Diagnostic Performance of MRI For Pregnant Patients With Clinically Suspected Appendicitis

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ª Springer Science+Business Media, LLC, part of Abdom Radiol (2018)

Abdominal Springer Nature 2018 https://doi.org/10.1007/s00261-018-1654-5

Radiology

Diagnostic performance of MRI for pregnant


patients with clinically suspected appendicitis
Sung Ah Wi,1 Dae Jung Kim ,1 Eun-Suk Cho,2 and Kyoung Ah Kim1
1
Department of Radiology, CHA Bundang Medical Center, CHA University, 351 Yatap-dong, Bundang-gu, Seongnam-si,
Gyeonggi-do 463-712, Korea
2
Department of Radiology, Yonsei University College of Medicine, Gangnam Severance Hospital, Seoul, Korea

Abstract appendix perforates, fetal loss risk dramatically increases


by up to 22%; therefore, early diagnosis and treatment is
Purpose: To evaluate the accuracy of magnetic resonance important [1, 2].
imaging (MRI) in the diagnosis of acute appendicitis in Computed tomography (CT) is widely used to eval-
pregnant patients and the value of additional diffusion- uate patients for suspected appendicitis with a reported
weighted MRI (DWI). sensitivity and specificity of 91%–98.5% and 90%–98%,
Methods: A total of 125 pregnant patients with clinically respectively [3, 4]; however, CT has disadvantages in
suspected appendicitis who underwent 1.5 T MRI were pregnant patients due to ionizing radiation and the use of
enrolled between May 2011 and January 2016. During iodinated contrast medium. Ultrasonography (US) is
this period, two radiologists prospectively predicted usually the first-line imaging modality in pregnant pa-
acute appendicitis on MRI during daily interpretation. tients with suspected appendicitis; however, the quality
We retrospectively reviewed clinical records, and radio- of US is heavily dependent on physician technique.
logical results were correlated with surgical pathology Identifying the appendix is difficult in pregnant patients
and clinical outcomes. We calculated the sensitivity, and the reported diagnostic yield varies widely; therefore,
specificity, and accuracy of MRI for diagnosing acute there is continued debate regarding the utility of US [5,
appendicitis. We performed additional DWI between 6].
August 2014 and January 2016, and we calculated With technical advances in magnetic resonance
sensitivity, specificity, and accuracy of MRI with or imaging (MRI), the routine identification of a normal or
without DWI. abnormal appendix is feasible and MRI has emerged as
Results: The sensitivity, specificity, and accuracy of MRI an alternative for the evaluation of patients presenting
for acute appendicitis were 100%, 95%, and 96%, with abdominopelvic pain. MRI has the safety-related
respectively. The sensitivity, specificity, and accuracy of advantage of avoiding exposure to ionizing radiation and
MRI without DWI (n = 72) vs. with DWI (n = 53) a high sensitivity for inflammation without exposure to
were 100%, 94.7%, and 95.8% versus 100%, 95%, and intravenous contrast material injection [7]. A recent
96%, respectively. meta-analysis study [8] reported that the sensitivity and
Conclusions: MRI has high accuracy for the diagnosis of specificity of MRI for the diagnosis of acute appendicitis
acute appendicitis in pregnant patients. Therefore, MRI were 96% (95% CI 95%–97%) and 96% (95% CI 95%–
is recommended for use as a first-line diagnostic test for 97%), respectively. In a subgroup of pregnant patients,
pregnant patients with clinically suspected appendicitis. the sensitivity and specificity of MRI were 94% (95% CI
87%–98%) and 97% (95% CI 96%–98%), respectively.
Diffusion-weighted MRI (DWI) can be applied to
Key words: Pregnancy—Magnetic resonance
abdominal imaging for evaluating inflammatory and
imaging—Appendix—Appendicitis
neoplastic diseases. Recently, a few studies have
demonstrated the feasibility of DWI for the evaluation of
acute appendicitis, and studies showed that DWI im-
Acute appendicitis is the most common non-obstetric proves the diagnosis accuracy of the acute appendicitis in
condition requiring surgery in pregnant patients. If the pediatric and consecutive patients [9, 10]. Until recently,
no study has demonstrated the feasibility of DWI for the
evaluation of acute appendicitis in pregnant patients.
Correspondence to: Dae Jung Kim; email: choikim75@gmail.com
S. A. Wi et al.: Diagnostic performance of MRI for pregnant patients

