Author's Accepted Manuscript

Challenges in MR Imaging for Suspected Acute

Appendicitis in Pregnant Patients
Noah G. Ditkofsky MD, FRCPC, Ajay Singh MD

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PII: S0363-0188(15)00002-X
DOI: http://dx.doi.org/10.1067/j.cpradiol.2015.01.001
Reference: YMDR334

To appear in: Curr Probl Diagn Radiol

Cite this article as: Noah G. Ditkofsky MD, FRCPC, Ajay Singh MD, Challenges in MR
Imaging for Suspected Acute Appendicitis in Pregnant Patients, Curr Probl Diagn
Radiol, http://dx.doi.org/10.1067/j.cpradiol.2015.01.001

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Title:
Challenges in MR Imaging for Suspected Acute Appendicitis in
Pregnant Patients

Authors & affiliations:

(Author 1 is corresponding author)

1. Noah G. Ditkofsky MD, FRCPC

Emory University School of Medicine
Emory University Hospital Midtown
Department of Radiology
50 Peachtree St NE
Atlanta, GA
30308

e-mail: ditkofsky@gmail.com
Telephone: 781-228-1566

2. Ajay Singh MD
Harvard Medical School
Massachusetts General Hospital
Department of Radiology
55 Fruit St.
Boston, MA
02114

The authors declare that we have no relevant financial disclosures.

Text that has been has been removed. Text in red has been added. Text in
green has been moved. Figure numbers have been changed to reflect reviewer
suggestions for reordering.

Introduction & background:

The assessment of a gravid patient with abdominal pain is a challenging

endeavor. One must consider not only the common etiologies for abdominal pain,
but also etiologies resulting directly from the patients’ gravid state(1). Further
complicating the assessment is the altered anatomy and physiology that result from
the enlarged uterus displacing and compressing normal anatomic structures. As a
pregnancy progresses and the uterus enlarges, it has been demonstrated that the
appendix and cecum are gradually and progressively displaced superiorly(2). This
results in an altered clinical picture than would be classic for appendicitis and
necessitates an imaging diagnosis.
Appendicitis in the gravid patient has the highest incidence in the second
trimester(3). Once appendicitis is complicated by perforation or abscess; there is an
increased risk of fetal loss (4-6). However, abdominal surgery during pregnancy
also increases the risk of a poor pregnancy outcome (6, 7). Thus, accurate and
timely imaging diagnosis of appendicitis has increased importance in the gravid
population.
When appendicitis is suspected, imaging investigation should not be delayed.
In 2009 Pedrosa et al demonstrated that MR in the setting of suspected acute
appendicitis results in a decreased negative laparotomy rate as well as decreased
risk of perforated appendicitis(8). Thus appropriate and timely imaging can result
in better patient outcomes.

If appendicitis is suspected in a pregnant patient how should I proceed?

When recommending imaging in any clinical scenario, one should refer to the
appropriateness criteria published by the American College of Radiology (ACR)
(Table1). The purpose of these criteria is to ensure that patients receive the most
appropriate evidence based care. In the setting of a gravid patient with suspected
acute appendicitis the first line imaging modality is abdominal ultrasound, which
garners an appropriate criteria of 8 followed by MRI of the abdomen and pelvis
without contrast with an appropriateness criteria of 7(9). Ultrasound is an
inexpensive test that should always precede MRI; however, it can be technically
challenging in the setting of pregnancy. MRI should be considered in the gravid
patient with equivocal ultrasound findings as it provides excellent anatomic detail
and involves no ionizing radiation. The drawbacks of MRI are increased costs and
decreased availability. CT is faster, cheaper and more available than MRI and has
been validated in the pregnant population(10). However, its use of ionizing
radiation relegates it to an ACR appropriateness criteria of 6. A graphical
representation of the imaging decision tree is summarized in Figure 1.
Is MRI safe in Pregnancy?

