Sonography of Normal Fetal Bowel Suhas G. Parulekar, MD, FACR
This is a prospective study of the sonographic appearance of normal small bowel and colon in 300 fetuses. Normal fetal bowel can be frequently seen during sonographic examination. The diameter of the lumen of the small bowel and colon increases as gestational age increases. The fetal small bowel lumen rarely exceeds 6 mm in diameter, and fetal colon lumen diameter rarely exceeds 23 mm. Small bowel peristalsis can be seen with increasing frequency with increasing gestational age. Colon peristalsis is not seen. Haustral folds
T
he normal fetal bowel can be demonstrated during obstetrical ultrasound examination. •-3 This prospective study was performed for evaluation of the appearance and size of the normal fetal small bowel and colon.
MATERIALS AND METHODS A total of 300 fetuses were prospectively evaluated; 243 fetuses, ranging in gestational age from 10 weeks to postterm (>40 weeks), were evaluated prospectively and consecutively by transabdominal sonography using 3.5-MHz mechanical sector scanner (Diasonics). A total of 57 fetuses, between 6 and 14 weeks gestational age, were evaluated prospectively, but not consecutively, using 7.5-MHz mechanical sector transvaginal transducer (Diasonics). Only women with uncomplicated pregnancies were included in this prospective study. All of the mothers have delivered without evidence of gastrointestinal abnormalities in their newborns. Received May 14, 1990, from the Department of Radiology, Divis'ion of Ultrasound, The Mt. Sinai Medical Center, Cleveland, Ohio. Revised manuscript accepted for publication October 17, 1990. Address correspondence and reprint requests to Dr. Suhas G. Paru\ekar: Department of Radiology, Division of Ultrasound, The Mt. Sinai Medical Center, One Mt. Sinai Drive, Cleveland, OH 44106.
in the colon can be frequently demonstrated. Meconium in the colon always remains hypoechoic relative to the fetal liver and bowel wall. Hyperechoic appearance of the small bowel in early gestation and cystic appearance of parts of the colon in later gestation may mimic pathology. Normal herniation of bowel into umbilical cord can be seen in early (8 to 11 weeks) gestation. KEY woRos: fetal bowel, small intestine, colon, bowel herniation, omphalocele. U Ultrasound Med 10: 211, 1991)
The fetal small bowel and the colon were evaluated prospectively for appearance and size. All of the sonographic examinations were performed by the author personally. The size of the lumen (internal diameter, from the inner bowel wall interfaces) of the fetal bowel was measured using mechanical calipers. To determine the presence of motion of peristalsis within the bowel, the small bowel and the colon were observed continuously for a period of at least 1 minute each. In each fetus, only the maximum diameter of the lumen of the small bowel and the colon was measured. Also, the maximum length of the longest contiguous segment of the small bowel and colon was measured. The fetal gestational ages are menstrual ages.
RESULTS A total of 57 fetuses ranging in gestational age from 6 to 14 weeks were examined by transvaginal sonography. Of these, 39 fetuses were between 6 and 10 weeks gestation. The small bowel could not be demonstrated in the fetal abdomen in any of these fetuses between 6 and 10 weeks gestation. Embryologically, the fetal small bowel does not begin to return into the peritoneal cavity within the abdomen until after 10 weeks gestation.4 In four fetuses, between 10 and 11 weeks gestation, the small bowel could be demonstrated as a
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A
c
B
Figure 1 Transvaginal sonograms. A, 11 weeks fetus. Transverse section. Hyperechoic area (curoed arrow) represents bowel herniated into umbilical cord near its entrance into fetal abdomen. Straigl1t arrows, umbilical cord. 8, 11 weeks fetus. Sagittal section. Bowel (large arrows) herniated into umbilical cord. Small arrows, umbilical cord. C, 12.5 weeks fetus. Sagittal section. Small bowel appears as a large hyperechoic area (arrows) in the fetal pelvis and abdomen .
solid hyperechoic area within the umbilical cord near its entrance into the fetal abdomen (Fig. l, A and B). The small bowel, which appeared as a hyperechoic (compared to fetal liver) area in the fetal abdomen, could be demonstrated in 6 out of 18 fetuses with gestational ages of 10 to 14 weeks (Fig. IC). The colon could not be demonstrated in any of the fetuses. A tota l of 243 fetuses ranging in gestational age from 10 weeks to postterm (>40 weeks) were examined by transabdominal sonography using a 3.5-MHz mechanical sector transducer (Table 1). The small bowel, appearing as a hyperechoic (compared to fetal liver) area in the feta! pelvis and lower abdomen could be dem-
onstrated in 44% of the fetuses between 10 and 15 weeks gestational age (Fig. 2, A and B). The hyperechoic small bowel could not be seen in any of the fetuses between 10 and 12 weeks gestation. The hyperechoic small bowel could not be seen in 30% of the fetuses between 12 and 13 weeks gestation, 57% of fetuses between 13 and 14 weeks gestation, and 58% of the fetuses between 14 and 15 weeks gestation. Fluid-filled lumen of small bowel was not seen prior to 13 weeks gestation. Between 13 and 20 weeks gestation, a few tiny (1 mm or less in diameter) hypoechoic round areas may be seen within the predominantly hyperechoic small bowel. These hypoechoic areas
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Table 1: Detection Rate, Lumen Diameter, and Length of Contiguous Bowel Segment Gestational Age, weeks
Number of Fetuses
>40 35- 40 30- 35 25- 30 20- 25 15- 20 10- 15
9 44 36 44 44 34 32
Percentage of Fetuses with Visible Lumen Small Bowel/Colon
100 100 100 100 100 88 44
100 100 100 100 89 24 6
Small Bowel Lumen Size•
Colon Lumen Size•
Average Length•
Average
Largest
Average
Largest
Small Bowel
Colon
4.4 3.7 2.9 1.8 1.4 1.2 1.0
6 8 6 3 2 2 1
18.7 16.8 11.4 8 4.4 3.6 1.5
28 26 16 13 6 5 2
11.3 11 9.8 7.9 4.5 4.5 2.4
63 70 55 37 19 9.8 10
• All measurements are in millimeters_The average lumen diameter and length of bowel segment are average maximum measurements. Gestational ages are menstrual ages.
