicitis. Equivocal radiologic interpretations of appendicitis were categorized as indeterminate and were not included in our initial test performance calculations.
A negative urgent laparotomy was considered negative when the pathology report indicated no histologic inflammation of the appendix. Perforation was based on macroscopic surgical findings.
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The age distribution of the 67 children less than 5 years old was the following: five (8%) children less than 2 years old, nine (13%) children from 2 to 3 years old, 32 (48%) children from 3 to 4 years old, and 21 (31%) children more than 4 years old. Although the majority of children were between 3 and 4 years old, more than 20% were younger (Fig. 1).
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Appendiceal perforation was present in 178 of 688 children (25.9%) with confirmed appendicitis. Children with a perforated appendix were significantly younger (mean age, 9.8 ± 4.5 years) than children with nonperforated appendicitis (mean age, 11.9 ± 3.5 years, p < 0.0001 by t test). In addition, the rate of appendiceal perforation was markedly higher in children less than 5 years old (41/57, 71.9%) compared with those 5 years old or above (137/631, 21.7%, p < 0.0001 by chisquare test). Logistic regression modeling indicated that the estimated odds of perforation in patients with appendicitis were more than 9 times higher for children less than 5 years old compared with children 5 years old or above (odds ratio = 9.2, 95% confidence interval 5.0-16.8, p < 0.001).
There is a highly significant inverse relationship between the likelihood of perforation and the age of the patient. The predicted probability of perforation, based on logistic regression modeling, is almost 60% for a 3-year-old, 50% for a 5-year-old, less than 30% for a 10-year-old, and approximately 10% for a 17-year-old. Figure 2 shows the nonlinear curve predicting perforation based on patient age.
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The majority of children in our study (521/769, 68%) were imaged only with CT. Sonography alone was the imaging technique of choice in 106 children (14%), and both CT and sonography were performed in 142 children (18%). There were no differences in use of CT, sonography, or both in combination between both age groups.
Performance Characteristics and Imaging Technique
The overall sensitivity related to imaging technique used for all ages was
as follows: for CT only, 471/482 (97.7%); for sonography only, 86/91 (94.5%);
and for combined sonography and CT studies, 113/115 (98.3%).
Table 3 shows the performance
characteristics for CT and sonography studies by age group. A trend toward
more frequent false-positive imaging results was found in younger children
less than 5 years old (9/67, 13%) (Fig.
3) compared with children 5 years old or above (61/702, 9%).
However this difference only approached statistical significance (p =
0.06).
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Out of a total of 769 studies, 33 (4.3%) were interpreted as indeterminate for appendicitis (Figs. 4A, 4B, and 5). Nineteen children with indeterminate imaging studies had appendicitis (58%), and 14 did not (42%). All indeterminate studies occurred in patients 5 years old or above. Of these, 21 studies (64%) were CT examinations only, 6 (18%) were sonography studies only, and 6 (18%) were combined CT and sonography studies. Indeterminate radiologic interpretations were included in the test performance calculations as positive studies. However, when indeterminate studies were included as negative studies or even excluded from the calculations, there were no significant differences in test performance characteristics (p > 0.5).
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True-positive, true-negative, and false-negative fractions for CT examinations were similar for both groups of children as shown in Table 3. There were more false-positive examinations in the younger group (14%) compared with older children (6.2%). In addition, 4.5% of CT examinations were classified as indeterminate in older children compared with none in the younger group. However, neither of these differences reached statistical significance (p > 0.5).
There were no significant differences in test performance characteristics of the sonography examinations between both age groups. As with CT examinations, there were more indeterminate sonography studies in the older age group. These differences did not reach statistical significance (p > 0.5). Similarly, there were no significant differences in test performance characteristics of combined sonography and CT examinations between both age groups.
Imaging Findings
The frequency and type of imaging findings on CT and sonography are shown
in Tables 4 and
5, respectively. The majority
of imaging findings were similar in both age groups. However, abnormal
enhancement of the appendix and free peritoneal fluid were twice as frequent
in children 5 years old or above compared with younger children (p
< 0.01 for both comparisons, Table
4). Conversely, abscess was four times as common in children less
than 5 years old compared with older children (p < 0.01). On
sonography, the findings of adenopathy and echogenic fat were significantly
more common in children 5 years old or above (p < 0.01 for both
comparisons, Table 5).
