Segmental dilatation of colon detected on prenatal ultrasound

Accepted Manuscript Segmental dilatation of colon detected on prenatal ultrasound Naoko Uga, Tatsuya Suzuki, Kouhei Sakurai, Tetsuya Tsukamoto, Tomonori Tuchiya, Yasuhiro Kondo, Atsuki Naoe, Shunsuke Watanabe, Toshihiro Yasui, Fujio Hara PII:

S2213-5766(19)30089-2

DOI:

https://doi.org/10.1016/j.epsc.2019.101208

Article Number: 101208 Reference:

EPSC 101208

To appear in:

Journal of Pediatric Surgery Case Reports

Received Date: 25 March 2019 Accepted Date: 7 April 2019

Please cite this article as: Uga N, Suzuki T, Sakurai K, Tsukamoto T, Tuchiya T, Kondo Y, Naoe A, Watanabe S, Yasui T, Hara F, Segmental dilatation of colon detected on prenatal ultrasound, Journal of Pediatric Surgery Case Reports (2019), doi: https://doi.org/10.1016/j.epsc.2019.101208. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT

Title Segmental dilatation of colon detected on prenatal ultrasound Naoko Uga1, Tatsuya Suzuki1, Kouhei Sakurai2, Tetsuya Tsukamoto2, Tomonori

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Tuchiya1, Yasuhiro Kondo1, Atsuki Naoe1, Shunsuke Watanabe1, Toshihiro Yasui1, Fujio Hara1 1

Department of Pediatric Surgery, Fujita Health University School of Medicine, Aichi,

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Japan

Department of Diagnostic Pathology, Fujita Health University School of Medicine,

Corresponding author: Naoko Uga, M.D.

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Aichi, Japan

Department of Pediatric Surgery, Fujita Health University School of Medicine, 1-98, Dengakugakubo, Kutsukake-cho, Toyoake, Aichi 470-1192, Japan phone number: +81-562-93-2000 (ext. 9247)

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fax number: +81-562-93-1951

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e-mail: [email protected]

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ACCEPTED MANUSCRIPT Abstract Segmental dilatation of the colon is a rare condition in which there is an abrupt segment of dilated colon between regions of normal colon, without obstruction. The condition causes bilious vomiting and abdominal distention in the neonate, and causes constipation or anemia in infants and adults. We herein report a case of segmental dilatation of the descending colon detected on prenatal developed

constipation

and

enterocolitis.

At

1

year

of

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sonography. The patient was born at 39 weeks’ gestation, weighing 3720 g. At 10 months, he age,

the

patient

underwent

laparoscopic-assisted resection of dilated colon with end-to-end anastomosis. Resection of the dilated segment alone was not sufficient, according to frozen biopsy. Therefore, we resected an additional 3 cm both proximally and distally, where teniae coli were grossly evident. Histological

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examination of the dilated segment showed muscular layer hypertrophy with hyperplasia and widening of Auerbach’s plexus. The patient’s 7-month follow-up was unremarkable. With improved

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quality of prenatal sonography, more patients will be diagnosed with segmental dilatation of the intestine. This is the first report in the English literature of segmental dilatation of the colon detected on prenatal ultrasound.

Key words

1. Introduction

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segmental dilatation of colon, segmental dilatation of intestine, prenatal ultrasound

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Segmental dilatation of the colon (SDC) is a rare condition involving colonic dilatation without obstruction, first described by Swenson and Rathauser in 1959 [1]. The criteria for diagnosis

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of this disease are 1) lack of radiographically demonstrable motility in the dilated segment, 2) normal appearance and function of the colon both proximal and distal to the dilated segment, 3) absence of teniae coli in the dilated segment, 4) normal ganglion cells, and 5) hypertrophy of the circular and longitudinal muscle layers in the dilated segment, as summarized by Brawner and Shafer in 1972 [2]. However, in previously reported cases, the muscle layer was often thin or irregular and ganglion cells have sometimes been described on histology. According to review articles, the segments of intestine most commonly affected by segmental dilatation are ileum and colon. The condition is rare in the jejunum and duodenum [3]. Almost half of patients with this condition have symptoms of abdominal distention or bilious vomiting as neonates; examination provides the diagnosis. We herein report one case of SDC diagnosed on prenatal ultrasound. This is the first report 2

ACCEPTED MANUSCRIPT to describe SDC detection in the fetus. 2. Case report A male neonate was delivered vaginally at 39 weeks, 3 days’ gestation. His birth weight was 3720 g; Apgar scores were 8 and 9 at 1 and 5 min, respectively. The patient had no apparent

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anomalies. His prenatal ultrasound had shown dilated colon and magnetic resonance imaging performed at 36 weeks’ gestation showed segmental dilated descending colon (Supplementary Fig. 1). No other anomalies were detected.