probably represent a small amount of fluid in the small bowel lumen. Between 20 and 40 weeks gestation, the small bowel appeared as a hyperechoic area containing anechoic fluid-filled loops of small bowel. The ane ~ choic lumen of small bowel was much easier to demonstrate after 20 weeks gestation. The small bowel lumen could be demonstrated in 44% of the fetuses between 10 and 15 weeks gestation, in 88% of the fetuses between 15 and 20 weeks gestation, and in 100% of the fetuses between 20 and 40 weeks gestation (Fig. 2, C- E). The average maximum diameter of the lumen of the small bowel increased as gestational age increased and ranged from less than 1 mm at 13 weeks gestation to 4.4 mm in postterm (>40 weeks) gestation (Fig. 2, AE; Table 1). Of 243 fetuses, only 6 had small bowel lumen diameter of 6 mm and 1 of 8 mm. The largest
diameter of the small bowel lumen demonstrated was 8 mm (Fig. 3). The average maximum length of the small bowel loop observed also increased as gestational age in, creased, ranging from 2.4 mm at 10 to 15 weeks gestation, to 11.3 mm in postterm (>40 weeks) gestation (Table 1). The maximum length of the contiguous segment of the small bowel demonstrated was 21 mm (Fig. 3). The colon could be recognized by its peripheral location and known anatomic configuration (Fig. 4). The colon could not be definitely demonstrated in fetuses between 10 and 18 weeks gestation. There was questionable but not definitive demonstration of colon in two fetuses between 14 and 15 weeks gestation, and one fetus at 17 weeks gestation. The fetal colon was quite small and difficult to demonstrate between 18
Figure 2 Transabdominal sonograms. A, 13 weeks fetus. Coronal section. Hyperechoic area (arrows) represents small bowel. B, 15 weeks fetus. Sagittal section. Hyperechoic area (arrows) represents small bowel.
A
B
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c
D Figure 2 C, 20 weeks fetus . Coronal section. Hyperechoic area (arrows) represents small bowel. Small bowel lumen (llypoecl1oic ro1111d areas) measures 1.5 mm. D, 30 weeks fetus. Coronal section. Anechoic small bowel lumen (arrows) measures 3 mm. E, 40 weeks fetus. Transverse section. Anechoic small bowel lumen (arrows) measures 7 to 8 mm . SP, spine.
and 22 weeks gestation. The colon could be seen in 44% of the fetuses between 18 and 20 weeks gestation and 89% of the fetuses between 20 and 25 weeks gestation . The colon could be seen in 100% of the fetuses after 25 weeks gestation. The average maximum diameter of the colon increased progressively from 18 weeks to postterm gestation, ranging in diameter from 3.6 mm between 15 and 20 weeks to 18.7 mm at postterm gestation (Fig. 5; Table 1). The largest diameter of the colon demon· strated was 28 mm (Fig. SB). Of 243 fetuses, only 2 had colon lumen diameter greater than 23 mm. The average maximum length of the contiguous segment of the colon demonstrated on the sonographic
examination also increased progressively from 9.8 mm between 15 and 20 weeks gestation, to 70 mm between 35 and 40 weeks gestation (Table 1). The maximum length of the contiguous segments of the colon demonstrated was 15 cm. The haustral folds in the colon could be seen in 73 of the fetuses between 20 and 25 weeks gestation, 61 % of the fetuses between 25 and 30 weeks, 78% of the fetuses between 30 and 35 weeks, 89% of the fetuses between 35 and 40 weeks, and 89% of the fetuses postterm (Table 2). The small bowel peristalsis could be seen as rapidly changing size and appearance of fluid-filled loops of small bowel. The small bowel peristalsis could be dem-
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contents was not seen at any time during gestation. In two fetuses between 35 and 40 weeks gestation, there was suggestion of single rapid contraction of parts of the fetal colon.
DISCUSSION
Figure 3 39 weeks fetus . Transverse section. Small bowel loop (straight arrows), 21 mm in length, demonstrating val+ vulae conniventes as thin linear echoes within the lumen. Large oval area (open curved arrow) represents fluid-.filled small bowel measuring 8 x 11 mm.
onstrated in 9% of the fetuses between 25 and 30 weeks gestation, in 47% of the fetuses between 30 and 35 weeks gestation, in 73% of the fetuses between 35 and 40 weeks gestation, and 77% of the fetuses in postterm (>40 weeks) gestation (Table 2). Small bowel peristalsis was not seen prior to 27 weeks gestation. Active peristalsis of the colon or motion of the colonic
Between 8 and 10 weeks gestation, the fetal intestine is within the umbilical cord, near its entrance into the fetal abdomen. 4 The rapidly growing liver and the developing mesonephri encroach on the available space in the embryonic coelom (abdomen) so much that the intestine is extruded into the umbilical coelom, ie, that part of the extraembryonic coelom which lies in the proximal end of the umbilical cord. 5 At 10 weeks gestation, the proximal limb (ie, the small intestine) returns into the abdomen. By 11 weeks gestation, the majority of intestine returns, and by 12 weeks gesta · tion, all the intestine returns into the abdomen.4 By transvaginal sonogram, the herniated intestine was seen as a solid hyperechoic area within the proximal end of the umbilical cord, between 10 and 11 weeks gestation (Fig. 1). Further investigation is necessary to determine how often normal herniation of bowel can be demonstrated in early gestation by transvaginal sonography. Normal herniation of small bowel into umbilical cord, between 8 and 10 weeks gestation, has been previously demonstrated by transabdominal sonography.6 Therefore, it has been suggested that the diagnosis of abdominal wall defect should not be made sonographically before 14 weeks of menstrual age. 6
Figure 4 35 weeks fetus. The entire colon is demonstrated. A, B, C are coronal sections. A, The cecum, ascending colon, and proximal transverse colon are demonstrated (arrows). Notice haustral folds in the cecum seen as hyperechoic lines in the lumen. B, urinary bladder. B, Transverse colon (arrows) is demonstrated. B, urinary bladder.
