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Outcome of infants presenting with echogenic bowel in the second trimester

of pregnancy

Article  in  Archives of Disease in Childhood - Fetal and Neonatal Edition · September 2012

DOI: 10.1136/archdischild-2012-302017 · Source: PubMed

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Original article
1
Division of Neonatology,
Beatrix Children’s Hospital,
University of Groningen,
University Medical Center
Groningen, Groningen,
The Netherlands
2 marker, incidentally seen on second trimester
Fetal Medicine Unit,
Department of Obstetrics and
Gynecology, University of
Groningen, University Medical
Center Groningen, Groningen,
The Netherlands
3 for foetal echogenic bowel vary a lot, it is
Department of Genetics,
University of Groningen,
University Medical Center
Groningen, Groningen,
The Netherlands
4
Department of Surgery,
University of Groningen,
University Medical Center
Groningen, Groningen,
The Netherlands
Correspondence to
Hannah Buiter, Division of
Neonatology, Beatrix Children’s
Hospital, University of
Groningen, University Medical
Center Groningen, P.O. Box
30.001, Groningen 9700 RB,
The Netherlands;
h.d.buiter@umcg.nl
Accepted 31 July 2012
Published Online First
18 September 2012
To cite: Buiter HD,
Holswilder-Olde
Scholtenhuis MAG,
Bouman K, et al. Arch Dis
Child Fetal Neonatal Ed
2013;98:F256–F259.
F256
Downloaded from http://fn.bmj.com/ on December 23, 2014 - Published by group.bmj.com
Outcome of infants presenting with echogenic
bowel in the second trimester of pregnancy
Hannah D Buiter,1 Marloes A G Holswilder-Olde Scholtenhuis,2 Katelijne Bouman,3
Robertine van Baren,4 Caterina M Bilardo,2 Arend F Bos1
ABSTRACT
Objective Fetal echogenic bowel (FEB) is a soft marker
found on second trimester sonography. Our main aim was
to determine the outcome of infants who presented with
FEB and secondarily to identify additional sonographic
findings that might have clinical relevance for the
prognosis.
Design We reviewed all pregnancies in which the
diagnosis FEB was made in our Fetal Medicine Unit during
2009–2010 (N=121). We divided all cases into five groups
according to additional sonographic findings. Group 1
consisted of cases of isolated FEB, group 2 of FEB
associated with dilated bowels, group 3 of FEB with one
or two other soft markers, group 4 of FEB with major
congenital anomalies or three or more other soft markers,
and group 5 consisted of FEB with isolated intrauterine
growth restriction (IUGR).
Results Of 121 cases, five were lost to follow-up. Of the
remaining 116 cases, 48 (41.4%) were assigned to group
1, 15 (12.9%) to group 2, 15 (12.9%) to group 3, 27
(23.2%) to group 4, and 11 (9.5%) to group 5. The
outcome for group 1 was uneventful. In group 2 and 3,
two anomalies, anorectal malformation and cystic fibrosis,
were detected postnatally (6.7%). In group 4, mortality
and morbidity were high (78% resp. 22%). Group 5 also
had high mortality (82%) and major morbidity (18%).
Conclusions If FEB occurs in isolation, it is a benign
condition carrying a favourable prognosis. If multiple
additional anomalies or early IUGR are observed, the
prognosis tends to be less favourable to extremely poor.
It has become common practice in prenatal care to
do a foetal anatomy survey during the second trimes-
ter of pregnancy, between 18 and 22 weeks of gesta-
tion. Besides structural anomalies, a number of subtle
sonographic variants, the so-called soft markers, are
observed. The clinical relevance of these soft markers
is not always clear. To establish their association with
other structural anomalies and with aneuploidies,
large prospective studies on general populations are
needed. One of these soft markers is foetal echogenic
bowel (FEB), with a prevalence of 0.2%–1.8% in the
general population.1–4
FEB is defined as increased echogenicity or
brightness of the foetal bowel on sonography. The
brightness can be graded by comparing the echo-
genicity of the bowel with the brightness of the
