Lin 2017
Lin 2017
Lin et al.
                                                                                                                                                               Reasons for Nonvisualization of Appendix on Graded Compres-
                                                                                                                                                               sion Sonography
                                                                                                                                                               Gastrointestinal Imaging
                                                                                                                                                               Original Research
ompared with CT, graded com- Among these challenges, the location of
                                                                                                                                                                                                                              C
                                                                                                                                                               Received February 6, 2017; accepted after revision
                                                                                                                                                               March 1, 2017.
                                                                                                                                                                                                                                          pression sonography offers sever-    the appendix may be uniquely amenable to in-
                                                                                                                                                               Based on a presentation at the 2016 Radiological Society                   al advantages in the evaluation of   novations in scanning methodology. For ex-
                                                                                                                                                               of North America annual meeting, Chicago, IL.                              patients with suspected appendi-     ample, recent implementation of a three-step
                                                                                                                                                                                                                             citis, including the absence of both ionizing     sequential positioning algorithm significant-
                                                                                                                                                                                                                             radiation and iodine-based contrast media as      ly improved appendiceal visualization and
                                                                                                                                                               1
                                                                                                                                                                 Department of Radiology, Stanford University School of
                                                                                                                                                               Medicine, 300 Pasteur Dr, H1307, Stanford, CA
                                                                                                                                                               94305-5105. Address correspondence to E. W. Olcott
                                                                                                                                                                                                                             well as lower cost [1–5]. However, the lower      decreased the utilization of CT after graded
                                                                                                                                                               (eolcott@stanford.edu).                                       rate of appendiceal visualization on graded       compression sonography [9]. Nonetheless, ap-
                                                                                                                                                                                                                             compression sonography remains an ongoing         pendiceal visualization rates of graded com-
                                                                                                                                                                                                                             challenge [1–10]. Nonvisualization of the ap-     pression sonography remain inferior to those
                                                                                                                                                               2
                                                                                                                                                                 Department of Radiology (114), Veterans Affairs Palo
                                                                                                                                                               Alto Health Care System, Palo Alto, CA.
                                                                                                                                                                                                                             pendix on graded compression sonography           of CT, with the former ranging from 2.4% to
                                                                                                                                                               WEB                                                           may be considered an inconclusive finding         greater than 70% and the latter ranging up to
                                                                                                                                                               This is a web exclusive article.                              and, as such, often leads to CT scanning, with    100% [2, 8, 14–19]. Accordingly, new meth-
                                                                                                                                                                                                                             its attendant radiation exposure, further de-     ods that improve visualization of the appendix
                                                                                                                                                               AJR 2017; 209:W128–W138
                                                                                                                                                                                                                             lays, and additional costs [2, 5, 6, 11]. Known   on sonography potentially can increase the
                                                                                                                                                               0361–803X/17/2093–W128                                        challenges for graded compression sonogra-        utility of graded compression sonography in
                                                                                                                                                                                                                             phy include large body habitus, retrocecal ap-    the evaluation of suspected appendicitis and
                                                                                                                                                               © American Roentgen Ray Society                               pendixes, and bowel gas [6, 9, 12–14].            decrease patients’ exposure to CT.
                                                                                                                                                                                                                                               A
                                                                                                                                                               Fig. 1—24-year-old woman with suspected appendicitis. Images show method
                                                                                                                                                               used for localizing appendixes.
                                                                                                                                                               A, Transverse CT image shows anteroposterior and right-to-left orthogonal
                                                                                                                                                               boundaries (lines) centered on ileocecal valve, defining anterolateral,
                                                                                                                                                               anteromedial, posterolateral, and posteromedial quadrants.
                                                                                                                                                               B, Coronal CT image shows boundary (line) connecting most superior aspects of
                                                                                                                                                               iliac crests, demarcating regions superior and inferior to iliac crests.
                                                                                                                                                                  For many years, graded compression so-              the institutional review board at Stanford Univer-     Additional scanning was performed by radiolo-
                                                                                                                                                               nography has been the first-line imaging mo-           sity School of Medicine, in view of the retrospec-     gists, as needed, for clarification of findings, as is
                                                                                                                                                               dality of choice at our institution for evaluating     tive nature of the investigation.                      typical in our practice. The appendix was identi-
                                                                                                                                                               patients with suspected appendicitis. Sonog-                                                                  fied as a blind-ending tubular structure associated
                                                                                                                                                               raphy is the modality preferred by the Ameri-          Patient Selection                                      with the cecal tip [2, 7, 14, 29, 31]. Final imaging
                                                                                                                                                               can College of Radiology for pediatric patients            An institutional database was searched to iden-    reports were generated by attending radiologists
                                                                                                                                                               [20] and has been proposed for adults in view          tify patients who had undergone graded compres-        with 5 years to more than 25 years of experience.