There are no long-term studies on the effect of in-utero MRI exposure. However
several short-term studies have identified no deleterious effects attributable to
MRI(11-13). In 2001, the ACR recognized the need for a guide to safe MRI practices
and convened the first Blue Ribbon Panel on MR Safety. In the intervening years the
recommendations of this panel have twice been revised with the most recent
iteration being published in 2013. The position of the Blue Ribbon Panel is that
although to date, there is no conclusive evidence of any deleterious effects upon the
developing fetus caution should nevertheless be exercised when utilizing MRI in the
pregnant patient. MRI is presumed to be safe at any stage of pregnancy; however,
examinations that can wait until the conclusion of pregnancy should be
postponed(14). If an exam cannot be postponed then there should be a clear risk-
benefit ratio warranting the study and the radiologist must document:
1. The required information cannot be acquired with ultrasound.
2. The information being sought has the potential to alter the care of the fetus
or the patient during the course of the pregnancy.
3. The information being sought is sufficiently important that “it would not be
prudent” to delay its acquisition cannot wait until the conclusion on the
pregnancy.
Currently, the principle concern with MRI safety in pregnancy relates to the
unknown effect of heating the fetal tissues that can ensue with deposition of radio-
frequency (RF) energy.

What sequences should I perform and in what order to maximized diagnostic

yield?

At our institution all MR examinations for appendicitis performed in the ED

are performed under the direct supervision of a radiologist. We use an 8-channel
surface coil and begin with the standard 3-plane localizer. We then perform 3-plane
single-shot half-Fourier T2-weighted sequences with a large field of view
encompassing the abdomen and pelvis. Although of limited resolution, they provide
means of anatomically localizing the appendix and can be done without the
radiologist present. Once the radiologist has reviewed the images to localize the
cecum and the expected region of the appendix, the exam is localized to the
pericecal region and a smaller field of view is employed. The technologist, without
the radiologist present, can then complete the remainder of the standard sequences.
3-plane single-shot half-Fourier T2-weighted sequences are again performed, this
time with fat saturation to assess for peri-appendiceal inflammation. Single-shot
half-Fourier T2-weighted sequences are performed at the beginning of the exam as
they take only minutes to perform (usually less than 60 seconds per plane) and will
usually provide some diagnostic information in the patient is unable to tolerate the
remainder of the sequences. We then perform an axial STIR sequence, and axial
breath hold T2 to better define appendiceal anatomy. Lastly an axial T2 fat
saturated sequence is performed to assess for subtler periappendiceal inflammatory
change. The radiologist then returns to the scanner and reviews the images (with
the patient on the table) in order to determine the need for additional imaging. As
the MR is performed with direct radiologist supervision, the protocol can be
modified as needed and under ideal circumstances requires approximately 20
minutes. The use of rectal saline is currently under investigation at Massachusetts
General Hospital and has not yet been validated however; in our experience we have
found it useful in providing cecal and appendiceal distension which can aid in
localization of the appendix. For further details see Table 2.

Pregnancy alters the normal anatomy of the pelvis, how does the position of
the appendix change as a pregnancy progresses?

As a pregnancy progresses, the gravid uterus increases in size and displaces

pelvic structures from their normal anatomic position; the appendix may be
displaced as far superiorly as the liver(15). In 1932, Baer et al used fluoroscopy to
serially evaluate the position of the appendix in 70 gravid patients with no
symptoms of appendicitis throughout their pregnancies. This study demonstrated
that during the course of the pregnancy, the appendix is gradually displaced
superiorly out of the pelvis(16). Thankfully, this study has never been replicated!
In 2006 however, Oto et al. sought to validate Baer’s findings by performing a
retrospective review of all gravid patients imaged by MRI at the University of Texas
Medical Branch over a two year period, and excluded those patients who had
abdominopelvic masses or prior surgery. Of the 72 patients enrolled in the study,
the appendix was identified in 47 (~65%)and found to be gradually displaced
superiorly as the pregnancy progressed with a moderate correlation between
position of the appendix and gestational age(2). Baer and Oto both found the
appendix to be below the iliac crest in the first trimester, at the level of the iliac crest
in the second trimester and displaced approximately 2.6 cm superior to the iliac
crest in the third trimester(2, 16) (Figure 2).

What about contrast?