The patient was brought to our hospital at 1 month of age because of a huge gas shadow in

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the left abdomen on plain abdominal X-ray (Fig. 1).

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Fig. 1. Huge gas shadow in left abdomen on plain abdominal X-ray. He had a normal physical examination and no symptoms. He tolerated feeding, but passed

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stool only once daily. A barium enema was administered to clarify the patient’s condition. This revealed dilated descending colon, with normal transverse and sigmoid colon and rectum. No sign of intestinal obstruction was detected (Fig. 2).

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Fig. 2. Barium enema reveals dilated descending colon, with normal transverse and sigmoid colon and rectum.

At 2 months of age, the patient underwent mucosubmucosal rectal biopsy and anorectal manometry. Examination results were normal for both procedures. No increase was observed in acetylcholinesterase-positive nerve fibers, and a normal anorectal reflex was observed. Based on

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these results, we excluded the possibility of Hirschsprung’s disease and diagnosed SDC. The patient’s parents chose not to pursue surgery at that time, because the infant had no clinical symptoms. We decided to monitor and use a glycerin enema once daily. At 10 months of age, the patient experienced recurrent constipation, diarrhea, and vomiting.

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Barium contrast enema showed fecal accumulation in the dilated segment. We diagnosed enterocolitis caused by chronically accumulating feces. After that the patient received twice-daily

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enemas, cathartic drugs, and several rectal washes. When the patient was 1 year of age, we determined that surgical intervention was

necessary and we scheduled laparoscopic-assisted resection of the dilated segment. Before the operation, a Foley catheter was inserted to evacuate the contents of the colonic lumen. A retractor was inserted into the umbilicus and 5-mm trocars were placed in the right upper and left lower abdomen. The descending colon in the left abdomen had no teniae coli and had prominent mesocolic vessels. After mobilization of the descending colon, the bowel was exteriorized through the umbilical port. We performed resection of only the dilated segment. Because the perioperative frozen biopsy of the removed section showed an increase in ganglion cells, we additionally resected 3 cm both proximal and distal to the initial resection, where the presence of teniae was grossly evident. End-to-end anastomosis was performed (Fig. 3). 4

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Fig. 3. Dilated descending colon, measuring 17 cm in length and 10 cm in maximum diameter, has no teniae coli and has prominent mesocolic vessels.

Fig. 4 shows the macroscopic view of the resected descending colon after formalin fixation. Histological examination using formalin-fixed paraffin embedded tissue of the dilated segment

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revealed a marked hypertrophy of both circular and longitudinal layers of muscularis propria, which was confirmed by immunohistochemical staining for desmin (Fig. 5A and B). An immunohistochemical staining for S-100 showed that Auerbach’s plexus was hyperplastic (Fig. 5C and D). In addition, a number of enlarged and abnormal arteries and veins were observed in serosa

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(Fig. 5A and E). In contrast, the additionally resected segments were normal in both the muscle layer and myenteric plexus, and the abnormal vessels were not observed in serosa. (Fig. 5F-I). We

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performed c-Kit immunostaining, but the distribution, numbers, and shape of the interstitial cells of Cajal was normal in both dilated and additionally resected segments (data not shown).

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Figure 4. Macroscopic view of the resected descending colon.

White arrow indicates the dilated region of the descending colon. The anal (right) and oral (left)

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surgical margins are additionally resected.

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Figure 5. Histological analysis of this case. (A) An image of hematoxylin and eosin (H&E) staining of the dilated segment (magnification 12.5×). A region surrounded by solid black line is focused in (C) and (D). A region surrounded by dotted black line is focused in (E). (B) An immunohistochemical staining for desmin in the same field and magnification with (A). (C). An image of H&E staining of the muscularis propria of the dilated segment (magnification 100×). (D) An immunohistochemical staining for S-100 in the same magnification with (C). (E) Elastica van Gieson (EVG) staining of the serosa of dilated segment (magnification 40×). (F) An image of H&E staining of the additionally resected segment (magnification 12.5×). (G) An immunohistochemical staining for desmin in the same field and magnification with (F). (H) An image of H&E staining of the additionally resected segment 7

ACCEPTED MANUSCRIPT (magnification 100×). (I) An immunohistochemical staining for S-100 in the same magnification with (H). The patient was discharged from hospital on the 17th postoperative day. He had experienced an

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uneventful postoperative course at 7-month follow-up. 3. Discussion

Segmental dilatation of intestine (SDI) is a rare condition in which discrete segments of dilatation are present without intrinsic or extrinsic barriers distal to the dilated segment and with abrupt transition between dilated and normal segments. The condition is most common in the ileum,

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followed by the colon, especially the left colon [4]. Cases of SDI in the jejunum and duodenum are rare.

