Wo m e n ’s I m a g i n g • C l i n i c a l O b s e r v a t i o n s

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Oto et al. MRI to Locate Appendix During Pregnancy

W O M E N ’S IMAGING

Revisiting MRI for Appendix Location During Pregnancy

Aytekin Oto1 Padmavathia N. Srinivasan Randy D. Ernst Mert Koroglu Fernando Cesani Thomas Nishino Gregory Chaljub

OBJECTIVE. The purpose of this study is to determine the location of the appendix in pregnant patients by MRI and to investigate the possibility of gradual upward displacement of the appendix during pregnancy. CONCLUSION. The gradual upward displacement of the appendix during pregnancy was confirmed. MRI can be used for determination of the appendix localization in pregnant patients. Further studies with a larger number of patients will be helpful to answer this clinically relevant question.

Oto A, Srinivasan PN, Ernst RD, et al.

ppendicitis complicates approximately 1 of 1,500 pregnancies and is the most common nonobstetric indication for surgical exploration of the gravid abdomen [1, 2]. Early diagnosis is crucial because fetal mortality may rise from 1.5% to as high as 36% when perforation occurs [3]. The single most reliable symptom in pregnant patients with appendicitis is abdominal pain [4]. Classical obstetrics teaching has been that the location of the pain of appendicitis migrates upward with the growing uterus [5]. This concept was based on the article written by Baer et al. [6] in 1932 describing a progressive upward displacement of the appendix during the course of pregnancy shown by serial barium enema studies performed in pregnant women. The findings of that article have been challenged by the results of recent clinical research studies [5, 7, 8]. The need for a new study using an imaging tool that does not expose pregnant patients to ionizing radiation was emphasized [8]. MRI has been used increasingly for the imaging of pregnant women for both maternal and fetal diseases and can provide multiplanar images with excellent soft-tissue contrast resolution and without ionizing radiation [9, 10]. The purpose of our study was to determine the location of the appendix in pregnant patients using MRI and to investigate the possibility of gradual upward displacement of the appendix during pregnancy.

Keywords: abdomen, abdominal imaging, appendix, emergency radiology, MRI, pregnancy DOI:10.2214/AJR.05.0270 Received February 16, 2005; accepted after revision April 29, 2005. 1All authors:

Department of Radiology, The University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555-0709. Address correspondence to A. Oto.

AJR 2006; 186:883–887 0361–803X/06/1863–883 © American Roentgen Ray Society

AJR:186, March 2006

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Materials and Methods Patient Selection A search of our database was performed to identify the pregnant patients who underwent abdominal or pelvic MRI examinations in our institution between April 2002 and April 2004. Patients with intraabdominal masses or history of abdominal surgery were excluded. Permission from the institutional review board was obtained to review the clinical MRI examinations and medical records for scientific research.

MRI Technique All of the patients were imaged using a 1.5-T MRI scanner (Signa, GE Healthcare) with a phased-array coil. Because the indications for MRI examinations were not the same for each patient, MRI protocols were not uniform. The MRI protocol for patients imaged for obstetrical reasons (fetal or placental diseases) included axial, coronal, sagittal, and oblique T2-weighted single-shot fast spinecho (SSFSE) images (TR/TE, infinite/80; matrix, 256 × 256; bandwidth, 31.25 Hz/pixel; slice thickness, 6 mm with 0–2 mm spacing) and axial T1weighted fast spin-echo images (700/minimum; number of excitations, 3; echo-train length, 2; matrix, 192 × 256; bandwidth, 20.83 Hz/pixel; slice thickness, 6 mm with 1-mm spacing). In addition to these sequences, axial fat-suppressed fast spinecho T2-weighted (2,500–3,200/90; number of excitations, 2; echo-train length, 17; matrix, 192 × 256; bandwidth, 20.83 Hz/pixel; slice thickness, 7 mm with 1-mm spacing) and axial STIR (7,750/34; inversion time, 150 msec; number of excitations, 2; echo-train length, 17; matrix, 160 × 256; bandwidth, 15.63 Hz/pixel; slice thickness, 7 mm with

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Oto et al. 1-mm spacing) images were obtained in patients imaged for maternal diseases. SSFSE images were obtained during suspended respiration (at the end of expiration). All other sequences were acquired during quiet respiration. IV gadolinium was not administered in any patient. The regions of interest and imaging planes were determined according to the clinical indication. The field of view varied from 25 to 40 cm.