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A total of 23 alternative diagnoses were identified. Pathologic diagnoses other than appendicitis were seen more commonly in younger children, 10/67 in children less than 5 years old (15%) compared with 12/702 children 5 years old or above (2%, p < 0.001). In the younger age group, all alternative diagnoses were nonsurgical in nature and included mesenteric adenitis (2), pneumonia (1), constipation (1), and nonspecific abdominal pain (6). In children less than 5 years old, four of the 12 alternative conditions required surgical treatment: individual cases of Meckel's diverticulum, ovarian tumor with torsion, carcinoid tumor of the small intestine, and Crohn's disease of the terminal ileum and appendix. The remaining nonsurgical diagnoses included ovarian cyst (4); mesenteric adenitis (2); and individual cases of ileitis, omental infarction, and torsion of an epiploic appendix.
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In addition, signs and symptoms commonly overlap with those present in other common conditions occurring in this age group, such as viral illnesses, intussusception, gastroenteritis, constipation, and mesenteric adenitis. Often these patients have already been evaluated by a primary care physician and have received treatment before being seen in the emergency department. In this study, the diagnosis of appendicitis was initially missed in four patients less than 5 years old. Each had a confusing and atypical clinical course and required up to three visits to the emergency department before the correct diagnosis was made. As a result of delays in diagnosis, the frequency of appendiceal perforation is higher in younger children [4].
This study confirms this higher risk of perforation in younger children. Our data also show that the risk for perforation appears to be inversely proportional to the age of the patient such that the predicted probability of perforation, based on logistic regression modeling, was almost 60% for a 3-year-old, 50% for a 5-year-old, less than 30% for a 10-year-old, and 10% for a 17-year-old. This higher risk was reflected in the higher frequency of abscesses on both CT and sonography examinations. In addition, echogenic fat on sonography was more commonly seen in younger patients. This finding is thought to be related to edema of the periappendiceal fat and is likely to be due to a higher frequency of transmural inflammation in this group.
Because of the high frequency of appendiceal perforation in younger children, a higher percentage of patients less than 5 years old had an interval appendectomy (13.4%) compared with children 5 years old or above (4.7%). As a result, imaging played an important additional role in this group by mapping the extent of the disease in preparation for planning of imaging-guided abscess treatment.
We found a higher number of false-positive imaging examinations in younger children. Yet, indeterminate studies were not an important clinical problem in this age group. The reasons for these age-related differences remain unclear.
CT was the imaging technique most frequently used, either alone or in combination with sonography for the initial evaluation of children with appendicitis, regardless of patient age. This practice probably relates to the difficulty in excluding early appendicitis by sonography. Lack of visualization of a normal appendix is a known limitation of sonography, and there are large institutional differences. Sivit et al. [18] reported visualization of 49% of normal appendixes using sonography, whereas in our study, a normal appendix could only be shown with sonography in 2% of cases [15]. A recent study by Kaiser et al. [19] shows that the imaging strategy of sonography followed by CT in patients with negative or indeterminate sonography studies had a significantly higher diagnostic accuracy by receiver operating characteristic analysis, compared with sonography alone and clinical evaluation alone.
We were concerned that imaging in younger children would be less accurate for detecting appendicitis than in older children. Our study was reassuring in that the imaging features in younger children are not appreciably different from those in older children. An interesting finding was the lack of indeterminate studies in younger children and the slightly higher frequency of false-positive studies in younger children. We hypothesize that imaging findings in younger children were more likely to be interpreted as definitive because of the higher frequency of more advanced appendicitis and the higher frequency of alternative diagnoses in the younger age group.
The limitations of this study are its retrospective design and a cohort limited to only those children with pathologic proof of appendicitis. Our research design did not allow us to determine the utility of imaging in the larger group of children with suspected appendicitis nor could we determine the relative frequency of young children with suspected appendicitis referred for imaging. We provided specificity values for imaging studies. However, these values can be misleading since they were derived from the small number of false-negative studies performed in the selected patients who underwent a laparotomy.
We conclude that appendicitis should be included in the practical differential diagnosis of young children with abdominal pain and that the imaging findings in this population are the result of a high frequency of appendiceal perforation. More work is needed to develop effective triage mechanisms for better identification of younger patients with appendicitis.
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  J. E. Jacobs CT and Sonography for Suspected Acute Appendicitis: A Commentary. Am. J. Roentgenol., April 1, 2006; 186(4): 1094 - 1096. [Full Text] [PDF]
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