The purpose of this study was to evaluate the accuracy of A study coordinator, who did not initially analyze the
MRI in the diagnosis of acute appendicitis in pregnant MRIs, retrospectively reviewed all MRI interpretation
patients with clinically suspected appendicitis and to records and clinical records. Radiological results were
determine whether additional DWI improves diagnostic correlated with surgical pathology. Patients were classi-
accuracy. fied as radiologically acute appendicitis positive or radi-
ologically acute appendicitis negative according to the
Materials and methods MRI interpretation records. In addition, patients were
classified as pathologically acute appendicitis positive or
This retrospective study was designed from May 2011 to
pathologically acute appendicitis negative according to
January 2016 after approval by the institutional review
the clinical records.
board and the requirement for informed consent from
We calculated the sensitivity, specificity, and accuracy
individual patients was waived. In the study period, 125
of MRI for diagnosing acute appendicitis compared with
pregnant patients (first trimester, n = 6; second trime-
the surgical pathology results. We also determined the
ster, n = 89; third trimester, n = 30; 20 to 44 years of
sensitivity, specificity, and accuracy of the combination
age; mean 32 years) with clinically suspected appendicitis
of MRI with additional DWI and compared results with
underwent 1.5 T MRI to diagnose or exclude acute
the surgical pathology results. We used a McNemar’s test
appendicitis.
to analyze the diagnosis of acute appendicitis for con-
MRI was performed using a 1.5 Tesla system (Mag-
ventional MRI without DWI and conventional MRI
netom Sonata; Siemens, Erlangen, Germany) with a six-
with additional DWI. A two-tailed P value was deter-
element phased-array surface coil. From the outset, we
mined, and the null hypothesis was rejected at P<0.05.
had composed the MR sequences, mainly T2 WI without
DWI, and the following imaging sequences were per-
formed. Breath-hold T2-weighted half-Fourier single-
Results
shot turbo spin-echo (HASTE) images (TR = infinite, Among the 125 pregnant patients, 29 patients were
TE = 86 ms, slice thickness = 6 mm) in axial, coronal, classified as radiologically acute appendicitis positive.
and sagittal planes and breath-hold fat saturation T2- Among these patients, 25 patients underwent surgery and
weighted HASTE images in the axial plane were ob- 24 cases were pathologically diagnosed as acute appen-
tained. Breath-hold true fast imaging with steady-state dicitis (Figs. 1 and 3). The sensitivity, specificity, and
precession (FISP) images (TR = 4.3 ms, TE = 2.1 ms, accuracy of MRI for acute appendicitis were 100%, 95%,
slice thickness = 6 mm) in the axial plane was obtained. and 96%, respectively (Table 1).
A double-echo chemical shift gradient-echo sequence Among the 125 pregnant patients, 53 patients
image (TR = 6.4 ms, first-echo TE = 2.0 ms [opposed underwent additional DWI. Among these patients, 11
phase], second-echo TE = 4.2 ms [in-phase], flip angle were classified as radiological acute appendicitis positive
70°) was obtained in the axial plane. From August 2014, and nine cases were pathologically diagnosed as acute
we performed additional DWI. DWI was performed appendicitis (Figs. 2 and 3). The sensitivity, specificity,
using a single-shot spin-echo echo-planar imaging (EPI) and accuracy of MRI without DWI (n = 72) and with
sequence that combined the two diffusion (motion- DWI (n = 53) were 100%, 94.7%, and 95.8% and 100%,
probing) gradients before and after the 180° pulse along 95%, and 96%, respectively (Table 1). There was no
the three directions of section-select, phase-encoding, statistically significant difference in MRI without DWI
and frequency-encoding. Data acquisition with EPI and MRI with DWI (p=0.146).
readout was obtained by applying two different b factors
of 50 and 400 s/mm2. Fat saturation was used system-
atically to suppress chemical shift artifacts. The se-
quences were obtained during free breathing with
respiratory triggering. All slices were acquired from the
diaphragm to the bottom of the pelvis. Oral and intra-
venous contrast material was not used.
Two radiologists (with more than 10 years of expe-
rience in MRI interpretation) predicted acute appen-
dicitis on MRI during daily interpretation. The following
criteria defined acute appendicitis on MRI: thickening of
the appendix (> 7 mm in outer diameter) and/or peri-
appendiceal inflammation/fluid collection. The following
criteria defined acute appendicitis on DWI: hyperinten-
sity of the appendiceal wall on DWI without ADC map Fig. 1. Flow chart depicting MRI in the diagnosis of acute
appendicitis in pregnant patients compared with surgical
information [7, 11].
pathologic results.
S. A. Wi et al.: Diagnostic performance of MRI for pregnant patients