foetal iliac wing or liver.2 3 During the third trimes-
ter, meconium can be present in the bowel of a
normal foetus. At this stage of pregnancy, FEB is
regarded as a normal sonographic finding. In the
second trimester, FEB may be transient, bearing no
clinical significance at all.5–7 It could, however, also
be a sign of underlying pathology.4 8
Buiter HD, et al. Arch Dis Child Fetal Neonatal Ed 2013;98:F256–F259. doi:10.1136/archdischild-2012-302017
What is already known on this topic
▸ Foetal echogenic bowel is a so-called soft
sonography.
▸ It may be caused by different underlying
diseases or bear no clinical significance at all.
▸ Since clinical importance and underlying causes
difficult to counsel parents appropriately.
What this study adds
▸ The majority of foetuses with foetal echogenic
bowel (FEB) carry a good prognosis.
▸ Additional sonographic findings may help to
predict outcome.
▸ FEB with other soft markers, major anomalies
or early intrauterine growth restriction bears a
less favourable to extremely poor prognosis.
As yet, limited data are available on the outcome
of pregnancies complicated by FEB in the second
trimester of pregnancy. Most studies were per-
formed in selected populations. It is also unknown
to what extent additional sonographic findings
could help predict outcome in these pregnancies.
The main aim of this study was, therefore, to
determine the outcome of all cases of FEB detected
in an unselected population of pregnant woman
referred to our Foetal Medicine Unit (FMU) after
routine second trimester sonography. Our second-
ary aim was to identify additional sonographic find-
ings with clinical relevance for the prognosis.
METHODS
Retrospectively, we included all cases of second tri-
mester ultrasound diagnoses of FEB recorded in our
FMU between January 2009 and December 2010.
FEB was diagnosed either at our unit or in women
referred to us from elsewhere. Our FMU acts as refer-
ral centre for a large area. All cases of suspected
anomalies are referred to FMU from other ultra-
sound clinics or level-II hospitals for confirmation of
diagnosis and further management. Diagnosis of FEB
was confirmed in our FMU on a second ultrasound
examination between week 18 and 24 of gestation.
Our FMU is similar to those of other level-III peri-
natal centres in The Netherlands.
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The ultrasound examinations were performed with a Voluson
730 (GE Healthcare, Waukesha, Wisconsin, USA) ultrasound
device with an AB 2-7, 4 MHz sector transducer or RAB 4-8,
4.5 MHz transducer. The foetus was thoroughly investigated for
congenital anomalies or sonomarkers. In addition, we noted
foetal biometry, placental position and amniotic fluid volume.
The diagnosis of FEB was made on the basis of bowel echogeni-
city similar to or greater than surrounding foetal bone (grade II
to III as described by Slotnick and Abuhamad).2
Each case of FEB was discussed in a multidisciplinary meeting
with a neonatologist, clinical geneticist and other paediatric specia-
lists, after which the women were counselled by the foetal medi-
cine specialist. We offered them additional investigations according
to a local protocol including amniocentesis for karyotyping, paren-
tal DNA cystic fibrosis testing and maternal serological infection
screening for toxoplasmosis, rubella, cytomegalovirus, herpes
simplex virus and parvovirus B19. Screening for cystic fibrosis was
based on DNA screening for any mutations in the cystic fibrosis
transmembrane regulator gene. Where indicated, scans were
repeated serially during pregnancy. All data concerning the pres-
ence of other major and minor foetal abnormalities on sonog-
raphy, the results of the additional investigations, maternal past
obstetric history, comorbidity, pregnancy-related complications
and outcome of the pregnancy (in terms of mortality, morbidity
and final diagnosis) were collected in a clinical computerised data-
base. Intrauterine growth restriction (IUGR) was defined as an