A
B
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c
D
Figure 4 C, Descendjng colon, sigmoid colon, and rectum are demonstrated (arrows) . Stomach is seen medial to the proximal descending colon. D, Transverse section, showjng peripherally located colon (arrows). SP, spine.
In early gestation (10 to 20 weeks), the small bowel lumen is quite difficult to demonstrate. The region of the small bowel, however, can be seen and appears as a hyperechoic (relative to fetal liver) area in the abdomen and pelvis. This hyperechoic appearance around the small bowel persists throughout the pregnancy and it was seen in all the fetuses in this study. Before 20 weeks gestation, especially between 12 and 16 weeks
gestation, this hyperechoic area, when seen, fills a large portion of the fetal pelvis and lower abdomen. In later gestation, the hyperechoic area becomes less prominent and is more centrally located in the fetal abdomen. Hyperechoic appearance could be secondary to reflections from walls of collapsed loops of small bowel. Hyperechoic appearance could also be from mesenteric fat between loops of collapsed small bowel, since in
Figure 5 Coronal sections. A, 31 weeks fetus. Descending colon, sigmoid and rectum are seen (arrows). Colon lumen 4 to 7.5 mm. Meconium appears quite hypoechoic. 8, 41 weeks fetus. Right colon and cecum are seen (arrows). Colon lumen 28 mm near cecum. Meconium much more echogenic than in A. 8, urinary bladder.
A
B
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Table 2: Detection Rate of Small Bowel Peristalsis and Colonic Haustral Folds Gestational . A Small Bowel Colome Haustral geks , Peristalsis, % Folds, % wee
>40 35- 40 30- 35 25- 30 20- 25 15- 20 10- 15
73
89 89
9
78 61
77
47 0
7
0
0
0
0
Gestational ages are menstrual ages.
c Figure 6 A, 15 weeks fetus. Sagittal section. Small bowel appearing as a hyperechoic area (arrows) anterior to sacrum, mimics pathologic mass. SP, spine. H, fetal head. B, 36 weeks fetus. Transverse section. Small bowel, appearing as a large hyperechoic area (arrows) anterior to the spine (SP), mimics pathologic mass. C, 32 weeks fetus. Sagittal section. Rounded hyperechoic area (closed arrows) represents small bowel her• niated into umbilical cord (ope11 arrows) in a fetus with omphalocele. B, urinary bladder.
A
B
later gestation, spaces between loops of fluid-filled small bowel also appear hyperechoic (Fig. 2, D and E). In some fetuses, especially before 20 weeks gestation, this hyperechoic area can be unusually prominent and should not be mistaken for a pathologic mass (Fig. 6A).7·e Follow-up sonograms in a few weeks will show change in appearance or complete disappearance of this hyperechoic area, thus excluding the possibility of pathologic mass. ~ Between 13 and 20 weeks gestation, small (1 to 1.5 mm in diameter) hypoechoic rounded areas may appear within this hyperechoic region. These probably represent small bowel lumen and when clearly seen should distinguish this hyperechoic area from a pathologic mass. Occasionally, even in later gestation (after 20 weeks), collapsed small bowel may appear as a large hyperechoic area and mimic a pathologic mass (Fig. 6B). Increased echogenicity in the fetal abdomen has been described secondary to calcifications in meconium per· itonitis, infection, neoplasms, and unknown causes.1• 9 Calcifications appear as scattered hyperechoic areas in liver, spleen, or peritoneal cavity, some associated with acoustic shadowing. Cystic mass with hyperechoic margin secondary to calcified wall may be seen in meconium pseudocyst formation secondary to meco·
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nium peritonitis Normal hyperechoic small bowel appears as a large focal area of increased echogenicity in the lower fetal abdomen and is not associated with shadowing, cystic masses, or other abnormal findings, such as ascites or polyhyramnios. In later gestation, presence of fluid-filled loops, frequently with visible peristalsis, helps differentiate the hyperechoic small bowel from pathologic mass. Meconium ileus may present with nonshadowing areas of increased echo ~ genicity in fetal lower abdomen and may be difficult to distinguish from normal small bowel in early gestation. Change in appearance of the hyperechoic area on follow-up sonograms, presence of normal fluid-filled loops with peristalsis within the hyperechoic area, and absence of proximal dilatation of small bowel may be helpful to distinguish normal hyperechoic small bowel from a nonshadowing area of increased echogenicity due to meconium ileus. The knowledge that collapsed (empty) loops of small intestine appear hyperechoic can be helpful in diagnosing omphalocele. The omphalocele can occasionally appear as a small solid hyperechoic mass within the proximal end of the umbilical cord, near its entrance into the abdomen (Fig. 6C). The hyperechoic mass represents collapsed loops of small bowel herniated into the umbilical cord. In this case, postnatal abdominal radiographs, small bowel series, and surgery confirmed the presence of small bowel in the omphalocele. No other organs were found within the omphalocele. The small bowel is located centrally in the abdomen and pelvis, and the fluid -filled small bowel loops appear as rounded areas. However, in later gestation, longer segments of the fluid· filled small bowel loops can be demonstrated (Fig. 3). The valvulae conniventes cannot be routinely demonstrated within the small bowel lumen. The valvulae could be demonstrated in only 9 of 243 patients (Fig. 3). Fetal intestinal musculature is poorly developed and peristalsis is weak and discontinuous until birth. 4 After 27 weeks gestation, the small bowel peristalsis could be demonstrated with increasing frequency with increasing gestational age. Active peristalsis of the colon or motion of the colonic contents was not seen at any time during gestation. In two fetuses between 35 and 40 weeks gestation, there was suggestion of single rapid contraction of parts of the fetal colon. The colon could be recognized by its anatomic locain the peripheral portion of the abdomen as well as its known anatomic configuration. Usually only parts of the colon could be demonstrated. Occasionally, especially in later gestation (after 30 weeks), almost the entire colon could be demonstrated (Fig. 4). The haustral folds, which also could be frequently demonstrated, differentiate the colon from the small bowel (Fig. 7). It has been stated that fetal colon lacks haustra and haustra develop in the first 6 months after birth. 4
A
B Figure 7 A, 30 weeks fe tus. Small haustral folds (black arrows) a1e seen in the colon. B, 38 weeks fetus. Larger haustral folds (arrows) are seen in the colon . Indentation and puckering of colon wall (black arrow) is seen near the haustral
fold .