Table 1. Acute appendicitis, sensitivity, specificity, and accuracy of


magnetic resonance imaging (MRI) with or without diffusion-weighted
Discussion
imaging (DWI)
Pregnant patients frequently present with non-specific
MRI MRI with DWI MRI without DWI abdominal pain that is challenging to diagnose. Clinical
(n = 125) (n = 72) (n = 53) diagnosis is particularly difficult because of multiple
Sensitivity 100 100 100 confounding factors related to normal pregnancy. Acute
Specificity 95 95 94.7 appendicitis in pregnancy is the most common non-ob-
Accuracy 96 96 95.8 stetric surgical emergency [1, 2]. In the past, many
laparotomies were performed for suspected clinically
acute appendicitis in pregnant patients with a negative
laparotomy rate of 25%–50% [12, 13]. In addition to
these reasons, alterations in the position of intraab-
dominal contents by the pregnant uterus can make
clinical symptoms difficult to interpret; therefore, preg-
nant patients rarely present with classic symptoms.
Laboratory findings such as leukocytes or elevated ery-
throcyte sedimentation rates are unreliable parameters
during pregnancy [1, 2, 12, 13]. Recently, a meta-analysis
study [8] reported that the sensitivity and specificity of
MRI for the diagnosis of acute appendicitis in pregnant
patients were 94% (95% CI 87%–98%) and 97% (95% CI
96%–98%), respectively. In this study, we defined acute
appendicitis in pregnant patients on MRI [7, 11] as fol-
lows: thickening of the appendix (> 7 mm in outer
diameter) and/or periappendiceal inflammation/fluid
Fig. 2. Flow chart depicting MRI with or without DWI in the
collection. The sensitivity and specificity of MRI for
diagnosis of acute appendicitis in pregnant patients compared
with surgical pathologic results.
acute appendicitis were 100% and 95%, respectively. Our
study also revealed good performance of acute appen-

Fig. 3. A 33-year-old pregnant woman with surgically (arrows) with periappendiceal inflammation. C Diffusion-
proven acute appendicitis. A, B Axial and coronal T2- weighted MRI with a b value of 400 s/mm2 shows
weighted MRI shows a fluid-filled 10-mm-diameter appendix hyperintensity of the appendiceal wall.
S. A. Wi et al.: Diagnostic performance of MRI for pregnant patients