Intravenous Gadolinium Chelates:

The maternal and fetal circulations are interconnected systems separated by
the placenta. Maternal blood transports oxygen and nutrients to the intervillous
spaces of the placenta, allowing them to pass into the fetal circulation by crossing a
single layer of chorionic epithelium(17). Drugs that are dissolved in maternal blood
reach the placenta and may diffuse across it, particularly those drugs which are
lipid-soluble, low molecular weight (<100 Da) or non-ionized water-soluble
molecules(17, 18). Although the high molecular weights of gadolinium chelates
restrict their diffusion across the placenta, they nevertheless do cross into fetal
circulation in small amounts(17, 18). Once gadolinium crosses the placenta into the
fetal circulation it follows the typical gadolinium excretory pathway - being filtered
out of fetal circulation by the kidneys. However, once the fetal kidneys have filtered
the gadolinium it passes into the amniotic fluid via the urine. The fetus is constantly
swallowing amniotic fluid and thus, a small amount of contrast material enters the
fetal gastrointestinal tract(18). This results in opportunity for gadolinium to de-
chelate and expose the developing fetus to toxic free gadolinium. The 2013 ACR blue
ribbon panel on MRI safety has recommended that intravenous gadolinium not be
routinely provided to pregnant patients. At our institution, gadolinium is not
administered to pregnant patients with suspected appendicitis. If gadolinium
administration is felt be necessary, the decision must be accompanied by a well-
documented and thoughtful risk–benefit analysis(14) demonstrating that the
expected benefit to the patient or fetus considerably outweighs the hypothetical but
real risks of long-term fetal exposure to free gadolinium ions, the sequelae of which
are uncertain. This should be documented in the chart. We also recommend
written consent from the patient. To date, no carcinogenic, mutagenic, teratogenic
or other long-term effects have been reported following in utero exposure to
gadolinium based contrast agents(18-20).

Oral Contrast:
At this time the use of oral contrast is not felt to aid in the detection of the
appendix on MRI(21) and at out institution, we do not routinely administer oral
contrast to patients undergoing MRI assessment for appendicitis.

Rectal Contrast:
A current review of the literature does not demonstrate any publications
detailing the use of rectal contrast for the investigation of appendicitis in pregnancy.
At our institution a radiologist carefully monitors all MRIs for appendicitis in gravid
patients, and rectal saline is being used on an investigational and problem solving
basis.

What are the MR features of the normal appendix and appendicitis?

The appendix is an approximately 9-10 cm long (range 5-35 cm(22)) blind

ending tubular structure arising from the posteromedial cecal wall, roughly 3cm
below the illeocecal valve (23, 24). The normal MRI appearance of the appendix is
that of a tubular structure that measures less than 6 mm in overall thickness with a
wall thickness of less than 2 mm(24). In the absence of endoluminal contrast, the
appendix has a cordlike appearance and intermediate signal intensity on all
sequences that parallels that of the wall of the adjacent terminal ileum and cecum
(23, 25) on both T2 (Figure 3) and T1 (Figure 4) weighted images. The normal
appendix is unlikely to be identified on STIR imaging(26).
The appearance of appendicitis on MRI can be divided into morphological
abnormalities and signal abnormalities. Morphologically the inflamed appendix
demonstrates a caliber of greater than 7mm and a thickened appearing wall(27).
The inflamed wall of the appendix also has altered signal characteristics, with
decreased signal intensity on T1 weighted images and increased signal intensity on
T2 weighted sequences (26)(Figure 5B). T2 fat saturated images are excellent in
depicting periappendiceal inflammation (Figure 5 & 6) as well as the inflamed
appendix(25). STIR imaging will also demonstrate these findings (Figure 7).
Although not a part of our standard protocol, diffusion weighted imaging (DWI) can
be a useful adjunct. The inflamed appendix will demonstrate increased DWI signal
at B-values of 500 and 1000 s/mm2 and decreased signal on ADC map due to
inflammation of the appendiceal wall and highly cellular and viscous material in the
appendiceal lumen(28). In the second and third trimester dilated pelvic veins can
simulate the appendix. Time of flight (TOF) imaging can be useful in differentiating
a vascular structure from the appendix, as there should be flow in the former but
not the latter(24).
Occasionally, an appendix will be morphologically indeterminate for
appendicitis (measure between 6 mm and 7 mm in diameter and not contain gas
([gas demonstrates low signal on T1 and T2 sequences with blooming on gradient
sequences]). In these cases, ancillary findings of appendicitis such a peri-
appendiceal inflammation can be useful(24). In the rare case where the appendix is
indeterminate by size criteria and there are no ancillary findings of appendicitis, we
advocate close clinical observation with the patient’s clinical picture dictating the
need for follow-up MRI or CT scan.
The differential diagnosis for right lower quadrant pain in the pregnant
patient is not limited to appendicitis but includes entities such as urolothiasis,
ovarian torsion, Crohn’s disease, diverticulitis and placental abruption. A complete
description of each of these is beyond the scope of this article; however, one should
be aware of that these entities might occasionally be encountered.