However, in this study, haustral folds in the lumen of the colon were seen quite frequently.. Haustral indentations on the surface of the colonic wall or sacculations were rarely seen (Fig. 78). .In early gestation, haustral folds appear as thin linear echoes within the lumen of the colon. In later gestation, as the colon diameter increases, the haustral folds becomes longer and thicker. Occasionally the haustral folds can be quite prominent. After 14 weeks gestation, lipid is absorbed from the fetal colon, and the remaining contents collect in the
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colon as meconium. 4 In all fetuses, the meconium within the lumen of the colon appeared hypoechoic relative to the fetal liver and in comparison with bowel wall. Rarely, near term, meconium became almost isoechoic with fetal liver. However, meconium was never seen to be hyperechoic during normal pregnancy. The echogenicity of the meconium appeared to increase slightly with increasing gestational age (Fig. 5). Occasionally, the meconium can appear quite anechoic. Prominent anechoic rounded segment of the transverse Figure 8 A, 36 weeks fetus. Coronal section. Rounded anechoic colon (C) mimics double-bubble sign of duodenal atresia. ST, stomach; B, urinary bladder. B, 40 weeks fetus. Transverse section. Rounded anechoic colon (arrows) mimics cystic mass. B, urinary bladder.
A
PARULEKAR 219
colon, located close to the fetal stomach, can mimic the double-bubble sign of duodenal atresia (Fig. 8A). By scanning in different planes, however, this rounded anechoic structure can be demonstrated to be part of the transverse colon. Prominent, rounded parts of the colon, especially the sigmoid colon, can also mimic pathologic mass, such as an ovarian cyst, in the pelvis (Fig. 88). The measurements of average maximum diameter of the lumen of the small bowel and colon in this study are similar to those published by Nyberg et al. 1 The largest diameters of the small bowel lumen (8 mm) and colon lumen (28 mm) demonstrated in this study are larger than those published by Nyberg et al. The colon, the small bowel lumen, and the small bowel peristalsis were seen earlier and more frequently in this study, perhaps partly because of a much larger number of fetuses examined in this study. In conclusion, the possibility of pathologic bowel dilatation should be considered if the lumen measurements exceed those described for different gestational age groups (Table 1). Near term, the small bowel lumen diameter should not exceed 6 mm and the colon lumen diameter 23 mm, even though the largest diameters in normal fetuses in this study were 8 mm for small bowel in one fetus near term, and for the colon, 26 mm near term and 28 mm postterm in two fetuses. Dilated bowel may be seen in fetal abdomen secondary to atresia, malrotation, or meconium ileus. 9 The diameter of small bowel and colon lumen increases progressively with increasing gestational age. The length of the contiguous bowel segment that is visible also increases progres• sively with increasing gestational age. Small bowel peristalsis can be seen with increasing frequency after 27 weeks gestation. Colon peristalsis is not seen. Haustral folds in the colon can be frequently demonstrated, whereas valvulae conniventes in the small bowel are rarely seen. Meconium in the colon always remained hypoech•.liC relative to the fetal liver and bowel wall. Hyperechoic appearance of the small bowel in early gestation and anechoic cystic appearance of colon in later gestation may mimic pathology. Normal hernia· tion of small bowel within the umbilical cord at its insertion into the fetal abdomen may be seen between 8 and 11 weeks gestation.
REFERENCES
B
1. Nyberg DA, Mack LA, Patten RM, et al: Fetal bowel: Normal sonographic findings. J Ultrasound Med 6:3, 1987 2. Lee TC, Warren BH: Antenatal ultrasonic demonstration of fetal bowel. Radiology 124:471, 1977 3. Zilianti M, Fernandez S: Correlation of ultrasonic images of fetal intestine with gestational age and fetal maturity. Obstet Gynecol 62:569, 1983
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4. England, MA: Color Atlas of Life Before Birth. Chicago, Year Book Medical Publishers, Inc., 1983; pp 132, 138 5. Wamick R, Williams P (eds): Gray'!i Anatomy. Philadel· phia, WB Saunders Co, 1973, p 173 6. Cyr DR, Mack LA, Schoenecker SA, et al: Bowel migra ~ tion in the normal fetus: US detection. Radiology 161:119, 1986 ~ 7. Fakhry J, Reiser M, Shapiro LR, et al: Increased echogen
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icity in the lower fetal abdomem A common normal variant in the second trimester. J Ultrasound Med 5:489, 1986 8. Lince OM, Pretorius DH, Manco-Johnson ML: The clinical significance of increased echogenicity in the fetal abdomen. AJR 145:683, 1985 9.. Goldstein RB, FiUy RA, Callen PW: Sonographic diagnosis of meconium ileus in utero. J Ultrasound Med 6:663, 1987
This is a prospective study of the sonographic appearance of normal small bowel and colon in 300 fetuses. Normal fetal bowel can be frequently seen during sonographic examination. The diameter of the lumen of the small bowel and colon increases as gestational age increases. The fetal small bowel lumen rarely exceeds 6 mm in diameter, and fetal colon lumen diameter rarely exceeds 23 mm. Small bowel peristalsis can be seen with increasing frequency with increasing gestational age. Colon peristalsis is not seen. Haustral folds
T
he normal fetal bowel can be demonstrated during obstetrical ultrasound examination. •-3 This prospective study was performed for evaluation of the appearance and size of the normal fetal small bowel and colon.