abdominal circumference below the 5th percentile.
Based on previous reports in literature, regarding aetiology of
FEB and additional sonographic findings, we categorised all
cases of FEB into five groups. Group 1 consisted of cases with
isolated FEB; group 2 of FEB with dilated bowels; group 3 of
FEB with one or two other sonographic soft markers; group 4
of cases with FEB associated with major congenital anomalies or
three or more other soft markers; and group 5 consisted of FEB
within the setting of isolated IUGR.
Data on neonatal outcome were collected post partum from
mid-wives, hospitals where the women had delivered and neonatal
departments. We recorded birth weight, gestational age at birth,
presence of bowel or other abdominal abnormalities, meconium
passage, congenital malformations, perinatal morbidity, and mor-
tality. We also noted whether birth weight was below the 5th per-
centile for the Dutch population (http://www.perinatreg.nl).
RESULTS
During the 2-year study period we collected 121 pregnancies
with FEB diagnosed on second trimester sonography; five cases
were lost to follow-up and excluded from analysis, leaving us
with 116 pregnancies.
Table 1 Outcome in terms of morbidity and mortality in groups with FEB and various additional sonographic abnormalities
Outcome n (%)
Group number with additional No morbidity or Minor
sonographic abnormalities n mortality morbidity
1. Isolated FEB 48 45 (93.7%) 3 (6.3%)
2. FEB+dilated bowel 15 14 (93.3%) – 1 (6.7%)
3. FEB+≤2 soft markers 15 12 (80%) 2 (13.3%)
4. FEB+major abnormalities or >2 soft 27 – –
markers
5. FEB+IUGR 11 – 1 (9.1%)
Total 116 71 (61.2%) 6 (5.2%)
FEB, foetal echogenic bowel; IUGR, intrauterine growth restriction.
Buiter HD, et al. Arch Dis Child Fetal Neonatal Ed 2013;98:F256–F259. doi:10.1136/archdischild-2012-302017
Original article
In table 1 we present the distribution of FEB among the five
groups in relation to outcome in terms of morbidity and
mortality.
Of 116 pregnancies, we diagnosed 48 (41.4%) as belonging
to group 1, isolated FEB; that is, FEB without any other sono-
graphic abnormalities or IUGR. These pregnancies were all
uneventful. At birth, two infants were small for gestational age,
while foetal biometry in the second trimester had been normal.
One foetus in this group was diagnosed antenatally with a
parvovirus infection, but it showed no abnormalities after birth.
We diagnosed 15 (12.9%) pregnancies as belonging to
group 2, FEB with dilated bowel. In one of these infants, a rec-
toperineal fistula (type of anorectal malformation) was diag-
nosed after birth. In this group, we found no other
abnormalities in either antenatal tests or in postpartum examina-
tions. There were no mortalities in this group.
Another 15 (12.9%) pregnancies belonged to group 3. In
these cases, we found one or two additional minor abnormal-
ities next to FEB that could be classified as soft markers, that is,
thickened nuchal fold, rhizomelic limb shortening, mild foetal
pyelectasis, echogenic intracardiac focus or choroid plexus cyst.
In this group, two infants were born small for gestational age,
despite normal foetal biometry in the second trimester. One
infant presented with failure to thrive several months after birth
and was diagnosed with cystic fibrosis. In this particular case,
pyelectasia and FEB were present on antenatal sonography. The
parents had not opted for antenatal parental DNA cystic fibrosis
testing.
Of 116 pregnancies, 27 (23.2%) belonged to group 4, FEB
associated with other major anomalies or three or more add-
itional soft markers detected on sonography. Karyotyping was
performed antenatally in 25 of these 27 pregnancies. There
were 13 pregnancies (11.2% of all 116 cases) with chromosomal
abnormalities, all diagnosed antenatally. These cases included
four cases of trisomy 21, one monosomy 21, one trisomy 18,
two cases of trisomy 13, and one Turner syndrome. Four cases
had various chromosomal unbalanced translocations. Pregnancy
was terminated in nine of the 13 cases.