                                                                                                                                                               of concerns about radiation exposure associat-         sion sonography and CT for suspected appendi-
                                                                                                                                                               ed with CT [1, 8, 11, 21–25]. On the basis of our      citis between mid-October 2012 and mid-March           Graded Compression Sonography
                                                                                                                                                               earlier experience, we elected to investigate po-      2015. Inclusion criteria were as follows: the ini-         Graded compression sonography was per-
                                                                                                                                                               tential anatomic reasons for nonvisualization of       tial imaging examination performed was appen-          formed using Logiq 9 ultrasound equipment
                                                                                                                                                               the appendix and determine whether nonvisu-            diceal graded compression sonography, the ap-          (GE Healthcare). A three-step sequential posi-
                                                                                                                                                               alized appendixes are located in the deep pos-         pendix was not visualized on graded compression        tioning algorithm was used [9]. In this algorithm,
                                                                                                                                                               terior pelvis beyond the cecum or within the           sonography, CT was performed within 48 hours of        when the appendix was not visualized on initial
                                                                                                                                                               abdomen superior to the iliac crests (regions          graded compression sonography and revealed the         traditional scanning performed with the patient in
                                                                                                                                                               not specifically emphasized in our laboratory          appendix, and reference standards were available,      the supine position, the patient was placed in a 45°
                                                                                                                                                               or in much of the literature [7, 11, 26–31], al-       including pathologic evaluation of resected speci-     left posterior oblique position and was scanned
                                                                                                                                                               though they were identified in a previous study        mens for patients treated with appendectomy and        through the right flank to examine the retroce-
                                                                                                                                                               [32]), or are located at depths beyond the range       6-week follow-up for patients who did not undergo      cal region. When the appendix still was not visu-
                                                                                                                                                               of the transducers of at least 10 MHz that are         surgery. A total of 197 patients met these criteria.   alized, the patient was returned to the supine po-
                                                                                                                                                               typically used in our laboratory. We sought to                                                                sition to undergo a second-look evaluation. We
                                                                                                                                                               evaluate these possibilities by evaluating pa-         Scanning Technique                                     typically use linear array transducers of at least
                                                                                                                                                               tients who underwent CT soon after appendi-               All imaging studies were performed by li-           10 MHz for appendiceal studies performed in our
                                                                                                                                                               ceal graded compression sonography failed to           censed CT technologists and one of six licensed        laboratory. By agreement with our emergency
                                                                                                                                                               visualize the appendix.                                sonographers with at least 5 years of clinical expe-   medicine and surgery departments, patients with
                                                                                                                                                                                                                      rience in graded compression sonography. These         a body mass index (weight in kilograms divided
                                                                                                                                                               Materials and Methods                                  technologists and sonographers were supervised         by the square of height in meters) of 30 or more,
                                                                                                                                                                 This study was HIPAA compliant. The require-         by attending radiologists, fellows, and residents in   or with peritoneal signs, were evaluated with CT
                                                                                                                                                               ment to obtain informed consent was waived by          our body imaging and pediatric imaging sections.       rather than sonography.
                                                                                                                                                               nipaque 350, GE Healthcare) injected at a rate of 3       provides a recognizable and essential landmark for         vide the pelvis from the abdomen [32, 33] (Fig. 1).
                                                                                                                                                               mL/s. Pediatric patients received 2 mL of contrast        identifying the appendix [2, 7, 14, 29, 31] and is a       Appendiceal tips lying on boundary lines were lo-
                                                                                                                                                               medium per kilogram of body weight, which was             unique point in space that is identifiable on both         calized using the immediately adjacent portion of
                                                                                                                                                               injected at a rate of 2 mL/s. Portal venous phase         sonography and CT. Each tip was localized in the           the appendix. Finally, appendiceal depth was de-
                                                                                                                                                               images of the abdomen and pelvis were recon-              transverse plane to one of four quadrants demarcat-        fined on axial images, with the use of the shortest
                                                                                                                                                               structed at a slice thickness of 1.25–5 mm with           ed by straight lines centered on the ileocecal valve,      distance from the tip to the skin surface without in-
                                                                                                                                                               sagittal and coronal reformations obtained at a           extending anteroposteriorly and from right to left         tervening osseous structures, reflecting the closest-
                                                                                                                                                               slice thickness of 2 mm.                                  and projected vertically, including the anterolater-       approach application of a sonographic transducer.
A B
                                                                                                                                                                                                                                                C                                                                                      D
                                                                                                                                                               Fig. 2—Appendiceal tips localized to each of four transverse quadrants in four patients. Boundaries (lines) centered on ileocecal valve, projected vertically, define
                                                                                                                                                               quadrants.
                                                                                                                                                               A, 63-year-old woman with suspected appendicitis. CT image shows appendiceal tip (arrow) in anterolateral quadrant.
                                                                                                                                                               B, 24-year-old woman with suspected appendicitis. CT image shows appendiceal tip (arrow) in anteromedial quadrant.
                                                                                                                                                               C, 37-year-old man with suspected appendicitis. CT image shows appendiceal tip (arrow) in posterolateral quadrant.
                                                                                                                                                               D, 85-year-old man with suspected appendicitis. CT image shows appendiceal tip (arrow) in posteromedial quadrant.