dicitis diagnosis, which shows high accuracy for the


diagnosis of acute appendicitis in pregnant patients.
Therefore, MRI may be acceptable for use as a first-line
diagnostic test to avoid unnecessary laparotomy and
complications of appendicitis in pregnant patients.
In the past, MRI had poorer spatial resolution com-
pared with that of CT, increased sensitivity to motion-
related artifacts, and long examination time. Until re-
cently, the higher cost of MRI compared to that of US or
CT was a major disadvantage to the use of MRI; how-
ever, technical advances give MRI many advantages for
the evaluation of pregnant patients presenting with ab-
dominopelvic pain. MRI also has a safety-related
advantage in avoiding exposure to ionizing radiation and
contrast materials and a high accuracy for acute appen-
dicitis diagnosis, even relative to the superior contrast
resolution and excellent characterization of pathologic
lesion in CT [14]. Long et al. [15] proposed a triage
workflow for pregnant patients where US is used as the Fig. 4. Flow chart depicting MRI in the diagnosis of beyond
first imaging test with MRI as an additional test if US acute appendicitis in pregnant patients.
results were indeterminate. US is readily available,
inexpensive, and safe; however, the appendix can be extracellular water molecules through Brownian motion
difficult to identify, particularly in pregnant patients, and provides information about the biophysical proper-
with visualization rates as low as 3% [5, 16]. Currently at ties of tissues such as cell organization and density,
our institution, MRI is a first-line diagnostic test for microstructure, and microcirculation [17]. Pathological
suspected appendicitis in pregnant patients. processes such as inflammation and neoplasia tend to
It is important to identify the cause of abdominal alter structural organization by destruction or regenera-
pain in pregnant patients, especially if that pain is outside tion of membranous elements or by a change in cellu-
the appendix. Numerous disease entities can cause larity. Therefore, DWI hyperintensity reflects high
abdominal pain during pregnancy, including gastroin- cellular density and structural distortion (diffusion
testinal, hepatobiliary, genitourinary, vascular, and restriction) with or without the T2 shine-through effect,
gynecologic origins. MRI is useful in diagnosing the which we suggest to be a neoplastic lesion or inflam-
cause of abdominal pain in pregnant patients because of matory lesion [17, 18]. Advances in MRI technology,
demonstrating a wide range of pathologic conditions in such as high-performance gradient coils, parallel imaging
the abdomen and pelvis beyond appendicitis [7, 14]. In techniques, and multiple phased-array receiver coils have
this study, 10 cases beyond acute appendicitis were de- enabled DWI to be applied to abdominal imaging with
tected in MRI (Figs. 4 and 5). The excellent contrast improved image quality [9]. Diffusion restriction of the
resolution of MRI has the added benefit of allowing for appendiceal wall had a strong association with acute
the evaluation of numerous additional structures within appendicitis [9, 11]. The diffusion restriction is caused by
the field of view to identify the actual source of the increased cell volume and viscosity in the inflamed ap-
abdominal pain. We suggest that further study is needed pendix wall. The advantage of DWI is that good visual
for investigating the ability of MRI to assist in the assessment is sufficient to detect an inflamed appendix
diagnosis of disease beyond acute appendicitis in preg- against a suppressed background signal. Leeuwenburgh
nant patients. et al. [19] reported a higher sensitivity for acute appen-
Leeuwenburgh et al. [11] reported that among the dicitis after viewing an additional DWI. Also, two
nine MRI features of acute appendicitis (appendix studies reported that DWI improves diagnosis accuracy
diameter, appendicolith, periappendiceal inflammation, of acute appendicitis [9, 10]. We had analyzed collecting
periappendiceal fluid collection, absence of gas in the data—generated by the additional DWI from August
appendix and destruction of the appendiceal wall struc- 2014 for the values of additional DWI. And then con-
ture, diffusion restriction of the appendiceal wall, diffu- ventional MRI with additional DWI had a slightly
sion restriction of the appendiceal lumen, and diffusion higher accuracy, but there was no statistically significant
restriction of focal fluid collections), dilatation of the difference in MRI without DWI and MRI with DWI
appendix (> 7 mm) and periappendiceal inflammation, (p = 0.146); However, these results with and without
and diffusion restriction of the appendiceal wall were DWI were within clinically acceptable ranges. Further
significantly associated with appendicitis in multivariate study is needed investigating the ability of DWI to
analysis. DWI is based on the de-phasing effect of diagnose the acute appendicitis in pregnant patients.
S. A. Wi et al.: Diagnostic performance of MRI for pregnant patients

Fig. 5. Beyond acute appendicitis. A, B Ureteral stone. with band adhesion (arrow) and normal appendix (arrow
Coronal T2-weighted MRI shows a signal void small lesion head). E Uterus rupture. Coronal T2-weighted MRI shows a
(arrow) in the right ureter with hydronephrosis and normal focal uterine wall defect (arrow) and normal appendix (arrow
appendix (arrow head). C, D Small bowel obstruction. Axial head).
and coronal T2-weighted MRI shows small bowel dilatation