MATERIALS AND METHODS A total of 300 fetuses were prospectively evaluated; 243 fetuses, ranging in gestational age from 10 weeks to postterm (>40 weeks), were evaluated prospectively and consecutively by transabdominal sonography using 3.5-MHz mechanical sector scanner (Diasonics). A total of 57 fetuses, between 6 and 14 weeks gestational age, were evaluated prospectively, but not consecutively, using 7.5-MHz mechanical sector transvaginal transducer (Diasonics). Only women with uncomplicated pregnancies were included in this prospective study. All of the mothers have delivered without evidence of gastrointestinal abnormalities in their newborns. Received May 14, 1990, from the Department of Radiology, Divis'ion of Ultrasound, The Mt. Sinai Medical Center, Cleveland, Ohio. Revised manuscript accepted for publication October 17, 1990. Address correspondence and reprint requests to Dr. Suhas G. Paru\ekar: Department of Radiology, Division of Ultrasound, The Mt. Sinai Medical Center, One Mt. Sinai Drive, Cleveland, OH 44106.
in the colon can be frequently demonstrated. Meconium in the colon always remains hypoechoic relative to the fetal liver and bowel wall. Hyperechoic appearance of the small bowel in early gestation and cystic appearance of parts of the colon in later gestation may mimic pathology. Normal herniation of bowel into umbilical cord can be seen in early (8 to 11 weeks) gestation. KEY woRos: fetal bowel, small intestine, colon, bowel herniation, omphalocele. U Ultrasound Med 10: 211, 1991)
The fetal small bowel and the colon were evaluated prospectively for appearance and size. All of the sonographic examinations were performed by the author personally. The size of the lumen (internal diameter, from the inner bowel wall interfaces) of the fetal bowel was measured using mechanical calipers. To determine the presence of motion of peristalsis within the bowel, the small bowel and the colon were observed continuously for a period of at least 1 minute each. In each fetus, only the maximum diameter of the lumen of the small bowel and the colon was measured. Also, the maximum length of the longest contiguous segment of the small bowel and colon was measured. The fetal gestational ages are menstrual ages.
RESULTS A total of 57 fetuses ranging in gestational age from 6 to 14 weeks were examined by transvaginal sonography. Of these, 39 fetuses were between 6 and 10 weeks gestation. The small bowel could not be demonstrated in the fetal abdomen in any of these fetuses between 6 and 10 weeks gestation. Embryologically, the fetal small bowel does not begin to return into the peritoneal cavity within the abdomen until after 10 weeks gestation.4 In four fetuses, between 10 and 11 weeks gestation, the small bowel could be demonstrated as a
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NORMAL FETAL BOWEL
A
c
B
Figure 1 Transvaginal sonograms. A, 11 weeks fetus. Transverse section. Hyperechoic area (curoed arrow) represents bowel herniated into umbilical cord near its entrance into fetal abdomen. Straigl1t arrows, umbilical cord. 8, 11 weeks fetus. Sagittal section. Bowel (large arrows) herniated into umbilical cord. Small arrows, umbilical cord. C, 12.5 weeks fetus. Sagittal section. Small bowel appears as a large hyperechoic area (arrows) in the fetal pelvis and abdomen .
solid hyperechoic area within the umbilical cord near its entrance into the fetal abdomen (Fig. l, A and B). The small bowel, which appeared as a hyperechoic (compared to fetal liver) area in the fetal abdomen, could be demonstrated in 6 out of 18 fetuses with gestational ages of 10 to 14 weeks (Fig. IC). The colon could not be demonstrated in any of the fetuses. A tota l of 243 fetuses ranging in gestational age from 10 weeks to postterm (>40 weeks) were examined by transabdominal sonography using a 3.5-MHz mechanical sector transducer (Table 1). The small bowel, appearing as a hyperechoic (compared to fetal liver) area in the feta! pelvis and lower abdomen could be dem-
onstrated in 44% of the fetuses between 10 and 15 weeks gestational age (Fig. 2, A and B). The hyperechoic small bowel could not be seen in any of the fetuses between 10 and 12 weeks gestation. The hyperechoic small bowel could not be seen in 30% of the fetuses between 12 and 13 weeks gestation, 57% of fetuses between 13 and 14 weeks gestation, and 58% of the fetuses between 14 and 15 weeks gestation. Fluid-filled lumen of small bowel was not seen prior to 13 weeks gestation. Between 13 and 20 weeks gestation, a few tiny (1 mm or less in diameter) hypoechoic round areas may be seen within the predominantly hyperechoic small bowel. These hypoechoic areas
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Table 1: Detection Rate, Lumen Diameter, and Length of Contiguous Bowel Segment Gestational Age, weeks
Number of Fetuses
>40 35- 40 30- 35 25- 30 20- 25 15- 20 10- 15
9 44 36 44 44 34 32
Percentage of Fetuses with Visible Lumen Small Bowel/Colon
100 100 100 100 100 88 44
100 100 100 100 89 24 6
Small Bowel Lumen Size•
Colon Lumen Size•
Average Length•
Average
Largest
Average
Largest
Small Bowel
Colon
4.4 3.7 2.9 1.8 1.4 1.2 1.0
6 8 6 3 2 2 1
18.7 16.8 11.4 8 4.4 3.6 1.5
28 26 16 13 6 5 2
11.3 11 9.8 7.9 4.5 4.5 2.4
63 70 55 37 19 9.8 10
• All measurements are in millimeters_The average lumen diameter and length of bowel segment are average maximum measurements. Gestational ages are menstrual ages.