                                                                                                                                                               TABLE 1:  Sonographically Nonvisualized Appendixes, Stratified by Quadrant Where Appendix Was Located, Patient
                                                                                                                                                                         Group, and Level of Appendix Relative to Iliac Crests
                                                                                                                                                                                                                                                  Location of Appendix                                                   pa
                                                                                                                                                                    Patient Group, and Level of Appendix              Anterolateral       Anteromedial         Posterolateral        Posteromedial       By Multinomial         By Fisher
                                                                                                                                                                           Relative to Iliac Crests                    Quadrant            Quadrant              Quadrant              Quadrant              Testb             Exact Testc
Downloaded from www.ajronline.org by Cochin-Port Royal on 08/23/17 from IP address 193.51.85.197. Copyright ARRS. For personal use only; all rights reserved
                                                                                                                                                               All levels
                                                                                                                                                                All patients (n = 197)
                                                                                                                                                                 No. of patients                                            13                   18                   43                   123               < 0.0001
                                                                                                                                                                 Percentage of patients (95% CI)                      6.6 (3.6–11.0)       9.1 (5.5–14.1)      21.8 (16.3–28.3)     62.4 (55.3–69.2)
                                                                                                                                                                                                                                                                                      p < 0.00001d
                                                                                                                                                                Patients with appendicitis (n = 31)
                                                                                                                                                                 No. of patients                                             2                   3                    11                    15                0.0015
                                                                                                                                                                 Percentage of patients (95% CI)                      6.5 (0.8–21.4)       9.7 (2.0–25.8)      35.5 (19.2–54.6)     48.4 (30.2–66.9)
                                                                                                                                                                                                                                                                                       p = 0.0056d
                                                                                                                                                                Patients without appendicitis (n = 166)
                                                                                                                                                                 No. of patients                                            11                   15                   32                   108               < 0.0001                 0.21
                                                                                                                                                                 Percentage of patients (95% CI)                      6.6 (3.4–11.5)       9.0 (5.1–14.5)      19.3 (13.6–26.1)     65.1 (57.3–72.3)
                                                                                                                                                                                                                                                                                      p < 0.00001d
                                                                                                                                                               Level superior to iliac crests
                                                                                                                                                                All patients (n = 39)
                                                                                                                                                                 No. of patients                                            11                   10                    5                    13                 0.32
                                                                                                                                                                 Percentage of patients (95% CI)                     28.2 (15.0–44.9)    25.6 (13.0–42.1)       12.8 (4.3–27.4)     33.3 (19.1–50.2)
                                                                                                                                                                                                                                                                                        p = 0.27d
                                                                                                                                                                Patients with appendicitis (n = 6)
                                                                                                                                                                 No. of patients                                             2                   2                     2                    0                   0.74
                                                                                                                                                                 Percentage of patients (95% CI)                      33.3 (4.3–77.7)     33.3 (4.3–77.7)       33.3 (4.3–77.7)       0.0 (0.0–45.9)
                                                                                                                                                                                                                                                                                        p = 0.35d
                                                                                                                                                                Patients without appendicitis (n = 33)
                                                                                                                                                                 No. of patients                                             9                   8                     3                    13                  0.10                  0.11
                                                                                                                                                                 Percentage of patients (95% CI)                     27.3 (13.3–45.5)    24.2 (11.1–42.3)       9.1 (1.9–24.3)      39.4 (22.9–57.9)
                                                                                                                                                                                                                                                                                        p = 0.069d
                                                                                                                                                               Level inferior to iliac crests
                                                                                                                                                                All patients (n = 158)
                                                                                                                                                                 No. of patients                                             2                   8                    38                   110               < 0.0001
                                                                                                                                                                 Percentage of patients (95% CI)                       1.3 (0.2–4.5)       5.1 (2.2–9.7)       24.1 (17.6–31.5)     69.6 (61.8–76.7)
                                                                                                                                                                                                                                                                                       p < 0.0001d
                                                                                                                                                                Patients with appendicitis (n = 25)
                                                                                                                                                                 No. of patients                                             0                   1                     9                    15               < 0.0001
                                                                                                                                                                 Percentage of patients (95% CI)                      0.0 (0.0–13.7)       4.0 (0.1–20.4)      36.0 (18.0–57.5)      60.0 (38.7–78.9)
                                                                                                                                                                                                                                                                                      p = 0.00021d
                                                                                                                                                                Patients without appendicitis (n = 133)
                                                                                                                                                                 No. of patients                                             2                   7                    29                    95               < 0.0001                 0.48
                                                                                                                                                                 Percentage of patients (95% CI)                       1.5 (0.2–5.3)       5.3 (2.1–10.5)      21.8 (15.1–29.8)     71.4 (63.0–78.9)
                                                                                                                                                                                                                                                                                      p < 0.00001d
                                                                                                                                                               Note—Please note that percentages may not total 100% because of rounding.
                                                                                                                                                               a All p values other than inequalities are presented to two significant digits after the decimal.
                                                                                                                                                               bMultinomial test with exhaustive enumeration was used to evaluate overall frequencies of appendixes in four quadrants across each row.
                                                                                                                                                               cThe Fisher exact test is a 2 × 4 comparison of the distribution of appendixes in four quadrants in patients with appendicitis versus patients without appendicitis.
                                                                                                                                                               d The null hypothesis is 25.0% distribution in each of the four quadrants.
                                                                                                                                                                                                                          regression relating
                                                                                                                                                               patients (20 male patients and 20 female patients)         measurements of two                                                40
                                                                                                                                                               chosen from among the 197 patients by use of sta-          modalities. Circles
                                                                                                                                                               tistical software (Stata, version 14.1, StataCorp), the    denote individual
                                                                                                                                                                                                                          patients, dashed line                                              20
                                                                                                                                                               distance from the anterior skin surface to a recog-        denotes regression
                                                                                                                                                               nizable deep point along the right external iliac ar-      line, and area outlined
                                                                                                                                                               tery was measured for each patient in side-by-side         by black line denotes
                                                                                                                                                                                                                          95% CI.                                                                  0
                                                                                                                                                               evaluations of both modalities performed by one re-
                                                                                                                                                                                                                                                                                                       20               40               60             80          100
                                                                                                                                                               viewer, with the conformation of the vessel as well                                                                                                 Right External Iliac Artery Depth on CT (mm)
                                                                                                                                                               as the adjacent boney and muscular features used as
                                                                                                                                                               landmarks. Regression analysis was used to evaluate        who recorded demographic information for each                                                  Results
                                                                                                                                                               relationships of appendiceal depth on graded com-          patient. Final pathology reports following surgery                                                The 197 patients who met the inclusion
                                                                                                                                                               pression sonography to depth on CT, producing the          for patients who underwent appendectomy, and                                                   criteria included 42 male patients (age, 3–65
                                                                                                                                                               equation Y = mX + b, where Y denotes depth on grad-        6-week postpresentation chart reviews for patients                                             years; mean, 21.9 years) and 155 female pa-
                                                                                                                                                               ed compression sonography, m denotes slope, X de-          who did not undergo surgery, were used as diag-                                                tients (age, 2–74 years; mean, 27.0 years).
