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Magnetic Resonance Imaging of Intestinal Necrosis in Preterm Infants

Elia F. Maalouf, MRCP*; Andrew Fagbemi, MRCP*; Philip J. Duggan, MRCP*;


Subramanyam Jayanthi, MRCS‡; Serena J. Counsell, DCR§; Helen J. Lewis, DCR§;
Alison M. Fletcher, DCR§; Kokila Lakhoo, FRCS‡; and A. David Edwards, FRCP*

ABSTRACT. Background and Objective. Noninvasive jury, usually ischemic; bacterial colonization of the
diagnosis of intestinal necrosis is important in planning gut; and the presence of high osmolality solutions,
surgery in preterm infants with necrotizing enterocolitis usually formula milk, within the gut lumen. NEC
(NEC). We aimed to assess the potential of magnetic usually involves the ileum and the proximal colon,
resonance imaging (MRI) for the diagnosis of intestinal but any part of the gastrointestinal tract may be
necrosis.
Study Participants and Methods. Abdominal MRI
affected.1 The diagnosis of NEC is based on clinical
scans were performed in a group of preterm infants with findings (abdominal distension, lethargy, gastroin-
suspected NEC and compared with surgical findings and testinal bleeding, abdominal wall erythema, and ac-
to MRI results in a group of control infants. In addition, idosis) and plain abdominal radiographic criteria (di-
MRI was performed in 2 preterm infants with suspected lated bowel loops, bowel-wall thickening, intramural
NEC who did not require surgery. gas, and portal venous gas).
Results. Six infants with a median birth weight of Despite appropriate medical treatment, surgical
1220 g (range, 760-1770 g) and median gestational age at intervention becomes necessary in 40% to 50% of
birth of 30 weeks (range, 28 –34 weeks) were studied at a cases of NEC. The ideal timing for surgery is after the
median postnatal age of 10 days (range, 4 –19 days). Four development of intestinal necrosis but before the
infants had a bubble-like appearance in part of the in-
testinal wall, intramural gas, and an abnormal fluid level
development of intestinal perforation.1,2 Noninvasive
within bowel lumen. At surgery, NEC was found in 5 diagnosis of intestinal necrosis is difficult1,3 and no
infants and sigmoid volvulus in 1. The site of the bubble- test has a high sensitivity.2
like appearance corresponded to the site of intestinal Preliminary experience with animal models4 –7 sug-
necrosis at surgery. Four control infants with a median gests that magnetic resonance imaging (MRI) may
birth weight of 1500 g (range, 730-2130 g) and a median have a role in the diagnosis of bowel ischemia. The
gestational age of 31 weeks (range, 26 –36 weeks) had aim of this pilot study was therefore to describe
abdominal MRI at a median postnatal age of 8 days abdominal MRI findings in NEC and to assess the
(range, 4 –70 days). None of the above findings were seen potential role of MRI as a safe, noninvasive tool in
in any control infant. The bubble-like appearance was the diagnosis of intestinal necrosis.
not seen in the 2 infants with suspected NEC who did not
require surgery. STUDY PARTICIPANTS AND METHODS
Conclusion. Abdominal MRI allows the noninvasive
diagnosis of bowel necrosis. This may aid the timing of Ethical approval for this study was given by the Hammersmith
Hospitals Research Ethics Committee and informed parental con-
surgical intervention in preterm infants with a clinical sent was obtained in each case. Preterm infants who had clinical
diagnosis of NEC. Pediatrics 2000;105:510 –514; gangrene, and radiologic signs suggestive of NEC and who subsequently
ischemia, MRI, necrotizing enterocolitis. underwent laparotomy were included in this study. The indica-
tions for surgical intervention were failure of medical treatment or
intestinal perforation. Abdominal MRI was obtained before and
ABBREVIATIONS. NEC, necrotizing enterocolitis; MRI, magnetic after operation and compared with surgical findings. The severity
resonance imaging; GA, gestational age; T1, longitudinal relax- of NEC was staged using clinical signs and criteria on plain
ation time; T2, transverse relaxation time; CT, computed tomog- abdominal radiographs (modified Bell criteria in which stage I is
raphy; CSE, conventional spin echo; FSE, fast spin echo. suspect, stage II is definite, and stage III is advanced NEC).8 The
presence and the site of intestinal necrosis was determined at
laparotomy.