probably represent a small amount of fluid in the small bowel lumen. Between 20 and 40 weeks gestation, the small bowel appeared as a hyperechoic area containing anechoic fluid-filled loops of small bowel. The ane ~ choic lumen of small bowel was much easier to demonstrate after 20 weeks gestation. The small bowel lumen could be demonstrated in 44% of the fetuses between 10 and 15 weeks gestation, in 88% of the fetuses between 15 and 20 weeks gestation, and in 100% of the fetuses between 20 and 40 weeks gestation (Fig. 2, C- E). The average maximum diameter of the lumen of the small bowel increased as gestational age increased and ranged from less than 1 mm at 13 weeks gestation to 4.4 mm in postterm (>40 weeks) gestation (Fig. 2, AE; Table 1). Of 243 fetuses, only 6 had small bowel lumen diameter of 6 mm and 1 of 8 mm. The largest
diameter of the small bowel lumen demonstrated was 8 mm (Fig. 3). The average maximum length of the small bowel loop observed also increased as gestational age in, creased, ranging from 2.4 mm at 10 to 15 weeks gestation, to 11.3 mm in postterm (>40 weeks) gestation (Table 1). The maximum length of the contiguous segment of the small bowel demonstrated was 21 mm (Fig. 3). The colon could be recognized by its peripheral location and known anatomic configuration (Fig. 4). The colon could not be definitely demonstrated in fetuses between 10 and 18 weeks gestation. There was questionable but not definitive demonstration of colon in two fetuses between 14 and 15 weeks gestation, and one fetus at 17 weeks gestation. The fetal colon was quite small and difficult to demonstrate between 18
Figure 2 Transabdominal sonograms. A, 13 weeks fetus. Coronal section. Hyperechoic area (arrows) represents small bowel. B, 15 weeks fetus. Sagittal section. Hyperechoic area (arrows) represents small bowel.
A
B
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c
D Figure 2 C, 20 weeks fetus . Coronal section. Hyperechoic area (arrows) represents small bowel. Small bowel lumen (llypoecl1oic ro1111d areas) measures 1.5 mm. D, 30 weeks fetus. Coronal section. Anechoic small bowel lumen (arrows) measures 3 mm. E, 40 weeks fetus. Transverse section. Anechoic small bowel lumen (arrows) measures 7 to 8 mm . SP, spine.
and 22 weeks gestation. The colon could be seen in 44% of the fetuses between 18 and 20 weeks gestation and 89% of the fetuses between 20 and 25 weeks gestation . The colon could be seen in 100% of the fetuses after 25 weeks gestation. The average maximum diameter of the colon increased progressively from 18 weeks to postterm gestation, ranging in diameter from 3.6 mm between 15 and 20 weeks to 18.7 mm at postterm gestation (Fig. 5; Table 1). The largest diameter of the colon demon· strated was 28 mm (Fig. SB). Of 243 fetuses, only 2 had colon lumen diameter greater than 23 mm. The average maximum length of the contiguous segment of the colon demonstrated on the sonographic
examination also increased progressively from 9.8 mm between 15 and 20 weeks gestation, to 70 mm between 35 and 40 weeks gestation (Table 1). The maximum length of the contiguous segments of the colon demonstrated was 15 cm. The haustral folds in the colon could be seen in 73 of the fetuses between 20 and 25 weeks gestation, 61 % of the fetuses between 25 and 30 weeks, 78% of the fetuses between 30 and 35 weeks, 89% of the fetuses between 35 and 40 weeks, and 89% of the fetuses postterm (Table 2). The small bowel peristalsis could be seen as rapidly changing size and appearance of fluid-filled loops of small bowel. The small bowel peristalsis could be dem-
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PARULEKAR 215
contents was not seen at any time during gestation. In two fetuses between 35 and 40 weeks gestation, there was suggestion of single rapid contraction of parts of the fetal colon.
DISCUSSION
Figure 3 39 weeks fetus . Transverse section. Small bowel loop (straight arrows), 21 mm in length, demonstrating val+ vulae conniventes as thin linear echoes within the lumen. Large oval area (open curved arrow) represents fluid-.filled small bowel measuring 8 x 11 mm.
onstrated in 9% of the fetuses between 25 and 30 weeks gestation, in 47% of the fetuses between 30 and 35 weeks gestation, in 73% of the fetuses between 35 and 40 weeks gestation, and 77% of the fetuses in postterm (>40 weeks) gestation (Table 2). Small bowel peristalsis was not seen prior to 27 weeks gestation. Active peristalsis of the colon or motion of the colonic
Between 8 and 10 weeks gestation, the fetal intestine is within the umbilical cord, near its entrance into the fetal abdomen. 4 The rapidly growing liver and the developing mesonephri encroach on the available space in the embryonic coelom (abdomen) so much that the intestine is extruded into the umbilical coelom, ie, that part of the extraembryonic coelom which lies in the proximal end of the umbilical cord. 5 At 10 weeks gestation, the proximal limb (ie, the small intestine) returns into the abdomen. By 11 weeks gestation, the majority of intestine returns, and by 12 weeks gesta · tion, all the intestine returns into the abdomen.4 By transvaginal sonogram, the herniated intestine was seen as a solid hyperechoic area within the proximal end of the umbilical cord, between 10 and 11 weeks gestation (Fig. 1). Further investigation is necessary to determine how often normal herniation of bowel can be demonstrated in early gestation by transvaginal sonography. Normal herniation of small bowel into umbilical cord, between 8 and 10 weeks gestation, has been previously demonstrated by transabdominal sonography.6 Therefore, it has been suggested that the diagnosis of abdominal wall defect should not be made sonographically before 14 weeks of menstrual age. 6
Figure 4 35 weeks fetus. The entire colon is demonstrated. A, B, C are coronal sections. A, The cecum, ascending colon, and proximal transverse colon are demonstrated (arrows). Notice haustral folds in the cecum seen as hyperechoic lines in the lumen. B, urinary bladder. B, Transverse colon (arrows) is demonstrated. B, urinary bladder.