                                                                                                                                                               notes depth on CT, and b denotes the y-intercept. Re-      nostic reference standards to establish the pres-                                              Of these patients, 13 male patients (31.0%;
                                                                                                                                                               gression analysis was also applied to sex, age, and        ence or absence of appendicitis.                                                               95% CI, 17.6–47.1%) and 18 female patients
                                                                                                                                                               diagnosis as revealed in the medical record.                                                                                                              (11.6%; 95% CI, 7.0–77.7%) underwent ap-
                                                                                                                                                                                                                          Statistical Analysis                                                                           pendectomy and had appendicitis as defined
                                                                                                                                                               Appendiceal Depth on Graded Compression                       Statistical analysis was performed using Stata                                              by the pathologic reference standard. All pa-
                                                                                                                                                               Sonography and Transducer Penetration                      software, utilizing the exact binomial distribution                                            tients who underwent appendectomy had ap-
                                                                                                                                                                  Using the relationship that transducer penetra-         to evaluate 95% CIs of proportions and appendi-                                                pendicitis according to this reference stan-
                                                                                                                                                               tion in centimeters equals approximately 60 divided        ceal frequencies in individual quadrants, the mul-                                             dard, and no patients who were managed
                                                                                                                                                               by the frequency in megahertz [34], the regression         tinomial exact test with exhaustive enumeration to                                             without surgery presented with appendicitis
                                                                                                                                                               model was solved for the CT depth measurement              compare overall four-quadrant distributions with-                                              during follow-up.
                                                                                                                                                               corresponding to the lowest-frequency penetration          in single groups, the 2 × 4 Fisher exact test to com-
                                                                                                                                                               of our typical transducers of at least 10 MHz. Pa-         pare four-quadrant distributions between groups,                                               Distribution of Appendixes Among Quadrants
                                                                                                                                                               tients whose appendiceal depths exceeded this val-         one-way ANOVA with the Bonferroni method                                                          As shown in Table 1, the distribution of
                                                                                                                                                               ue were then identified. Similar computations were         to adjust for multiple comparisons and a t test to                                             appendixes among the four quadrants was
                                                                                                                                                               performed for 6-MHz transducers.                           compare depth measurements, and linear regres-                                                 statistically significantly nonuniform in the
                                                                                                                                                                                                                          sion to relate depth measurements between graded                                               entire sample of 197 patients (p < 0.0001)
                                                                                                                                                               Review of Medical Records                                  compression sonography and CT. Results with p <                                                as well as in the 31 patients with appendi-
                                                                                                                                                                  Electronic medical records were reviewed by             0.05, including those indicated by nonoverlapping                                              citis (p = 0.0015) and the 166 patients with-
                                                                                                                                                               an individual not otherwise involved in the study          95% CIs, were considered significant.                                                          out appendicitis (p  < 0.0001). A significant
                                                                                                                                                                                                                                                                                                                         majority lay in the posteromedial quadrant
                                                                                                                                                                                                                                                                                                                         among all patients and those without appen-
                                                                                                                                                               TABLE 2:  Appendixes Not Visualized by Sonography, Stratified by Patient
                                                                                                                                                                         Group and Level of Appendix Relative to Iliac Crests                                                                                            dicitis (with nonoverlapping 95% CIs be-
                                                                                                                                                                                                                                                                                                                         tween the posteromedial quadrant and each
                                                                                                                                                                             Patient Group                   Superior to Iliac Crests   Inferior to Iliac Crests                                            pa           of the other quadrants) and a nonsignificant
                                                                                                                                                                All patients (n = 197)                                                                                                                                   majority was present in the posteromedi-
                                                                                                                                                                                                                                                                                                                         al quadrant of patients with appendicitis. In
                                                                                                                                                                 No. of patients                                         39                         158
                                                                                                                                                                                                                                                                                                                         all three patient groups (all patients, patients
                                                                                                                                                                 Percentage of patients (95% CI)                 19.8 (14.5–26.1)           80.2 (73.9–85.5)                                                             with appendicitis, and patients without ap-
                                                                                                                                                                Patients with appendicitis (n = 31)                                                                                                                      pendicitis), appendixes were significantly
                                                                                                                                                                 No. of patients                                         6                          25                                                                   more frequently located in the posteromedial
                                                                                                                                                                                                                                                                                                                         quadrant compared with the 25.0% rate ex-
                                                                                                                                                                 Percentage of patients (95% CI)                  19.4 (7.5–37.5)           80.6 (62.5–92.5)
                                                                                                                                                                                                                                                                                                                         pected by chance (p < 0.00001, p = 0.0056,
                                                                                                                                                                Patients without appendicitis (n = 166)                                                                                                                  and p < 0.00001, respectively); the null hy-
                                                                                                                                                                 No. of patients                                         33                         133                                                     1.00         pothesis was that appendixes are distributed
                                                                                                                                                                 Percentage of patients (95% CI)                 19.9 (14.1–26.8)           80.1 (73.2–85.9)                                                             equally among the four quadrants. Overall
                                                                                                                                                                aBy                                                                                                                                                      four-quadrant distributions between patients
                                                                                                                                                                    Fisher exact test (a 2 × 2 comparison of the presence or absence of appendicitis with the location of
                                                                                                                                                                 the appendix superior or inferior to the iliac crests). The p value is presented to two significant digits                                              with and without appendicitis did not differ
                                                                                                                                                                 after the decimal.                                                                                                                                      significantly (p = 0.21).