My patient is in too much discomfort to remain still for MRI, can she be
sedated?

If the MRI is deemed indispensable to the patient’s care, but the patient
cannot tolerate MR due to pain or claustrophobia, sedation may be considered.
Gravid patients have elevated oxygen consumption with decreased functional
residual capacity. These factors can contribute to a rapid decrease in maternal PaO2
during even brief episodes of apnea(29, 30). Hemodynamic changes also occur
during pregnancy and include decreased blood pressure due to vasodilatation, the
low-resistance placenta, and aortocaval compression by the gravid uterus(31).
There is increased cardiac output, and decreased maternal hematocrit(30). Due to
the complexities of maternal and fetal physiology we do not advocate that the
radiologist independently attempt sedation. Rather an experienced obstetrical
anesthesiologist skilled in conscious sedation and airway management should
sedate the patient and remain attendant during image acquisition. Frequently used
medications include midazolam, remifentanil, propafol, nitrous oxide and
ketamine(31). If sedation does prove to be necessary, imaging should be performed
with the radiologist present at the scanner in order to remove any unnecessary
sequences and add any that are deemed diagnostically necessary with the goal of
reducing overall time under sedation.

How can I improve image quality?

MR imaging requires the patient to remain still and/or suspend respiration

during image acquisition. This can be challenging for the gravid patient, partially
due to the abdominal pain that necessitate the exam, but also due to a myriad of
physical discomforts common in pregnancy. This necessitates rapid imaging in a
motion resistant manner. MR imaging protocols for assessment of appendicitis can
generally be classified into free-breathing protocols and breath-hold protocols.
Free-breathing protocol should be used for patients who are unable to suspend
respiration for longer than 20 seconds(32). Free breathing protocols rely on
magnetization-prepared T1-weighted sequences and single-shot half-Fourier T2-
weighted sequences that acquire each section sequentially at a rate of
approximately 1 section per second(27). The rapidity of single-shot half-Fourier
T2-weighted sequences and the sequential nature of their acquisition make them
relatively motion insensitive compared to standard spin echo T2-weighted
imaging(24). Use of a multichannel surface coil can also speed the acquisition of
images and increase signal to noise ratio(33).

Conclusion:

- MRI of the appendix is safe in pregnancy and should be performed in the

setting of appendicitis and equivocal ultrasound.
- The exam can performed in approximately 20 minutes of MRI time under
ideal circumstances.
- Use of surface coil and rapid motion resistant sequences will provide the best
image quality.
- A radiologist should monitor the exam and add or alter sequences as needed.
- The results of appendiceal MRI can significantly alter the course of patient
care.
- Pregnancy alters the normal location of the appendix and knowledge of this
is important when trying to locate the appendix.

Conflict of Interest:
The authors declare that they have no conflict of interest.

Acknowledgements:
The authors would like to thank Sue Loomis of REMS for her assistance with graphic
design for this project.