Of the 27 pregnancies in group 4, FEB with major malforma-
tions, 14 foetuses (12.1% of all 116 cases) had a variety of
underlying pathologies. These included two foetuses with con-
genital heart defects, two with gastroschisis, hydrops associated
with a placental chorangioma in one foetus and nine foetuses
with multiple congenital anomalies. Most of the major malfor-
mations consisted of cerebral anomalies (Dandy–Walker malfor-
mation, meningomyelocele and hydrocephalus), heart defects,
orofacial clefts or urological malformations. In this group of
FEB with major sonographic abnormalities, high rates of mortal-
ity and major morbidity occurred.
Major Perinatal Termination of Foetal
morbidity mortality pregnancy demise
– – – –
– – –
1 (6.7%) – – –
6 (22.2%) 4 (14.8%) 15 (55.6%) 2 (7.4%)
1 (9.1%) 2 (18.2%) 1 (9.1%) 6 (54.5%)
9 (7.7%) 6 (5.2%) 16 (13.8%) 8 (6.9%)
F257
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Original article
Of 116 pregnancies, we diagnosed 11 (9.5%) cases as belong-
ing to group 5, FEB and IUGR in the absence of other major
abnormalities. This led to a high rate of foetal deaths (seven out
of 11) and two live-born infants died soon after preterm birth.
Only two infants in this group survived; both were born
preterm and growth retarded. In all these early IUGR cases,
pregnancies were eventually complicated by placental insuffi-
ciency and/or haemolysis, elevated liver enzymes, low platelets
(HELLP) syndrome in the mother. Placenta pathological exam-
ination was performed in nine of the 11 cases. These nine pla-
centas were all hypoplastic, six of them with infarctions and
signs of ischaemia. One had a subchorial haematoma, apart
from the small placenta.
With regard to the additional investigations offered ante-
natally, 37 (31.9%) of parents were screened for cystic fibrosis
mutations, 73 (62.9%) of mothers were screened for infection
and in 46 (39.7%) cases we performed amniocentesis for foetal
karyotyping. This led to antenatal diagnoses in 39 (33.6%) of
cases. Of the 48 cases in group 1, isolated FEB, 45 (93.7%) had
no pathological abnormalities post partum. Apart from four
small for gestational age infants and the one infant with cystic
fibrosis, no additional diagnoses were made after birth.
Table 2 shows all FEB diagnoses, both antenatally and post
partum, for our cohort of pregnancies. Of all 116 pregnancies
with FEB, we found 71 (61.2%) without any pathology.
Pregnancies complicated by FEB and additional soft markers,
major anomalies or early IUGR had a significant increased risk
for poor outcome, for example, death or major morbidity, as
opposed to pregnancies with isolated FEB or FEB and bowel
dilatation (OR 157.1; 95% CI 19.9 to 1237.4; p<0.001).
DISCUSSION
First, this study demonstrated that the majority of foetuses with
FEB had no underlying diseases and they had a good prognosis.
This is especially true for the group with isolated FEB. The
prognosis was only slightly less favourable if FEB was associated
with dilated bowels, or with one or two other soft markers. Of
the total of 30 cases in groups 2 and 3, only 6.7% had under-
lying pathology, and no deaths occurred in these two groups. If
FEB was associated with major anomalies, three or more add-
itional soft markers, or with early IUGR, the prognosis was
extremely poor, with death rates of approximately 80%. Our
study was striking in that the number and nature of additional
sonographic abnormalities clearly differentiated between favour-
able and poor outcome.
Our study showed that FEB with major anomalies or three or
more soft markers on sonography suggested chromosomal
Table 2 Final diagnoses in the whole cohort
Diagnosis already made
Final diagnosis n (%) during pregnancy
No pathology 71 (61.2)
Small for gestational age/ 15 (12.9) 11
intrauterine growth restriction
Major/multiple congenital 14 (12.1) 14
malformations
Chromosomal abnormality 13 (11.2) 13
Cystic fibrosis 1 (0.9) – subjectivity.2 4 21 We also took great care to use the proper