                                                                                                                                                               TABLE 3:  Depths of Appendixes Not Visualized by Sonography, Stratified by Patient Group and Quadrant Where
                                                                                                                                                                         Appendix Was Located
                                                                                                                                                                                                                                                       Location of Appendix
                                                                                                                                                                                                                                   Anterolateral          Anteromedial           Posterolateral          Posteromedial
                                                                                                                                                                             Patient Group                 All Quadrants            Quadrant               Quadrant                Quadrant                Quadrant                  pa
Downloaded from www.ajronline.org by Cochin-Port Royal on 08/23/17 from IP address 193.51.85.197. Copyright ARRS. For personal use only; all rights reserved
                                                                                                                                                               Level of Appendixes Relative to Iliac Crests                four quadrants was statistically significantly             teromedial quadrant frequency that exceed-
                                                                                                                                                                  As shown in Table 2, a statistically significant         nonuniform for all three patient groups (p <               ed the 25.0% rate expected by chance. Over-
                                                                                                                                                               majority of appendixes were located inferior to             0.0001, for each). For each patient group, most            all four-quadrant distributions between patients
                                                                                                                                                               the iliac crests among all patients, patients with          appendixes found below the iliac crests were               with appendicitis and patients without appen-
                                                                                                                                                               appendicitis, and patients without appendicitis,            located within the posteromedial quadrant,                 dicitis did not differ significantly whether the
                                                                                                                                                               as indicated by the nonoverlapping 95% CIs                  at a frequency that significantly exceeded the             appendix was found above (p = 0.11) or below
                                                                                                                                                               between appendixes superior and appendixes                  25.0% frequency expected by chance (for all                (p = 0.48) the iliac crests.
                                                                                                                                                               inferior to the iliac crests for each of these three        patients, p < 0.00001; for patients with appen-
                                                                                                                                                               patient groups. In addition, the presence or ab-            dicitis, p = 0.00021; and for patients without ap-         Depth of Appendixes on CT
                                                                                                                                                               sence of appendicitis was not associated with               pendicitis, p < 0.00001). Above the iliac crests,             Appendiceal depth on CT ranged from 7
                                                                                                                                                               location of the appendix superior or inferior to            however, relatively few appendixes were pres-              to 163 mm (mean, 78.9 mm) among the 197
                                                                                                                                                               the iliac crests (p = 1.00).                                ent and none of the three patient groups exhib-            patients, and it did not differ significantly be-
                                                                                                                                                                  As shown in Table 1, the distribution of ap-             ited significant four-quadrant nonuniformity, a            tween patients with appendicitis and patients
                                                                                                                                                               pendixes below the iliac crests among the                   majority in the posteromedial quadrant, or pos-            without appendicitis (p = 0.45) (Table 3).
                                                                                                                                                                                                                                                   A                                                                                       B
                                                                                                                                                               Fig. 4—38-year-old woman with appendicitis who was not included in sample of 197 patients. Sonographic images show value of sonography performed with 6-MHz
                                                                                                                                                               transducer after nonvisualization of appendix on sonography performed with 10-MHz transducer.
                                                                                                                                                               A, Initial gray-scale sonographic image obtained at 10 MHz shows no appendix within posteromedial quadrant.
                                                                                                                                                               B, Color Doppler image obtained at 6 MHz after image shown in A shows appendix (arrow) and vessels in posteromedial quadrant.
                                                                                                                                                                                                                                                                                                   (Fig. 4 continues on next page)
                                                                                                                                                                                                                                                              sonography performed
                                                                                                                                                                                                                                                              with 6-MHz transducer         calculations. Linear regression of depth on
                                                                                                                                                                                                                                                              after nonvisualization of     graded compression sonography as a function
                                                                                                                                                                                                                                                              appendix on sonography
                                                                                                                                                                                                                                                              performed with 10-MHz
                                                                                                                                                                                                                                                                                            of depth on CT yielded a slope of 0.61 (95%
                                                                                                                                                                                                                                                              transducer.                   CI, 0.48–0.73), a y-intercept of −3.03 mm, p <
                                                                                                                                                                                                                                                              C, Gray-scale ultrasound      0.001, and R2 = 0.71 (Fig. 3).
                                                                                                                                                                                                                                                              image obtained at 6 MHz
                                                                                                                                                                                                                                                              permits measurement of
                                                                                                                                                                                                                                                              enlarged 9-mm appendix        Appendiceal Depth on Graded Compression
                                                                                                                                                                                                                                                              (between calipers) in         Sonography Versus Transducer Penetration
                                                                                                                                                                                                                                                              posteromedial quadrant.          Using the relationship between transducer
                                                                                                                                                                                                                                                                                            penetration and frequency reported by Sza-
                                                                                                                                                                                                                                                                                            bo and Lewin [34], transducers of at least
                                                                                                                                                                                                                                                       C
                                                                                                                                                                                                                                                                                            10 MHz, such as those typically used in our
                                                                                                                                                                  As evaluated with ANOVA (Table 3), all                    (p = 1.00, for each pairwise combination). Ap-                  laboratory, would penetrate to a maximum
                                                                                                                                                               patients and patients without appendicitis had               pendiceal depth in the posteromedial quadrant                   depth of 60 mm. Substituting this value into
                                                                                                                                                               significant nonuniformity in mean appen-                     did not differ significantly between patients                   the linear regression model yielded an equiv-
                                                                                                                                                               diceal depth among the four quadrants (p =                   with appendicitis and patients without appen-                   alent CT depth of 103 mm.