The American College of Radiology (ACR) approves 24/29) revealed that the surgeon had made a clinical
pregnant patient MRI in any trimester, but ACR decision of early appendicitis (n = 3) and enteritis
emphasizes the need to assess the potential risk versus (n = 1) and antibiotic treatment was performed. Also,
benefit of MRI in pregnant patients [20]. Radiofrequency some cases of negative MRI results revealed that the
energy in MRI deposits on the patient’s body as heat; surgeon made a clinical decision of early appendicitis,
therefore, all MRI machines monitor the specific and antibiotic treatment was performed. We do not be-
absorption rate to ensure compliance with safety guide- lieve that the results can be explained by improvement in
lines. However, studies have demonstrated that the physical examination skills, but this cannot be deter-
maximum localized specific absorption rate occurs in the mined by our study. A prospective study design would
mother, not the fetus. No studies have demonstrated the help to evaluate the influence of treatment decisions
effects on the fetus secondary to MRI so the potential according to MRI results. Second, we included one
risk of heating the fetus and amniotic fluid should be lymphoid hyperplasia appendix case, among the MRI
considered [21, 22]. We always consider the potential risk false-positive cases (24/29). Lymphoid hyperplasia was
versus benefit of MRI in the pregnant patient. indistinguishable from clinically acute appendicitis, also
Our study had several limitations. First, this was a using either primary or secondary CT signs [23]. Third,
retrospective study based on surgical results and it was we checked clinical results according to the electronic
not possible to correct for all potential confounders. chart review and did not conduct patient interviews.
MRI probably influenced the decision for surgery; Lastly, the small number of patients at each group
however, it was not possible to determine exactly how maybe influenced in this study.
many patients progressed to surgery according to the In conclusion, MRI has high accuracy for the diag-
MRI results or how many surgeries were avoided. In this nosis of acute appendicitis in pregnant patients with
study, four cases of false-positive MRI results (n = 5, clinically suspected appendicitis. Therefore, MRI may be
S. A. Wi et al.: Diagnostic performance of MRI for pregnant patients

acceptable for use as a first-line diagnostic test for pa- 8. Duke E, Kalb B, Arif-Tiwari H, et al. (2016) A systematic review
and meta-analysis of diagnostic performance of MRI for evaluation
tients with clinically suspected appendicitis. And addi- of acute appendicitis. AJR Am J Roentgenol 206:508–517
tional DWI statistically did not improve diagnostic 9. Inci E, Kilickesmez O, Hocaoglu E, et al. (2011) Utility of diffu-
accuracy. Further study is needed for investigating the sion-weighted imaging in the diagnosis of acute appendicitis. Eur
Radiol 21:768–775
ability of DWI to diagnose the acute appendicitis in 10. Bayraktutan U, Oral A, Kantarci M, et al. (2014) Diagnostic per-
pregnant patients. formance of diffusion-weighted MR imaging in detecting acute
appendicitis in children: comparison with conventional MRI and
Compliance with ethical standards surgical findings. J Magn Reson Imaging 39:1518–1524
11. Leeuwenburgh MM, Jensch S, Gratama JW, et al. (2014) MRI
Conflict of interest All authors declare no conflicts of interest or features associated with acute appendicitis. Eur Radiol 24:214–222
sources of funding. 12. Maslovitz S, Gutman G, Lessing JB, Kupferminc MJ, Gamzu R
(2003) The significance of clinical signs and blood indices for the
Ethical approval All procedures performed in this study were in diagnosis of appendicitis during pregnancy. Gynecol Obstet Invest
accordance with the ethical standards of the responsible committee on 56:188–191
human experimentation (institutional and national) and were in accord 13. Andersen B, Nielsen TF (1999) Appendicitis in pregnancy: diag-
with the Helsinki Declaration of 1964 and later versions. nosis, management and complications. Acta Obstet Gynecol Scand
78:758–762
14. Singh A, Danrad R, Hahn PF, et al. (2007) MR imaging of the
Informed consent This study was described after approval by the
acute abdomen and pelvis: acute appendicitis and beyond. Radio-
institutional review board, and the requirement for informed consent
graphics 27:1419–1431
from individual patients was waived.
15. Long SS, Long C, Lai H, Macura KJ (2011) Imaging strategies for
right lower quadrant pain in pregnancy. AJR Am J Roentgenol
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