Image Analysis Two radiologists with fellowship training in abdominal imaging and more than 8 years of experience in body MRI reviewed the images together to detect the appendix and the cecum. First, the cecum was localized in the right lower quadrant. After identification of the terminal ileum and ileocecal valve, the second blind-ending tubular structure connecting to the cecum was accepted as the appendix. This decision was made by consensus. If the cecum and the appendix were identified both on a coronal and an axial sequence, measurements were obtained to determine the superoinferior distance between the base of the appendix and the level of the iliac crest and the superoinferior distance between the most inferior portion of the cecum and the level of the iliac crest. Images were reviewed using eFilm Workstation 2.0 software (Merge Healthcare) allowing simultaneous review of different sequences and displaying the level of the image plane of the selected sequence as a reference line on the other displayed sequences on the screen. This feature was used to measure the iliac crest—appendix and iliac crest–cecum distances. If the base of the appendix or most inferior portion of the cecum was seen on an axial image, the level of the axial image was displayed on the coronal image showing the iliac crest. The superoinferior distance between the reference line and the level of iliac crest was measured on the coronal image and recorded. If the base of the appendix or most inferior portion of the cecum was seen on a coronal image and the same coronal image also showed the iliac crest, then the superoinferior distance between them and the level of iliac crest was measured and recorded. If the iliac crest was not seen on the coronal image where the base of the appendix or most inferior portion of cecum was identified, then the axial image passing through the iliac crest was determined, and its level was displayed on the same coronal image as a reference line representing the level of the iliac crest. Superoinferior distance measurements were performed on the coronal image and recorded. The distances were accepted as “+” if the appendix or cecum was above the level of the iliac crest and were accepted as “–” if the appendix or cecum was below the level of the iliac crest.

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Data Analysis Superoinferior distance (appendix–iliac crest) and superoinferior distance (cecum–iliac crest) were classified into three groups based on the trimester of pregnancy. The mean and the range of distances were calculated for each trimester. Statistical comparison of the mean measurements of different trimester subgroups was not performed due to the small sample size of the subgroups. Pearson’s correlation coefficient (r) was used to measure the strength of the linear correlation between the mean superoinferior distances of appendix and cecum to iliac crest and the gestational week of pregnancy.

Results The records of 72 pregnant patients were initially retrieved from the database. Seven patients were excluded due to the presence of an intraabdominal mass or previous abdominopelvic surgery. After review of the MRI images of the remaining patients, the appendix could be identified in 47 patients on both axial and coronal images. Eight (17.0%) of these patients were in the first trimester, 18 (38.3%) were in the second trimester, and 21 (44.7%) were in the third trimester. Mean superoinferior base of appendix–iliac crest distance was –2.7 cm (ranging between –8 and 2.3 cm), −0.1 cm (ranging between –5.5 and 3.1 cm), and 2.6 cm (ranging between –3.2 and 6.4 cm) for the pregnant patients in the first, second, and third trimesters, respectively. The cecum was identified in 57 patients on both axial and coronal images. Nine (15.8%) of these patients were in the first trimester, 22 (38.6%) were in the second trimester, and 26 (45.6%) were in the third trimester. Mean superoinferior cecum–iliac crest distance was –3.3 cm (ranging between –7.1 and 2.5 cm), −1.2 cm (ranging between –6.3 and 2.7 cm), and 1.4 cm (ranging between –4.2 and 6.4 cm) for the pregnant patients in the first, second, and third trimesters, respectively. The wide range of both mean superoinferior appendix–iliac crest and superoinferior cecum–iliac crest measurements in all three trimesters indicated substantial individual variability of the appendix and cecum location (Figs. 1–3). The Pearson’s correlation coefficient test indicated a moderate correlation between mean superoinferior base of appendix–iliac crest distance and gestational weeks of pregnancy (r = 0.64) and mean cecum–iliac crest distance and gestational weeks of pregnancy (r = 0.62) (Figs. 4 and 5).