Gastrointestinal obstruction 1 (0.9) – transducer frequency. A transducer frequency of more than
Congenital foetal infection 1 (0.9) 1 5 MHz could lead to an overdiagnosis of FEB. Another limita-
Total 116 (100) 39
F258 Buiter HD, et al. Arch Dis Child Fetal Neonatal Ed 2013;98:F256–F259. doi:10.1136/archdischild-2012-302017
abnormalities or major congenital anomalies. These underlying
pathologies are probably associated with the poor outcome in
this group of FEB.
FEB with early IUGR is thought to be the result of early pla-
cental insufficiency due to pre-eclampsia and/or early HELPP
syndrome. This resulted in high rates of foetal demise or peri-
natal death, the latter after elective very preterm birth in case
the pregnancy had reached a gestational age beyond the limit of
potential neonatal survival. Although the exact pathophysio-
logical cause of FEB was probably multifactorial, it remained
unclear in many instances. In case of early IUGR, it is speculated
to be caused by either oedema of the intestinal wall or by an
abnormal characteristic of meconium inside the small bowel due
to impaired circulation of the intestines. This is a complex area
with probable links among FEB, uteroplacental insufficiency and
functional intestinal obstruction.9–11 In our IUGR cases, we
found placental lesions consistent with uteroplacental insuffi-
ciency, that is, hypoplasia of the placenta. These findings are in
line with the hypothesis that placental insufficiency is related to
early IUGR and FEB.
We compared our findings to the international literature
regarding FEB. In their review, Carcopino et al summarised
several studies published between 1992 and 2003.12 Their data
showed that incidences of underlying diseases vary considerably
between studies. Most of the reviewed studies dated prior to
2000. We found seven more recent articles reporting on
outcome in FEB-complicated pregnancies.4 8 13–17 Data of these
recent studies, together with the data of the review of
Carcopino et al, are shown in table 3. Prevalence rates in these
studies varied as much as reported by Carcopino et al.
Incidence of antenatal testing and population background differ-
ences may be the underlying cause of these variations. Taking
into account these differences in study population, study design,
and inclusion and exclusion criteria, we conclude that our
prevalence of different pathology of FEB did not differ substan-
tially from previous reports.
The strength of this study is that our cohort was population-
based and derived from a large referral region in the north of The
Netherlands. Considering the outcome of all FEB-complicated
pregnancies and the value of additional sonographic findings, we
lost only 4.1% (5 out of 121) cases in follow-up. A remarkable
finding was that in our investigation all cases with underlying
chromosomal abnormalities also had other major malformations
or three or more other soft markers on sonography. This is in con-
flict with data from Snijders et al and Strocker et al. Even in iso-
lated FEB they found a prevalence of chromosomal defects of
6%.18 19 Since the study was performed more than 10 years ago, it
is possible that improved sonographic techniques in our study led
to improved recognition of soft markers or subtle anomalies.
Another explanation is that selection bias might play a role.
Snijders et al studied a high risk population, whereas our study
was performed on cases selected on the basis of abnormal findings
on routine ultrasound screening.
We also recognise some limitations to our study. The diagno-
sis of FEB is prone to subjectivity since it is based on the
grading of echogenicity.20 We tried solving this by using an
objective definition of FEB based on echogenicity of bowel at
least as bright as the adjacent iliac wing. We refrained from
scoring different grades of echogenicity to reduce the effect of
tion was the retrospective nature of our study; we might have
missed cases.
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Original article