                                                                                                                                                               0.0034 and p = 0.0032, respectively); these                  dicitis (p = 0.19) (Table 3).                                      Appendiceal depths on CT exceeded 103 mm
                                                                                                                                                               findings reflected significant pairwise differ-                                                                              in 38 of the 197 patients (19.3%; 95% CI, 14.0–
                                                                                                                                                               ences between the posteromedial quadrant and                 Relationship Between Depth Measurements                         25.5%). As shown in Table 4, the distribution of
                                                                                                                                                               the anterolateral quadrant (and only between                 on Graded Compression Sonography and CT                         appendixes with a depth exceeding 103 mm was
                                                                                                                                                               the posteromedial quadrant and anterolater-                     In linear regression analysis of the subset                  statistically significantly nonuniform among the
                                                                                                                                                               al quadrant) for these two patient groups (p =               of 40 randomly selected patients, depth mea-                    four quadrants for all patients and for patients
                                                                                                                                                               0.0070 and p = 0.0090, respectively). Patients               surements on CT correlated significantly with                   without appendicitis (p < 0.0001 for both pa-
                                                                                                                                                               with appendicitis exhibited neither significant              depth measurements on graded compression                        tient groups), with the posteromedial quadrant
                                                                                                                                                               nonuniformity among the four quadrants by                    sonography in both univariate (p < 0.001) and                   accounting for a statistically significant majority
                                                                                                                                                               ANOVA (p = 0.65) (Table 3) nor significant                   multivariate analysis (p < 0.001). Sex, age, and                of appendixes in both patient groups (with non-
                                                                                                                                                               pairwise differences among the four quadrants                diagnosis did not correlate significantly with                  overlapping 95% CIs between the posteromedi-
                                                                                                                                                               TABLE 4:  Appendixes Not Visualized by Sonography and Located at Depths Exceeding the Penetration of Transducers
                                                                                                                                                                         of at Least 10 MHz, Stratified by Patient Group and Quadrant Where Appendix Was Located
                                                                                                                                                                                                                                                       Location of Appendix                                                 pa
                                                                                                                                                                                                                       Anterolateral         Anteromedial          Posterolateral         Posteromedial       By Multinomial      By Fisher
                                                                                                                                                                                   Patient Group                        Quadrant              Quadrant               Quadrant               Quadrant              Testb          Exact Testc
                                                                                                                                                                All patients (n = 38)
                                                                                                                                                                 No. of patients                                              0                    4                      7                     27               < 0.0001
                                                                                                                                                                 Percentage of patients (95% CI)                         0 (0.0–9.3)         10.5 (2.9–24.8)        18.4 (7.7–34.3)       71.1 (54.1–84.6)
                                                                                                                                                                                                                                                                                           p < 0.00001d
                                                                                                                                                                Patients with appendicitis (n = 5)
                                                                                                                                                                 No. of patients                                              0                    0                      3                      2                 0.18
                                                                                                                                                                 Percentage of patients (95% CI)                       0.0 (0.0–52.2)        0.0 (0.0–52.2)       60.0 (14.7–94.7)        40.0 (5.3–85.3)
                                                                                                                                                                                                                                                                                             p = 0.60d
                                                                                                                                                                Patients with appendicitis (n = 33)
                                                                                                                                                                 No. of patients                                              0                    4                      4                     25               < 0.0001           0.046
                                                                                                                                                                 Percentage of patients (95% CI)                        0.0 (0.0–10.6)       12.1 (3.4–28.2)       12.1 (3.4–28.2)        75.8 (57.7–88.9)
                                                                                                                                                                                                                                                                                           p < 0.00001d
                                                                                                                                                                a All p values other than inequalities are presented to two significant digits after the decimal.
                                                                                                                                                                bMultinomial test with exhaustive enumeration was used to evaluate overall frequencies of appendixes in four quadrants across each row.
                                                                                                                                                                cThe Fisher exact test is a 2 × 4 comparison of the distribution of appendixes in four quadrants in patients with appendicitis versus patients without appendicitis.
                                                                                                                                                                d The null hypothesis is 25.0% distribution in each of the four quadrants.
                                                                                                                                                                                                                                             A                                                                                 B
                                                                                                                                                               Fig. 6—27-year-old woman with appendicitis who was not included in sample of 197 patients. Sonographic images show value of scanning above iliac crests after
                                                                                                                                                               nonvisualization of appendix below iliac crests.
                                                                                                                                                               A, Initial transverse gray-scale sonographic image shows iliac artery and vein (arrows) but no appendix in region below iliac crests.
                                                                                                                                                               B, Transverse gray-scale sonogram obtained after image in A shows appendix (arrows) adjacent to psoas muscle in region above iliac crests.