Discussion Baer et al. [6] showed by serial barium enema studies that the appendix undergoes progressive displacement superiorly starting after the third month, reaches the level of the iliac crest at the end of the sixth month, and rises above this level during the third trimester. In that study, the authors also mentioned that the long axis of the appendix underwent a counterclockwise rotation. The findings of their study have never been replicated due to obvious risks of radiation exposure to the fetus. However, the results have led to two clinically significant consequences. Theoretically, the upward displacement of the appendix would change the location of the perceived pain toward the right upper quadrant with advancing gestational age. Therefore, right upper quadrant pain has been accepted as a sign of acute appendicitis in third trimester pregnant patients [4]. Second, as a result of the Baer et al. study, the choice of appendectomy incision during the second and third trimester is frequently debated, and many surgeons have modified the McBurney incision to more superior incisions [11]. Within the last 5 years, the results of the Baer et al. [6] study have been challenged by several clinical studies [5, 7, 8]. In their review of 67 pregnant patients with probable appendicitis, Mourad et al. [5] concluded that pain in the right lower quadrant of the abdomen was the most common presenting symptom of appendicitis in pregnancy regardless of gestational age. Hodjati and Kazerooni [7] reviewed 26 pregnant patients with acute appendicitis and stated that based on their findings, the concept of the appendix being located in the right upper quadrant during pregnancy can cause inappropriate delay of treatment. To ascertain the optimal incision for removal of appendix during pregnancy, Popkin et al. [8] retrospectively reviewed the medical records of pregnant patients who underwent appendectomy between 1995 and 2000. Within this period, 23 pregnant patients underwent appendectomy; 18 incisions were made over McBurney’s point and five were created superior to McBurney’s point. The authors reported that the appendix was easily located in 94% of the incisions made through McBurney’s point. Their conclusion was that a McBurney incision could be successfully used in pregnant patients in all trimesters. In the discussion of their article, Popkin et al. mentioned that a study to examine the localization of the appendix in pregnant patients by MRI would be a welcome addition to the literature.

AJR:186, March 2006

MRI to Locate Appendix During Pregnancy

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Fig. 1—Normal appendix in 18-year-old pregnant patient at 12-weeks’ gestation. A, Axial T2-weighted single-shot fast spin-echo image through pelvis shows normal appendix (arrow) within pelvis. B, Coronal T2-weighted image shows level of base of appendix (dotted line) and level of iliac crest (IC). Note that appendix is below level of iliac crest.

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Fig. 2—Normal appendix in 29-year-old pregnant patient at 14-weeks’ gestation. A, Axial fat-suppressed T2-weighted single-shot fast spin-echo image shows appendix posterolateral to cecum (arrow). B, On coronal fat-suppressed T2-weighted image, level of appendix (dotted line) is same as level of iliac crest.

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MRI has been described as a valuable technique for the evaluation of both adult and pediatric patients with acute appendicitis [12, 13]. Recently, several studies suggested that

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MRI is helpful in evaluation and diagnosis of acute appendicitis in pregnant patients by showing the inflamed appendix and other potential conditions mimicking appendicitis

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such as adnexal torsion [14–16]. These studies also showed that MRI could show the appendix (healthy or inflamed) in more than 80% of the pregnant patients [14, 15].

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Fig. 3—Normal appendix in 28-year-old pregnant patient at 26-weeks’ gestation. A and B, Axial (A) and coronal (B) T2-weighted single-shot fast spin-echo sequence shows normal appendix (arrows) arising from medial aspect of cecum. Appendix is above level of iliac crest (IC).