N
ecrotizing enterocolitis (NEC) is the most A control group of preterm infants of similar gestational age
common surgical emergency in preterm in- (GA) and with no symptoms or signs suggestive of NEC were also
fants. It is generally believed to be secondary studied for comparison. In addition, MRI was performed in 2
infants with suspected NEC who responded to conservative med-
to several underlying factors including: intestinal in- ical treatment and did not require surgery.

From the Departments of *Paediatrics and ‡Surgery and Gastroenterology; MRI Acquisition
and §Robert Steiner Magnetic Resonance Unit and Medical Research Coun- Patients were scanned 2 to 3 hours before undergoing laparot-
cil Clinical Science Centre, Imperial College School of Medicine, Hammer- omy and as soon as practical afterward. MRI was performed using
smith Hospital, London, England. a 1-Tesla neonatal magnetic resonance system (Oxford Magnet
Received for publication Feb 22, 1999; accepted Jun 15, 1999. Technology, Oxford, UK/Picker, Cleveland, OH) located within
Reprint requests to (A.D.E.) Department of Paediatrics, Imperial College the neonatal intensive care unit. The magnet has a 380-mm bore
School of Medicine, Hammersmith Hospital Campus, Du Cane Road, Lon- length, which allows good access to the infant for monitoring and
don W12 ONN, England. E-mail: david.edwards@ic.uc.uk. ventilation during scanning. Full intensive care and monitoring
PEDIATRICS (ISSN 0031 4005). Copyright © 2000 by the American Acad- were continued during scanning as previously described.9 Longi-
emy of Pediatrics. tudinal relaxation time (T1)-weighted CSE and transverse relax-

510 PEDIATRICS Vol. 105 No. 3 March 2000


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TABLE 1. Pulse Sequence Parameters
Pulse Sequence TR, TE/TEeff, Slice Number of NSA Phase Echo Train Interecho
ms ms Thickness, Slices Matrix Length Spacing
mm
T1-weighted CSE 600 20 4/5 12 2 192 – –
T2-weighted FSE 2430 96 4/5 9 4 256 16 16
T2-weighted FSE 3000 208 4/5 9 4 256 16 16
NSA indicates number of signal acquisitions; TR, repetition time; TE, echo time; TEeff, effective echo time.