Table 3 Foetal echogenic bowel and outcome, review of literature from 2004 onwards
Author and year Population and No Congenital Intrauterine GI tract Chromosomal Major
of study n period pathology CF infection growth restriction malformation abnormality malformations

Carcopino12 2007 1682 Review of 11 * 2% 3% 6% * 7% *

articles, 1992–2003
Patel17 2004 109 Local population, * 2% * * * 1% 1%
1994–2000
Aboujaoude15 2006 65 Referral population, * 0% 0% 2% * 2% 2%
2004–2005,†
Scotet16 2010 289 1992–2007‡ 68% 8% 4% * 7% 4% *
Iruretagoyena13 56 Referral population, 78% 0% 2% * * 7% 7%
2010 2005–2008
Goetzinger4 2011 260 Referral population, 57% 2% 2% 19% * 7% 16%
1990–2008
Ameratunga8 2012 63 Referral population, 67% 2% 10% 6% * 8% 6%
2004–2009
Saha14 2012 139 Referral population, * 0% 1% 20% 1% 4% *
2005–2010
Present study 2012 116 Referral population, 61% 1% 1% 13% 1% 11% 12%
2009–2010
*Unknown, not reported in article. †Only African American or Hispanic patients. ‡Population from Brittany, France referred for analysis of cystic fibrosis transmembrane regulator gene
analysis with foetal echogenic bowel. CF, cystic fibrosis; GI, gastrointestinal.

Our study may have immediate implications for foetal health-
care. In all groups with FEB, sonographic follow-up and a post-
partum physical examination by the paediatrician is necessary.
Furthermore, a serological test for infections can be easily per-
formed since these examinations bear no risks for the foetus.
This also applies to CF carrier screening, although parents
should be aware that if one mutation is detected in one of the
parents, CF cannot be excluded. This study, however, found no
major congenital anomalies or chromosomal abnormalities in
the children born with FEB without major sonographic abnor-
malities or more than three soft markers. Therefore, amniocen-
tesis for karyotyping in pregnancies with FEB should not be
offered in all cases, but be reserved for those cases with other
major anomalies or additional soft markers. As FEB associated
with early IUGR has a poor prognosis, these pregnancies
warrant close observation since they are often complicated by
pre-eclampsia or HELLP syndrome later on.
In conclusion, in pregnancies complicated by FEB, additional
sonographic findings may help to determine prognosis. In the
majority of cases with FEB, FEB is isolated and carries a favour-
able prognosis. Isolated FEB in association with early IUGR has
a high perinatal mortality. FEB in the presence of multiple soft
markers or major congenital anomalies was associated with
chromosomal abnormalities or major anomalies and carries a
poor prognosis. These findings may help to stimulate the
correct use of diagnostic tools and appropriate counselling of
parents during pregnancy.
Acknowledgements We acknowledge the help of Dr T Palthe for correcting the
English manuscript.
Contributors HDB was the main author of this paper, was responsible for the
design of this study and analysis of the data. She completed the first draft.
MAGH-OS was responsible for the design of this study and analysis of the data. KB
and RvB helped to revise the article critically. CMB helped with the interpretation of
the data. She revised the article critically for important intellectual content. AB was
involved in the conception and design of this study, interpretation of the data and
helped with the draft and revisions of this paper.
Competing interests None.
Ethics approval Provided by the Medical Ethical Committee University Medical
Center Groningen.
Provenance and peer review Not commissioned; externally peer reviewed.
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Buiter HD, et al. Arch Dis Child Fetal Neonatal Ed 2013;98:F256–F259. doi:10.1136/archdischild-2012-302017 F259
 Downloaded from http://fn.bmj.com/ on December 23, 2014 - Published by group.bmj.com

Outcome of infants presenting with

echogenic bowel in the second trimester of
pregnancy
Hannah D Buiter, Marloes A G Holswilder-Olde Scholtenhuis, Katelijne
Bouman, Robertine van Baren, Caterina M Bilardo and Arend F Bos

Arch Dis Child Fetal Neonatal Ed 2013 98: F256-F259 originally

published online September 18, 2012
doi: 10.1136/archdischild-2012-302017

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Topic Articles on similar topics can be found in the following collections

Collections Epidemiologic studies (843)
Pregnancy (1473)
Reproductive medicine (1389)
Cystic fibrosis (15)
Pancreas and biliary tract (53)

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