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r2 = 0.4093

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–2 –4 –6 –8

Appendix SI Displacement (cm)

Appendix SI Displacement (cm)

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Oto et al.

6 r 2 = 0.3818

4 2 0 0

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Gestation (weeks)

Gestation (weeks) Fig. 4—Plot of mean superoinferior base of appendix–iliac crest distance (cm) as function of weeks of gestation. Diamonds (♦) represent individual measurements made from MR images. Solid line represents best fit to data using standard leastsquares method. The Pearson’s correlation coefficient for these data is r = 0.64, thus indicating moderate positive correlation. SI = superoinferior.

The results of our study showed a gradual superior displacement trend in both the appendix and cecum as the pregnancy progresses. Our results indicated a moderate correlation between the location of the appendix and gestational age. While the appendix was well below the iliac crest in the first trimester, it rose to the level of the iliac crest in the second trimester and further progressed superiorly, with a mean of 2.6 cm above the iliac crest in the third trimester. Our results are similar to the

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Fig. 5—Plot of mean superoinferior cecum–iliac crest distance (cm) as function of weeks of gestation. Diamonds (♦) represent individual measurements made from MR images. Solid line represents best fit to data using standard least-squares method. Pearson’s correlation coefficient for these data is r = 0.62, thus indicating moderate positive correlation. SI = superoinferior.

findings of Baer et al. [6]. They have also reported the appendix to be located an average of 2 fingerbreadths above the iliac crest after 8 months of pregnancy. In addition, the range of distances between the iliac crest and appendix was wide in all trimesters in our study. This may be secondary to the small number of patients in each trimester; however, it may also potentially indicate a significant individual variation in the location of the appendix during pregnancy. In any case, MRI can enable the

surgeon to choose an incision site customized for the pregnant patient by demonstrating the exact location of the inflamed appendix. Some limitations should be considered when reviewing the results of this study. First, the study was retrospective, and not all of the MRI examinations were designed to detect the location of the appendix and the cecum. Second, the small number of patients included in the study, especially after classification into three subgroups based on gestational age, is

AJR:186, March 2006

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MRI to Locate Appendix During Pregnancy not enough to make statistical comparisons. Further prospective studies with larger numbers of patients will be necessary to definitively describe the location of the appendix. In conclusion, our results confirmed the classical teaching of a gradual upward displacement of the appendix during pregnancy, and MRI can be a useful tool for determination of the appendix localization in pregnant patients. Further studies with larger numbers of patients will be helpful to resolve this clinically relevant issue.

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3. Babaknia A, Parsa H, Woodruff JD. Appendicitis during pregnancy. Obstet Gynecol 1977; 50:40–44 4. Sharp HT. The acute abdomen during pregnancy. Clin Obstet Gynecol 2002; 45:405–413 5. Mourad J, Elliott JP, Erickson L, Lisboa L. Appendicitis in pregnancy: new information that contradicts long-held clinical beliefs. Am J Obstet Gynecol 2000; 182:1027–1029 6. Baer JL, Reis RA, Arens RA. Appendicitis in pregnancy. JAMA 1932; 52:1359–1364 7. Hodjati H, Kazerooni T. Location of appendix in the gravid patient: a re-evaluation of the established concept. Int J Gynaecol Obstet 2003; 81:245–247 8. Popkin CA, Lopez PP, Cohn SM, Brown A, Lynn M. The incision of choice for pregnant women with appendicitis is through McBurney’s point. Am J Surg 2002; 183:20–22 9. Nagayama M, Watanabe Y, Okumura A, Amoh Y, Nakashita S, Dodo Y. Fast MR imaging in obstetrics. RadioGraphics 2002; 22:563–582 10. Leyendecker JR, Gorengaut V, Brown JJ. MR imaging of maternal diseases of the abdomen and pel-

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