                                                                                                                                                               ures 6 and 7 show the value of scanning above       corroborate these findings and to evaluate                      role of abdominal wall thickness and appendiceal
                                                                                                                                                               the iliac crests when the appendix is not visu-     the costs and benefits of the maneuvers sug-                    location. Emerg Radiol 2011; 18:525–531
                                                                                                                                                               alized in a typical pelvic position.                gested for addressing them.                                	15.	Lane MJ, Katz DS, Ross BA, Clautice-Engle TL,
                                                                                                                                                                   Several limitations deserve mention. We                                                                         Mindelzun RE, Jeffrey RB Jr. Unenhanced helical
                                                                                                                                                               used the appendiceal tip to localize the ap-        References                                                      CT for suspected acute appendicitis. AJR 1997;
                                                                                                                                                               pendix because the tip must be seen to confi-       	 1.	Doria AS, Moineddin R, Kellenberger CJ, et al.             168:405–409
Downloaded from www.ajronline.org by Cochin-Port Royal on 08/23/17 from IP address 193.51.85.197. Copyright ARRS. For personal use only; all rights reserved
                                                                                                                                                               dently identify the appendix as a blind-ending           US or CT for diagnosis of appendicitis in children    	16.	Lane MJ, Liu DM, Huynh MD, Jeffrey RB Jr,
                                                                                                                                                               structure [2, 7, 14, 29, 31] and because the tip         and adults? A meta-analysis. Radiology 2006;               Mindelzun RE, Katz DS. Suspected acute appen-
                                                                                                                                                               constitutes a unique point in space. We chose            241:83–94                                                  dicitis: nonenhanced helical CT in 300 consecu-
                                                                                                                                                               to permit a 48-hour period between graded           	 2.	Hernanz-Schulman M. CT and US in the diagno-               tive patients. Radiology 1999; 213:341–346
                                                                                                                                                               compression sonography and CT, to include                sis of appendicitis: an argument for CT. Radiology    	17.	Rao PM, Rhea JT, Novelline RA, et al. Helical CT
                                                                                                                                                               patients with more straightforward and less              2010; 255:3–7                                              technique for the diagnosis of appendicitis: pro-
                                                                                                                                                               straightforward clinical courses, as has been       	 3.	Kaiser S, Frenckner B, Jorulf HK. Suspected ap-            spective evaluation of a focused appendix CT ex-
                                                                                                                                                               done in previous studies [19, 30, 39]; other pe-         pendicitis in children: US and CT—a prospective            amination. Radiology 1997; 202:139–144
                                                                                                                                                               riods could have been chosen. This is a sin-             randomized study. Radiology 2002; 223:633–638         	18.	Rao PM, Rhea JT, Novelline RA, Mostafavi AA,
                                                                                                                                                               gle-institution, retrospective study; therefore,    	 4.	Sivit CJ, Applegate KE, Stallion A, et al. Imaging         Lawrason JN, McCabe CJ. Helical CT combined
                                                                                                                                                               it is possible that patients could have present-         evaluation of suspected appendicitis in a pediatric        with contrast material administered only through
                                                                                                                                                               ed elsewhere with recurrent symptoms with-               population: effectiveness of sonography versus             the colon for imaging of suspected appendicitis.
                                                                                                                                                               out our being able to tabulate these individu-           CT. AJR 2000; 175:977–980                                  AJR 1997; 169:1275–1280
                                                                                                                                                               als. The sample in this study was not adequate      	 5.	Strouse PJ. Pediatric appendicitis: an argument       	19.	Shah BR, Stewart J, Jeffrey RB, Olcott EW. Value
                                                                                                                                                               to permit meaningful stratification by sex and           for US. Radiology 2010; 255:8–13                           of short-interval computed tomography when so-
                                                                                                                                                               age, characteristics that will await later inves-   	 6.	Ung C, Chang ST, Jeffrey RB, Patel BN, Olcott              nography fails to visualize the appendix and
                                                                                                                                                               tigation. Our evaluation of transducer penetra-          EW. Sonography of the normal appendix: its var-            shows otherwise normal findings. J Ultrasound
                                                                                                                                                               tion uses a relationship between frequency and           ied appearance and techniques to improve its vi-           Med 2014; 33:1589–1595 [Erratum in J Ultra-
                                                                                                                                                               penetration that is likely approximate [34], and         sualization. Ultrasound Q 2013; 29:333–341                 sound Med 2014; 33:1589]
                                                                                                                                                               we thus consider our depth analysis helpful yet     	 7.	Stewart JK, Olcott EW, Jeffrey RB. Sonography         	20.	Smith MP, Katz DS, Lalani T, et al. ACR Appro-
                                                                                                                                                               approximate. Also, a variety of factors can af-          for appendicitis: nonvisualization of the appendix         priateness Criteria® right lower quadrant pain–
                                                                                                                                                               fect appendiceal sonography, in addition to the          is an indication for active clinical observation           suspected appendicitis. Ultrasound Q 2015;
                                                                                                                                                               factors that we specifically address. Scanning           rather than direct referral for computed tomogra-          31:85–91
                                                                                                                                                               at 6 MHz provides greater penetration than               phy. J Clin Ultrasound 2012; 40:455–461               	21.	Poortman P, Oostvogel HJM, Bosma E, et al. Im-
                                                                                                                                                               does scanning at at least 10 MHz, although          	 8.	Mostbeck G, Adam EJ, Nielsen MB, et al. How to             proving diagnosis of acute appendicitis: results of
                                                                                                                                                               penetration may be limited by increased num-             diagnose acute appendicitis: ultrasound first. In-         a diagnostic pathway with standard use of ultraso-
                                                                                                                                                               bers of intervening bowel loops, bowel gas, and          sights Imaging 2016; 7:255–263                             nography followed by selective use of CT. J Am
                                                                                                                                                               decreased spatial resolution. At our institution,   	 9.	Chang ST, Jeffrey RB, Olcott EW. Three-step se-            Coll Surg 2009; 208:434–441
                                                                                                                                                               clinical decisions regarding management and              quential positioning algorithm during sonograph-      	22.	Hall EJ, Brenner DJ. Cancer risks from diagnostic
                                                                                                                                                               referral for imaging are made by clinical col-           ic evaluation for appendicitis increases appendi-          radiology. Br J Radiol 2008; 81:362–378
                                                                                                                                                               leagues; different decisions could have been             ceal visualization rate and reduces CT use. AJR       	23.	Brown MA. Imaging acute appendicitis. Semin