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According to previous reports, about 50% of SDI patients have symptoms as neonates [5]. Sakaguchi et al reported that the onset of symptoms in patients with dilated small bowel was frequently in the neonatal period; in contrast, patients with dilated colon frequently show symptoms later in infancy. The most common symptoms in neonates are abdominal tenderness and bilious vomiting caused by obstruction; in contrast, constipation is more frequently seen later in infancy [3]. Other clinical presentations, including abdominal pain, gastrointestinal bleeding, and anemia, are nonspecific.

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Associated anomalies are found in more than 50% of patients with SDI, and include anorectal anomaly, malrotation, and omphalomesenteric duct [[6], [7], [8], [9]]. SDI is difficult to diagnose not only prenatally but also antenatally, especially preoperatively. A huge air-filled shadow in an infant on plain abdominal X-rays suggests numerous

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conditions to surgeons and neonatologists. In neonates, Hirschsprung’s disease and volvulus may be excluded first. A barium enema reveals SDI, particularly SDC. Computed tomography or magnetic

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resonance imaging are often helpful in patients with small intestinal dilatation and to rule out other diseases [[10], [11]].

Most reported cases of SDI have been detected after birth, including in the neonatal period.

To the best our knowledge, only nine cases of SDI in the English literature were detected in the prenatal period. All nine cases showed liquid-filled, dilated intestine on routine prenatal ultrasound. With improved quality of prenatal sonography, more patients may be diagnosed with SDI, with or without associated anomalies. A hypoechoic image in the fetal abdomen suggests possible intestinal obstruction, volvulus, bowel duplication, or even choledochal cyst. Table 1 summarizes various aspects of reported cases, including our own [[6], [7], [10], [12], [13], [14], [15], [16]].

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ACCEPTED MANUSCRIPT Gestati

Se

tional

onal

x

age

age

at

birth,

diagn

Birth

osis

weight

29 wk

41 wk

1996

Symptoms

Localization,

Surgical

Age

size

procedure

at

at

opera tion

F

3360 g

Bilious

Jejunum

End-to-end

vomiting,

15×7 cm

anastomosis,

abdominal

appendectomy

3980 g

M

Unknown

Normal

Jejunum

End-to-end

Unkno

Normal ganglion cells,

6×9 cm

anastomosis

wn

edematous mucosa

Abdominal

Distal

End-to-end

Unkno

Unknown

h,

distention,

duodenum

anastomosis

wn

2004

respiratory

10 cm

2001 Manikot

30 wk

Term

M

distress

2007

M

3800 g

Park,

Unkn

2010

own

Okada,

37 wk

25 wk

37 wk 2695 g

F

F

Ileum

End-to-end

Unkno

Normal ganglion cells,

at 1 mo

6.8×3.5 cm

anastomosis,

wn

surface ulceration in patchy

Unknown

2011

9 wk

38 wk

3456 g

F

End-to-end

distribution 2 days

anastomosis

Irregular thickness of muscle layer, normal ganglion cells

Distal

End-to-end

vomiting,

duodenum–

anastomosis

abdominal

proximal

thin and coarse c-kit-positive

jejunum

cells

distention

Katsura,

Ileum

appendectomy

Bilious

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2010

38 wk

Bloody stool

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18 wk

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Waters,

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30 wk

1 wk

SC

distention Hosie,

Histology

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Mboyo,

Gesta

Abdominal

1 day

Partial thin muscle layer, irregular Auerbach’s plexus,

8×5×7 cm Duodenum

distention

First:

First:

Normal Auerbach’s plexus,

gastrostomy,

1 day

decreased c-kit-positive cells

duodenostomy

Secon

Second:

d: 28

partial

days

resection

9

ACCEPTED MANUSCRIPT Paradiso,

35 wk

2013

35 wk

M

2880 g

Abdominal

Ileum

End-to-end

Unkno

Normal

distention at 2

30 cm

anastomosis

wn

Bilious

Ileum

End-to-end

7 days

vomiting,

10 cm

anastomosis,

ectopic pancreatic tissue in

abdominal

Ladd’s

myenteric layer

distention

operation

weeks

2220 g

Present

Unkn

39 wk

case

own

3720 g

M

Normal ganglion cells,

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F

SC

37 wk

Constipation,

Descending

End-to-end

1 yr, 2

Hypertrophic muscle layer,

enterocolitis

colon

anastomosis

mo

Auerbach’s

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37 wk

was

hyperplastic and wide.