ation time (T2)-weighted FSE images in the coronal and transverse 1500 g (range, 730-2130 g) and a median GA of 31
planes were obtained in all infants. In addition, postcontrast T1- weeks (range, 26 –36 weeks) were scanned at a me-
weighted CSE images were obtained in the coronal and transverse
planes using intravenous dimeglumine gadopentetate (0.1 mmol/ dian postnatal age of 8 days (range, 4 –70 days). Two
kg) as a contrast agent. Control infants were scanned once without infants with a birth weight of 715 and 2006 g and a
the use of contrast agents. Infants with suspected NEC who did GA of 25 and 36 weeks were scanned at a postnatal
not require surgery were scanned within 48 hours of developing age of 49 and 4 days, respectively.
symptoms and signs suggestive of NEC. The sequence parameters
for T1-weighted CSE and T2-weighted FSE are summarized in
Table 1. Radiograph Findings
On plain abdominal radiography, all 6 infants who
MRI Analysis underwent surgery had dilated bowel loops and in-
The images were analyzed before surgery, and results were tramural gas; 5 had thickening of the bowel wall
compared with findings at laparotomy. Abnormal features re- (cases 1–5); 1 had air in the portal system (case 1);
corded were the presence or absence of bowel-wall thickening,
dilated bowel loops, intramural gas, abnormal fluid levels within and 2 had evidence of free intraperitoneal gas (cases
bowel lumen, mesenteric edema, and bubble-like appearance in 2 and 6). Plain radiographs were not obtained in the
parts of the intestinal wall. control infants. The 2 infants with suspected NEC
Bowel-wall thickening and bowel-loop dilatation were assessed who did not require surgery had generalized bowel
subjectively in comparison to control infants. Intramural gas ap-
peared as a line of low signal intensity within the bowel wall on
distension, dilated bowel loops, and intramural gas
T1- and T2-weighted images. Fluid levels within bowel lumen had on plain abdominal radiographs.
low signal intensity on T1-weighted images and high signal in-
tensity on T2-weighted images. Mesenteric edema had high signal Surgical Findings
intensity on T2-weighted images. Infants with a bubble-like ap-
pearance in parts of the intestinal wall had multiple small circular The diagnosis of NEC was surgically confirmed in
low-signal intensity lesions within the bowel wall giving a char- 5 of these infants (cases 1–5) but sigmoid volvulus
acteristic appearance on T2-weighted images. The site of bubble- with perforation was diagnosed intraoperatively in
like appearance of bowel was compared with the site of bowel the sixth (Fig 1) (case 6). Four of the infants with NEC
necrosis observed at surgery with the help of detailed diagrams of
operative findings. (cases 1– 4) had nonviable necrotic bowel and re-
quired bowel resection and exteriorization. Bowel
RESULTS necrosis was subsequently confirmed on histologic
Six infants suspected of having NEC with a me- examination. The fifth infant with NEC (case 5) had
dian birth weight of 1220 g (range, 760-1770 g) and a dusky but nonnecrotic bowel and did not require
median GA of 30 weeks (range, 28 –34 weeks) were bowel resection or exteriorization. The infant with
included in the study. Prelaparotomy MRI scans volvulus had healthy looking bowel. Table 2 sum-
were acquired at a median postnatal age of 10 days marizes the surgical findings.
(range, 4 –19 days) and postlaparotomy MRI scans
were acquired at a median of 8 days (range, 5–19 MRI Findings
days) after surgery. Table 2 summarizes the clinical Figure 2 summarizes pre- and postoperative MRI
details and the timing of the MRI scans in all cases. findings in the 6 infants who required surgery. Pre-
Four control infants with a median birth weight of operative MRI was less motion artifacted in all in-

TABLE 2. Clinical Details and Timing of MRI in Infants Who Required Surgery
Infant Birth GA, Sex Postnatal Age Postnatal Age Bell Operative Findings
Weight, Weeks at Pre-op at Post-op Stage8
g MRI, days MRI, days
1 1415 30 M 7 15 III NEC with necrosis of small and
large bowel. Bowel resection.
2 1058 29 F 15 24 III NEC with necrosis of small and
large bowel. Bowel resection.
3 760 33 F 4 23 III NEC with necrosis of small and
large bowel. Bowel resection.
4 1770 34 F 14 26 III NEC with necrosis of small and
large bowel. Bowel resection.
5 1038 28 M 7 12 III NEC with dusky large bowel.
Bowel viable, no resection.
6 1050 31 M 19 25 II Sigmoid volvulus with bands.
Bowel viable, no resection.
M indicates male; F, female.

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had persistence of either bowel-wall thickening, mes-
enteric edema, and/or dilated bowel loops. The 2
infants scanned on postoperative days 12 and 19 did
not have any of the above findings. There was no
correlation between bowel wall enhancement on
postcontrast T1-weighted images and sites of bowel
necrosis.
MRI scans obtained in control infants showed mo-
tion artifact secondary to bowel peristalsis. These
infants did not have dilated bowel loops, bowel-wall
thickening, abnormal fluid levels within bowel lu-
men, mesenteric edema, or any of the other findings
described above.
MRI scans obtained in the 2 infants with suspected
NEC who did not require surgery showed dilated
and thickened bowel loops with mesenteric edema.
There was no fluid level seen within the bowel lu-
men, no intramural gas, and no bubble-like appear-
ance in any part of the intestine.