                                                                                                                                                               made at other institutions. Finally, we did not          2014; 203:1006–1012                                        Ultrasound CT MR 2008; 29:293–307
                                                                                                                                                               address the additional costs of the maneuvers       	10.	Terasawa T, Blackmore CC, Bent S, Kohlwes RJ.         	24.	Brenner DJ, Hall EJ. Computed tomography: an
                                                                                                                                                               that we suggest for use when the appendix is             Systematic review: computed tomography and ul-             increasing source of radiation exposure. N Engl J
                                                                                                                                                               not initially visualized.                                trasonography to detect acute appendicitis in              Med 2007; 357:2277–2284
                                                                                                                                                                   In conclusion, appendixes not visualized             adults and adolescents. Ann Intern Med 2004;          	25.	Nielsen JW, Boomer L, Kurtovic K, et al. Reduc-
                                                                                                                                                               on graded compression sonography are lo-                 141:537–546                                                ing computed tomography scans for appendicitis
                                                                                                                                                               cated in the posteromedial quadrant in a sta-       	11.	Krishnamoorthi R, Ramarajan N, Wang NE, et al.             by introduction of a standardized and validated
                                                                                                                                                               tistically significant majority of patients, are         Effectiveness of a staged US and CT protocol for           ultrasonography report template. J Pediatr Surg
                                                                                                                                                               superior to the iliac crests in nearly 20% of            the diagnosis of pediatric appendicitis: reducing          2015; 50:144–148
                                                                                                                                                               patients, and are located at depths exceeding            radiation exposure in the age of ALARA. Radiol-       	26.	Trout AT, Towbin AJ, Fierke SR, Zhang B, Larson
                                                                                                                                                               the range of transducers of at least 10 MHz              ogy 2011; 259:231–239                                      DB. Appendiceal diameter as a predictor of ap-
                                                                                                                                                               in 19.3% of patients. Accordingly, more in-         	12.	Hörmann M, Scharitzer M, Stadler A, Pokieser P,            pendicitis in children: improved diagnosis with
                                                                                                                                                               tensive scanning of the posteromedial quad-              Puig S, Helbich T. Ultrasound of the appendix in           three diagnostic categories derived from a logistic
                                                                                                                                                               rant and the region above the iliac crests, and          children: is the child too obese? Eur Radiol 2003;         predictive model. Eur Radiol 2015; 25:2231–2238
                                                                                                                                                               with lower frequency (e.g., 6 MHz) transduc-             13:1428–1431                                          	27.	Jeffrey RB Jr, Laing FC, Townsend RR. Acute ap-
                                                                                                                                                               ers, may reveal appendixes that are other-          	13.	Josephson T, Styrud J, Eriksson S. Ultrasonogra-           pendicitis: sonographic criteria based on 250 cas-
                                                                                                                                                               wise nonvisualized on graded compression                 phy in acute appendicitis: body mass index as se-          es. Radiology 1988; 167:327–329
                                                                                                                                                               sonography, potentially leading to improved              lection factor for US examination. Acta Radiol        	28.	Puylaert JB. Acute appendicitis: US evaluation us-
                                                                                                                                                               diagnosis by graded compression sonogra-                 2000; 41:486–488                                           ing graded compression. Radiology 1986;
                                                                                                                                                               phy and correspondingly less exposure to            	14.	Butler M, Servaes S, Srinivasan A, Edgar JC, Del           158:355–360
                                                                                                                                                               CT. Prospective studies will be needed to                Pozo G, Darge K. US depiction of the appendix:        	29.	Goldin AB, Khanna P, Thapa M, McBroom JA,
                                                                                                                                                                    Garrison MM, Parisi MT. Revised ultrasound cri-             in children. Pediatr Radiol 2006; 36:1171–1176        	37.	Chan L, Shin LK, Pai RK, Jeffrey RB. Pathologic
                                                                                                                                                                    teria for appendicitis in children improve diagnos-    	33.	Baldisserotto M, Marchiori E. Accuracy of non-             continuum of acute appendicitis: sonographic
                                                                                                                                                                    tic accuracy. Pediatr Radiol 2011; 41:993–999               compressive sonography of children with appen-             findings and clinical management implications.
                                                                                                                                                                    PubMed                                                      dicitis according to the potential positions of the        Ultrasound Q 2011; 27:71–79
                                                                                                                                                               	30.	Xu Y, Jeffrey RB, Shin LK, DiMaio MA, Olcott                appendix. AJR 2000; 175:1387–1392                     	38.	Prendergast PM, Poonai N, Lynch T, McKillop S,
                                                                                                                                                                    EW. Color Doppler imaging of the appendix: cri-        	34.	Szabo TL, Lewin PA. Ultrasound transducer se-              Lim R. Acute appendicitis: investigating an opti-
Downloaded from www.ajronline.org by Cochin-Port Royal on 08/23/17 from IP address 193.51.85.197. Copyright ARRS. For personal use only; all rights reserved
                                                                                                                                                                    teria to improve specificity for appendicitis in the        lection in clinical imaging practice. J Ultrasound         mal outer appendiceal diameter cut-point in a
                                                                                                                                                                    borderline-size appendix. J Ultrasound Med                  Med 2013; 32:573–582                                       pediatric population. J Emerg Med 2014; 46:157–
                                                                                                                                                                    2016; 35:2129–2138                                     	35.	de Souza S, da Costa S, de Souza I. Vermiform              164
                                                                                                                                                               	31.	Baldisserotto M, Peletti AB. Is colour Doppler so-          appendix: positions and length—a study of 377         	39.	Jones RP, Jeffrey RB, Shah BR, Desser TS,
                                                                                                                                                                    nography a good method to differentiate normal              cases and literature review. J Coloproctology              Rosenberg J, Olcott EW. Journal Club: the Alvara-
                                                                                                                                                                    and abnormal appendices in children? Clin Radiol            2015; 35:212–216                                           do score as a method for reducing the number of
                                                                                                                                                                    2007; 62:365–369                                       	36.	Wakeley CP. The position of the vermiform ap-              CT studies when appendiceal ultrasound fails to
                                                                                                                                                               	32.	Peletti AB, Baldisserotto M. Optimizing US exami-           pendix as ascertained by an analysis of 10,000             visualize the appendix in adults. AJR 2015;
                                                                                                                                                                    nation to detect the normal and abnormal appendix           cases. J Anat 1933; 67:277–283                             204:519–526