A
B
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c
D
Figure 4 C, Descendjng colon, sigmoid colon, and rectum are demonstrated (arrows) . Stomach is seen medial to the proximal descending colon. D, Transverse section, showjng peripherally located colon (arrows). SP, spine.
In early gestation (10 to 20 weeks), the small bowel lumen is quite difficult to demonstrate. The region of the small bowel, however, can be seen and appears as a hyperechoic (relative to fetal liver) area in the abdomen and pelvis. This hyperechoic appearance around the small bowel persists throughout the pregnancy and it was seen in all the fetuses in this study. Before 20 weeks gestation, especially between 12 and 16 weeks
gestation, this hyperechoic area, when seen, fills a large portion of the fetal pelvis and lower abdomen. In later gestation, the hyperechoic area becomes less prominent and is more centrally located in the fetal abdomen. Hyperechoic appearance could be secondary to reflections from walls of collapsed loops of small bowel. Hyperechoic appearance could also be from mesenteric fat between loops of collapsed small bowel, since in
Figure 5 Coronal sections. A, 31 weeks fetus. Descending colon, sigmoid and rectum are seen (arrows). Colon lumen 4 to 7.5 mm. Meconium appears quite hypoechoic. 8, 41 weeks fetus. Right colon and cecum are seen (arrows). Colon lumen 28 mm near cecum. Meconium much more echogenic than in A. 8, urinary bladder.
A
B
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PARULEKAR
217
Table 2: Detection Rate of Small Bowel Peristalsis and Colonic Haustral Folds Gestational . A Small Bowel Colome Haustral geks , Peristalsis, % Folds, % wee
>40 35- 40 30- 35 25- 30 20- 25 15- 20 10- 15
73
89 89
9
78 61
77
47 0
7
0
0
0
0
Gestational ages are menstrual ages.
c Figure 6 A, 15 weeks fetus. Sagittal section. Small bowel appearing as a hyperechoic area (arrows) anterior to sacrum, mimics pathologic mass. SP, spine. H, fetal head. B, 36 weeks fetus. Transverse section. Small bowel, appearing as a large hyperechoic area (arrows) anterior to the spine (SP), mimics pathologic mass. C, 32 weeks fetus. Sagittal section. Rounded hyperechoic area (closed arrows) represents small bowel her• niated into umbilical cord (ope11 arrows) in a fetus with omphalocele. B, urinary bladder.
A
B
later gestation, spaces between loops of fluid-filled small bowel also appear hyperechoic (Fig. 2, D and E). In some fetuses, especially before 20 weeks gestation, this hyperechoic area can be unusually prominent and should not be mistaken for a pathologic mass (Fig. 6A).7·e Follow-up sonograms in a few weeks will show change in appearance or complete disappearance of this hyperechoic area, thus excluding the possibility of pathologic mass. ~ Between 13 and 20 weeks gestation, small (1 to 1.5 mm in diameter) hypoechoic rounded areas may appear within this hyperechoic region. These probably represent small bowel lumen and when clearly seen should distinguish this hyperechoic area from a pathologic mass. Occasionally, even in later gestation (after 20 weeks), collapsed small bowel may appear as a large hyperechoic area and mimic a pathologic mass (Fig. 6B). Increased echogenicity in the fetal abdomen has been described secondary to calcifications in meconium per· itonitis, infection, neoplasms, and unknown causes.1• 9 Calcifications appear as scattered hyperechoic areas in liver, spleen, or peritoneal cavity, some associated with acoustic shadowing. Cystic mass with hyperechoic margin secondary to calcified wall may be seen in meconium pseudocyst formation secondary to meco·
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nium peritonitis Normal hyperechoic small bowel appears as a large focal area of increased echogenicity in the lower fetal abdomen and is not associated with shadowing, cystic masses, or other abnormal findings, such as ascites or polyhyramnios. In later gestation, presence of fluid-filled loops, frequently with visible peristalsis, helps differentiate the hyperechoic small bowel from pathologic mass. Meconium ileus may present with nonshadowing areas of increased echo ~ genicity in fetal lower abdomen and may be difficult to distinguish from normal small bowel in early gestation. Change in appearance of the hyperechoic area on follow-up sonograms, presence of normal fluid-filled loops with peristalsis within the hyperechoic area, and absence of proximal dilatation of small bowel may be helpful to distinguish normal hyperechoic small bowel from a nonshadowing area of increased echogenicity due to meconium ileus. The knowledge that collapsed (empty) loops of small intestine appear hyperechoic can be helpful in diagnosing omphalocele. The omphalocele can occasionally appear as a small solid hyperechoic mass within the proximal end of the umbilical cord, near its entrance into the abdomen (Fig. 6C). The hyperechoic mass represents collapsed loops of small bowel herniated into the umbilical cord. In this case, postnatal abdominal radiographs, small bowel series, and surgery confirmed the presence of small bowel in the omphalocele. No other organs were found within the omphalocele. The small bowel is located centrally in the abdomen and pelvis, and the fluid -filled small bowel loops appear as rounded areas. However, in later gestation, longer segments of the fluid· filled small bowel loops can be demonstrated (Fig. 3). The valvulae conniventes cannot be routinely demonstrated within the small bowel lumen. The valvulae could be demonstrated in only 9 of 243 patients (Fig. 3). Fetal intestinal musculature is poorly developed and peristalsis is weak and discontinuous until birth. 4 After 27 weeks gestation, the small bowel peristalsis could be demonstrated with increasing frequency with increasing gestational age. Active peristalsis of the colon or motion of the colonic contents was not seen at any time during gestation. In two fetuses between 35 and 40 weeks gestation, there was suggestion of single rapid contraction of parts of the fetal colon. The colon could be recognized by its anatomic locain the peripheral portion of the abdomen as well as its known anatomic configuration. Usually only parts of the colon could be demonstrated. Occasionally, especially in later gestation (after 30 weeks), almost the entire colon could be demonstrated (Fig. 4). The haustral folds, which also could be frequently demonstrated, differentiate the colon from the small bowel (Fig. 7). It has been stated that fetal colon lacks haustra and haustra develop in the first 6 months after birth. 4
A
B Figure 7 A, 30 weeks fe tus. Small haustral folds (black arrows) a1e seen in the colon. B, 38 weeks fetus. Larger haustral folds (arrows) are seen in the colon . Indentation and puckering of colon wall (black arrow) is seen near the haustral
fold .