DISCUSSION
Fig 1. Infant with volvulus born at 31 weeks’ gestation and im- We have described the abdominal MRI findings in
aged at a postnatal age of 19 days (case 6). Transverse relaxation a small group of preterm infants with clinical suspi-
time-weighted FSE (repetition time, 3000 ms; echo time, 208 ms) cion of NEC who underwent surgery, compared
transverse image showing dilated bowel loops but there is no those to a group of control infants and to 2 infants
bubble-like appearance of the bowel wall and no abnormal fluid
level within bowel lumen. with NEC who were treated medically. We have
showed that the imaging appearances and in partic-
ular the sites of abnormality were closely related to
fants with NEC compared with postoperative studies perioperative findings.
and control infants’ MRI. All findings described were The noninvasive diagnosis of bowel necrosis,
seen on both transverse and coronal planes. which is the main indication for surgical intervention
On preoperative MRI dilated bowel loops, mesen- in preterm infants with NEC in the absence of pneu-
teric edema and thick bowel wall were present in all moperitoneum, has proved to be difficult.1–3 Plain
6 infants. In addition to the above findings, the 4 abdominal radiographic features such as portal ve-
infants who required bowel resection had an abnor- nous gas and fixed intestinal loops; and laboratory
mal fluid level within bowel lumen, intramural gas, markers such as white blood cell count, immature to
and a bubble-like appearance in parts of the intesti- total neutrophil ratio, platelet count, and base excess
nal wall (Figs 3–5). The site of the bubble-like appear- have all been used to assist in the timing of surgery
ance on MRI corresponded well to the site of intes- but none of these tests has a high sensitivity.2,3
tinal necrosis at surgery. Abdominal ultrasound scanning with Doppler has
Postoperative MRI showed resolution of the ab- been used to diagnose bowel necrosis without per-
normal fluid level within bowel lumen, the intramu- foration but different reports give conflicting assess-
ral gas, and the bubble-like appearance of the intes- ments of its value in differentiating necrotic from
tine in all 4 infants with necrotic bowel. Infants inflammatory bowel changes.10,11
scanned between postoperative day 5 and day 9 still Computed tomography (CT) findings of thickened

Fig 2. Surgical diagnosis, preoperative and postoperative magnetic resonance imaging findings in infants who required surgery.
Abbreviations: MRI, magnetic resonance imaging; pre, preoperative MRI findings; post, postoperative MRI findings. W indicates present.
³ indicates absent.

512 MAGNETIC RESONANCE IMAGING OF NECROTIZING ENTEROCOLITIS


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Fig 3. Infant with necrotizing enterocolitis born at 33 weeks’ gestation and imaged at a postnatal age of 4 days (case 3). A, coronal
transverse relaxation time-weighted fast spin echo (repetition time, 3000 ms; echo time, 208 ms) image showing the bubble-like
appearance in the intestinal wall (arrows). B, transverse relaxation time-weighted fast spin echo (repetition time, 3000 ms; echo time, 208
ms) image showing intramural gas (short arrow) and an abnormal fluid level within bowel lumen (long arrow).

Fig 4. Infant with necrotizing enterocolitis born at 30 weeks’ gestation and imaged at a postnatal age of 7 days (case 1). A, transverse
relaxation time-weighted fast spin echo (repetition time, 3000 ms; echo time, 208 ms) image showing a bubble-like appearance within
bowel wall (arrows). B, transverse relaxation time-weighted fast spin echo (repetition time, 3000 ms; echo time, 208 ms) image showing
mesenteric edema (long arrow) and thickened bowel wall (short arrow).