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17×10 cm

plexus

Table 1. Summarization of reported cases and our own. Seven of nine patients (77.8%) were full-term infants. Six of the nine (66.7%) had bowel dilatation.

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symptoms as neonates and underwent surgery as early as the 7th day. All nine patients had small

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Our patient is the first case of SDC detected with prenatal ultrasound. The patient was

discharged from hospital as a neonate, with no symptoms. Symptoms began at 10 months of age, with constipation and enterocolitis, despite once-daily enemas. These findings are consistent with a previous study that reported that patients with dilated colon show symptoms in infancy [3]. Patients with symptoms or anomalies must undergo surgery. However, it remains unclear whether patients without symptoms should have surgery. Treatment of SDI is simple: resection of the dilated segment with end-to-end anastomosis. A laparoscopic approach has been applied in patients with SDC, even in infants [11]. Collapsing the colon by evacuating luminal contents before surgery simplifies the laparoscopic procedure. The typical SDC segment has no teniae and has abundant serosal vascularization [4]. In our case, 10

ACCEPTED MANUSCRIPT resection of the dilated segment alone was insufficient according to histology; the definitive resection line was determined according to the presence of teniae, because histology was normal. In critically ill patients, surgeons may create a temporary stoma without excision [17]. If the dilated segment is duodenal, it is difficult to perform usual resection because the ampulla of Vater may be in the dilated segment. In these cases, partial resection with duodenal modeling or side-to-end

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duodenojejunal anastomosis have been performed [12]. Prognosis is generally good after excision [9].

Postoperative histological examination allows diagnosis confirmation. Previous studies have reported various histological findings. The muscle layer is almost always hypertrophic [9], which is consistent with the criteria described by Brawner [2]. However, normal, very thin [5], or

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irregular [14] muscle layers have also been reported. Lack of muscular hypertrophy may indicate the effect of chronic obstruction. Ganglion cells are generally normal [[18], [19]]. Mahadevaiah et al

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described atypical positioning of the nerve plexus, which was more within the circular muscle layer than in its normal location [5]. Nagi et al first described moderate hypertrophy of the nerve bundles [20]. Two studies have reported decreased or thin c-kit-positive cells in Auerbach’s plexus on immunohistochemistry staining [[12], [13]].

The etiology of SDC remains unclear; intrauterine vascular accident, impairment of organogenesis, strangulation of intestine in the umbilical ring, vitelline vessels or omphaloenteric

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band, defective muscular development, and neurogenic causes have all been proposed [[4], [13]]. The variable histopathological findings indicate that SDI may be a collective term for different

4. Conclusion

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diseases causing bowel dilatation, not a single entity.

This is the first case of SDC detected in the prenatal period. The patient had no symptoms

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until 10 months of age. The optimal timing of surgery remains uncertain. Laparoscopic-assisted resection was useful in this case. Patient consent

Consent to publish the case report was not obtained. This report does not contain any personal information that could lead to the identification of the patient. Funding No funding or grant support was received for production of this manuscript. Authorship All authors attest that they meet the current ICMJE criteria for Authorship. Conflict of interest 11

ACCEPTED MANUSCRIPT The following authors have no financial disclosures: N.U, T.S, K.S, T.T, T.T, Y.K, A.N, S.W, T.Y, F.H,

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ACCEPTED MANUSCRIPT [16] Paradiso FV, Coletta R, Olivieri C, et al. Antenatal ultrasonography features associated with segmental dilatation: an unusual neonatal condition mimicking congenital small bowel obstruction. Pediatr and Nenonat2013;54:339-343 [17] Ragavan M, Arunkumar S, Balaji N. Segmental dilatation of near total colon managed by colon preserving surgery. APSP J Case Rep2012;3:18. intestine in neonate: report of three case. J Neonat Surg2016;5:55

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Surg1992;27:506-508

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