However, in this study, haustral folds in the lumen of the colon were seen quite frequently.. Haustral indentations on the surface of the colonic wall or sacculations were rarely seen (Fig. 78). .In early gestation, haustral folds appear as thin linear echoes within the lumen of the colon. In later gestation, as the colon diameter increases, the haustral folds becomes longer and thicker. Occasionally the haustral folds can be quite prominent. After 14 weeks gestation, lipid is absorbed from the fetal colon, and the remaining contents collect in the
J Ultrasound Med 10: 211- 220, 1991
colon as meconium. 4 In all fetuses, the meconium within the lumen of the colon appeared hypoechoic relative to the fetal liver and in comparison with bowel wall. Rarely, near term, meconium became almost isoechoic with fetal liver. However, meconium was never seen to be hyperechoic during normal pregnancy. The echogenicity of the meconium appeared to increase slightly with increasing gestational age (Fig. 5). Occasionally, the meconium can appear quite anechoic. Prominent anechoic rounded segment of the transverse Figure 8 A, 36 weeks fetus. Coronal section. Rounded anechoic colon (C) mimics double-bubble sign of duodenal atresia. ST, stomach; B, urinary bladder. B, 40 weeks fetus. Transverse section. Rounded anechoic colon (arrows) mimics cystic mass. B, urinary bladder.
A
PARULEKAR 219
colon, located close to the fetal stomach, can mimic the double-bubble sign of duodenal atresia (Fig. 8A). By scanning in different planes, however, this rounded anechoic structure can be demonstrated to be part of the transverse colon. Prominent, rounded parts of the colon, especially the sigmoid colon, can also mimic pathologic mass, such as an ovarian cyst, in the pelvis (Fig. 88). The measurements of average maximum diameter of the lumen of the small bowel and colon in this study are similar to those published by Nyberg et al. 1 The largest diameters of the small bowel lumen (8 mm) and colon lumen (28 mm) demonstrated in this study are larger than those published by Nyberg et al. The colon, the small bowel lumen, and the small bowel peristalsis were seen earlier and more frequently in this study, perhaps partly because of a much larger number of fetuses examined in this study. In conclusion, the possibility of pathologic bowel dilatation should be considered if the lumen measurements exceed those described for different gestational age groups (Table 1). Near term, the small bowel lumen diameter should not exceed 6 mm and the colon lumen diameter 23 mm, even though the largest diameters in normal fetuses in this study were 8 mm for small bowel in one fetus near term, and for the colon, 26 mm near term and 28 mm postterm in two fetuses. Dilated bowel may be seen in fetal abdomen secondary to atresia, malrotation, or meconium ileus. 9 The diameter of small bowel and colon lumen increases progressively with increasing gestational age. The length of the contiguous bowel segment that is visible also increases progres• sively with increasing gestational age. Small bowel peristalsis can be seen with increasing frequency after 27 weeks gestation. Colon peristalsis is not seen. Haustral folds in the colon can be frequently demonstrated, whereas valvulae conniventes in the small bowel are rarely seen. Meconium in the colon always remained hypoech•.liC relative to the fetal liver and bowel wall. Hyperechoic appearance of the small bowel in early gestation and anechoic cystic appearance of colon in later gestation may mimic pathology. Normal hernia· tion of small bowel within the umbilical cord at its insertion into the fetal abdomen may be seen between 8 and 11 weeks gestation.
REFERENCES
B
1. Nyberg DA, Mack LA, Patten RM, et al: Fetal bowel: Normal sonographic findings. J Ultrasound Med 6:3, 1987 2. Lee TC, Warren BH: Antenatal ultrasonic demonstration of fetal bowel. Radiology 124:471, 1977 3. Zilianti M, Fernandez S: Correlation of ultrasonic images of fetal intestine with gestational age and fetal maturity. Obstet Gynecol 62:569, 1983
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4. England, MA: Color Atlas of Life Before Birth. Chicago, Year Book Medical Publishers, Inc., 1983; pp 132, 138 5. Wamick R, Williams P (eds): Gray'!i Anatomy. Philadel· phia, WB Saunders Co, 1973, p 173 6. Cyr DR, Mack LA, Schoenecker SA, et al: Bowel migra ~ tion in the normal fetus: US detection. Radiology 161:119, 1986 ~ 7. Fakhry J, Reiser M, Shapiro LR, et al: Increased echogen
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icity in the lower fetal abdomem A common normal variant in the second trimester. J Ultrasound Med 5:489, 1986 8. Lince OM, Pretorius DH, Manco-Johnson ML: The clinical significance of increased echogenicity in the fetal abdomen. AJR 145:683, 1985 9.. Goldstein RB, FiUy RA, Callen PW: Sonographic diagnosis of meconium ileus in utero. J Ultrasound Med 6:663, 1987