bowel wall with postcontrast enhancement, dilated ratory and peristaltic motion. Infants with NEC or
fluid filled bowel, intramural gas, and intramural sigmoid volvulus tend to have an ileus as part of
low attenuation zones have been described in adults their illness and therefore the preoperative MRI ob-
with bowel ischemia12–14 but the use of CT in preterm tained from study infants showed very little motion
infants with NEC has not yet been reported. A spe- artifact.
cific CT finding for bowel necrosis in adults is intes- MRI has been used in the diagnosis of early and
tinal pneumatosis which may be seen as cyst-like late intestinal ischemia in several animal models.4 –7
collections of gas in the bowel mucosa.13 The appear- High signal intensity on T2-weighted and isointense
ance of bubble-like collections of gas on CT have also or slightly increased signal intensity on T1-weighted
been described in adults with Fournier’s gangrene.15 images was reported early (within 45 minutes) after
The development of MRI in the abdomen has been an ischemic insult.5,6 High signal intensity on both
impeded by motion artifact secondary to both respi- T1- and T2-weighted images was reported late (24

ARTICLES 513
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diographs in 85% of cases of NEC and is not indica-
tive of bowel necrosis.1 An abnormal fluid level
within bowel lumen has been described as a CT
finding in bowel ischemia in adults12–14 but is not a
specific sign of bowel necrosis.

CONCLUSION
In summary, dilatation of bowel loops, thickening of
bowel wall, and mesenteric edema are nonspecific MRI
findings and may be present in all infants with NEC.
The additional findings of fluid level within the bowel
lumen, intramural gas, and in particular bubble-like
appearance in parts of the intestinal wall on MRI are
highly suggestive of the presence of intestinal necrosis.
These results suggest that MRI is likely to be of
value in diagnosing intestinal necrosis and determin-
ing the need for surgical intervention. MRI may also
be of value in other intestinal conditions where gut
necrosis is a feature. We suggest that further studies
to determine the value of MRI in the diagnosis of
intestinal necrosis are warranted.
Fig 5. Infant with necrotizing enterocolitis born at 34 weeks’ ges-
tation and imaged at a postnatal age of 14 days (case 4). A, ACKNOWLEDGMENTS
transverse relaxation time-weighted fast spin echo (repetition
time, 3000 ms; echo time, 208 ms) image showing a bubble-like This work was supported by Wellbeing, the Medical Research
appearance of the intestinal wall (arrow). Council, the Garfield Weston Foundation, Picker International,
and Oxford Magnet Technology.
We thank Professor G. M. Bydder for his support and his help
in interpreting the magnetic resonance images.
hours) after an ischemic insult.4 Postcontrast enhance-
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514 MAGNETIC RESONANCE IMAGING OF NECROTIZING ENTEROCOLITIS


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Magnetic Resonance Imaging of Intestinal Necrosis in Preterm Infants
Elia F. Maalouf, Andrew Fagbemi, Philip J. Duggan, Subramanyam Jayanthi,
MRCS?; Serena J. Counsell, Helen J. Lewis, Alison M. Fletcher, Kokila Lakhoo and
FRCS?; and A. David Edwards
Pediatrics 2000;105;510
DOI: 10.1542/peds.105.3.510

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Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it
has been published continuously since . Pediatrics is owned, published, and trademarked by the
American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois,
60007. Copyright © 2000 by the American Academy of Pediatrics. All rights reserved. Print ISSN:
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Magnetic Resonance Imaging of Intestinal Necrosis in Preterm Infants
Elia F. Maalouf, Andrew Fagbemi, Philip J. Duggan, Subramanyam Jayanthi,
MRCS?; Serena J. Counsell, Helen J. Lewis, Alison M. Fletcher, Kokila Lakhoo and
FRCS?; and A. David Edwards
Pediatrics 2000;105;510
DOI: 10.1542/peds.105.3.510

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://pediatrics.aappublications.org/content/105/3/510

Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it
has been published continuously since . Pediatrics is owned, published, and trademarked by the
American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois,
60007. Copyright © 2000 by the American Academy of Pediatrics. All rights reserved. Print ISSN:
.

Downloaded from http://pediatrics.aappublications.org/ by guest on February 2, 2018

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