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Figures revised

Table 1: Imaging recommendations for suspected

appendicitis in pregnancy
Adapted from: Rosen M, et al. ACR Appropriateness
Criteria, right lower quadrant pain -suspected
appendicitis. JACR. 2011;8(11):749-55
Study ACR recommendation

Ultrasound of Abdomen: 8

MRI abdomen and pelvis without contrast 7

Ultrasound of the Pelvis 6

CT abdomen and pelvis with contrast 6

CT abdomen and pelvis without contrast 5

Abdominal Radiograph 2

Barium Enema 2

99mTc WBC scan abdomen and pelvis 2

Table 2: Suggested Appendicitis in Pregnancy
Protocol. These sequences are performed in this order
to reduce the likelihood of a non-diagnostic examination
and are directly supervised by a radiologist. The
administration of rectal saline is currently under
investigation at our institution and is only administered
on an as needed basis, typically either at the conclusion
of the above protocol (followed by tri-plane fat saturated
SSFSE sequences) or between the SSFSE and the fat
saturated SSFSE sequences in the above protocol.
 Coil Used: 8 Channel Surface

Field of View: 32 cm

Matrix size: 256 X 192

Slice
Plane Weighting Type Breath Hold TE (ms) TR (ms) TI (ms) Slice Thickness spacing ECHO train

3-plane localizer T2 Gradient No

Coronal T2 SSFSE Spin Echo Yes 140 Minimum n/a 4 mm 1 mm 0

Sagital T2 SSFSE Spin Echo Yes 100 Minimum n/a 4 mm 1 mm 0

Axial T2 SSFSE Spin Echo Yes 140 Minimum n/a 4 mm 1 mm 0

Coronal T2 SSFSE (fat saturated) Spin Echo Yes 140 Minimum n/a 4 mm 1 mm 0

Sagital T2 SSFSE (fat saturated) Spin Echo Yes 100 Minimum n/a 4 mm 1 mm 0

Axial T2 SSFSE (fat saturated) Spin Echo Yes 140 Minimum n/a 4 mm 1 mm 0

Axial IR STIR Yes 68 4000 150 5 mm 1 mm 10

Axial T2 FRFSE-XL Spin Echo Yes 90 2100 n/a 4 mm 0 mm 16

T2 FRFSE-XL Fat
Axial Saturation Spin Echo Yes 90 2100 n/a 4mm 0 mm 16
Figure 1: Imaging algorithm for appendicitis in a gravid
patient. A pregnant patient with right lower quadrant pain goes to
the ER. The surgeon comes to see the patient and suspects
appendicitis and orders an ultrasound. If the ultrasound is positive
the patient goes for appendectomy. If the ultrasound is
indeterminate then the next most appropriate imaging modality is
MRI.
Figure 2. Graphic illustration of the gradual superior
displacement of the cecum and appendix as a pregnancy
progresses.
(T = Trimester)
Figure 3: Normal appendix in a gravid patient. Axial T2 image
demonstrates the proximal portion of the normal appendix in long
axis section (arrow). Note the small caliber and how the signal of
the appendiceal wall parallels that of the adjacent cecum. Note
the adjacent gravid uterus (arrowheads).
Figure 4: Normal appendix. Axial T1 image demonstrates the
normal appendix in cross section (arrow). Note the small caliber
and how the signal parallels that of the adjacent cecum.
Figure 5. Acute appendicitis in a 37 year old gravid female
presenting with right lower quadrant pain. A. Axial T2 fat
saturated demonstrates the appendix (arrow) in cross section with
a low signal intensity wall and fluid filled high signal intensity
lumen with surrounding high signal inflammatory change
(arrowhead). Note the gravid uterus (*) B. Sagital T2 non fat
saturated images again demonstrates the appendix (arrows), this
time in long axis profile with a low signal wall and high signal
lumen. Note that the inflammatory change so easily seen in “A”
blends into the fat signal surrounding the appendix in “B” and that
the wall of the appendix although of low signal intensity relative to
the adjacent fat demonstrates higher signal than that of the
adjacent colon.
A B

*
Figure 6. Appendicitis in a gravid patient on fat saturated T2
weighted image. Axial T2 SSFSE fat saturated image
demonstrates the dilated fluid filled appendix (arrows) as well as
adjacent fluid and inflammatory change (arrow heads). Note the
adjacent gravid uterus(*).
*
Figure 7. Appendicitis in a gravid patient on STIR. Axial STIR
image in a gravid patient with appendicitis demonstrates both the
appendix (arrow) and inflammation of the adjacent tissues
(arrowheads). Note the adjacent gravid uterus.