Abstract
Background
Microcolon helps diagnose small bowel atresia (SBA) using contrast enema. However, there are no ultrasonography (US) microcolon criteria for diagnosing SBA. Therefore, this study aimed to evaluate colon accuracy and other characteristics for diagnosing SBA by US, using surgical or clinical information as the reference standard.
Methods
US was performed on 46 neonates aged ≤ 7 days old. In the study group (n = 15), neonates with SBA were confirmed following surgery. In the study group without SBA (n = 15), neonates with other gastrointestinal problems besides SBA were confirmed by surgical or clinical follow-up. Sixteen neonates without gastrointestinal problems were classified as the control group. The colonic diameter was measured, and colonic gas was sought and observed. Statistical analysis was performed to compare US parameters between the study group and other two groups. The optimal cut-off value of the colonic diameter for SBA diagnosis was obtained using receiver operating characteristic analysis.
Results
Colonic diameters (0.5 cm) in the study group (interquartile ranges [IQR], 0.5–0.6 cm) was significantly smaller than that in the group without SBA (0.9 cm; IQR, 0.8–1.2 cm) (P < 0.001) and in the control group (1.2 cm; IQR, 0.8–1.35 cm) (P < 0.001). Optimum cut-off value for diagnosing SBA was 0.65 cm (sensitivity, 90.3%; specificity, 86.7%; accuracy, 89.1%) for the colonic diameter. Combining microcolon and gas-negativity showed the best performance in SBA diagnosis using US, with increased accuracy (91.3%).
Conclusion
A colon < 0.65 cm in diameter should be called a microcolon; combining US with gas-negativity is an essential diagnostic basis for SBA.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12887-022-03629-z.
Keywords: Neonate, Intestinal atresia, Intestinal obstruction, Ultrasonography, Small bowel atresia
Background
Congenital small bowel atresia (SBA), including duodenal, jejunal, and ileal atresia, is a common cause of neonatal intestinal obstruction, with an incidence ranging from 1.3 to 2.8 of 10,000 live births [1]. Prenatal ultrasound can be used to diagnose intestinal obstruction, but it can only play a role of preliminary screening for SBA, as dilated bowel loops and polyhydramnios provide a low overall detection rate [2, 3]. Neonates with SBA need further examination for diagnosis after birth. Diagnosing neonatal SBA primarily depends on clinical manifestations and imageological examination. Plain abdominal radiographs can be used to investigate intestinal obstruction. Upper gastrointestinal contrast studies can identify obstruction levels and rule out volvulus and malrotation diseases [4]. A contrast enema helps investigate suspected Hirschsprung disease [5]. Although barium and water-soluble enema can detect microcolon and facilitate SBA diagnosis, the radiation and risk of intestinal perforation have led many scholars to recommend minimising their use [6–9]. Ultrasonography (US), a safe, convenient and inexpensive imaging method, is suitable for neonates because of their thin abdominal wall. The microcolon without gas, significantly smaller than a normal colon, can be used to diagnose SBA by US [10]. However, no standard colonic measurement is available for new-borns because of the lack of consistency in US scans. Moreover, there is no standard diametric value for diagnosing SBA, which limits the diagnostic ability of clinical sonographers. A better US method for differentiating patients with SBA from those without SBA could reduce the need for contrast enema and upper gastrointestinal contrast. Therefore, this study aimed to evaluate colon accuracy and other characteristics for diagnosing SBA by US, using surgical or clinical information as the reference standard.
Methods
Patients
Institutional review board approval was obtained for this study. The need for informed consent was waived because our examination was performed as a routine abdominal US. Between July 2019 and October 2021, 71 consecutive neonates aged ≤ 7 days underwent US in our hospital’s ultrasound department (Fig. 1). Of these, 19 neonates were excluded because they underwent upper gastrointestinal or contrast enema before US. Furthermore, we excluded five neonates whose colon could not be identified clearly using ultrasound and one who was lost to follow-up. Consequently, 46 neonates were included in our study (male-to-female ratio, 25:21; preterm-to-term ratio, 20:26). Thirty neonates who were vomiting underwent upper gastrointestinal contrast or contrast enema after the ultrasound examination. As a study group, SBA was confirmed at surgery in 15 vomiting cases (male-to-female ratio, 7:8; preterm-to-term ratio, 5:10), including duodenal (n = 2), jejunal (n = 7), and ileal atresia (n = 6). In the group without SBA, 15 vomiting cases with other gastrointestinal illnesses besides SBA were confirmed with surgical or clinical follow up (male-to-female ratio, 9:6; preterm-to-term ratio, 5:10), including annular pancreas (n = 5), intestinal stenosis (n = 3), anal atresia (n = 1), congenital megacolon (n = 2), gastroesophageal reflux (n = 1), and neonatal vomiting (n = 3), according to surgery or upper gastrointestinal contrast. The remaining 16 cases without gastrointestinal problems were classified as the control group (male-to-female ratio, 9:7; preterm-to-term ratio, 10:6). We recorded their postnatal time, and clinical follow-up was carried out until they were 1 month old (Table 1).
Fig. 1.
Flow diagram of inclusion criteria of neonates
Table 1.
Clinical data findings of patients with study group and other groups
| Variable | Study group(n = 15) | Study group without SBA(n = 15) | Control group(n = 16) | P Value |
|---|---|---|---|---|
| Male-to-female ratio | 7:8 | 9:6 | 9:7 | 0.715†, 0.724‡ |
| Preterm-to-term ratio | 5:10 | 5:10 | 10:6 | 1.000†, 0.156‡ |
| Patient age (days)* | 1 (0.71, 2 ), (0.58-7) | 1 (0.63, 3), (0.54-4) | 2 (1, 4.5) (0.16-6) | 0.3129 |
| Clinical feature | duodenal atresia (n = 2), jejunal atresia (n = 7), ileal atresia (n = 6) | annular pancreas (n = 5), intestinal stenosis (n = 3), anal atresia (n = 1), congenital megacolon (n = 2), gastroesophageal reflux (n = 1), neonatal vomiting (n = 3) |
jaundice (n = 12) exomphalos (n = 4) |
Study group, SBA neonates;
Study group without SBA, neonates with gastrointestinal problems different that SBA;
Control group, neonates without gastrointestinal disease
*Data are median (quartile), followed with the ranges in parentheses
† The P value concerns statistical comparison between study group and study group without SBA. The χ2 test was used for statistical comparison
‡ The P value concerns statistical comparison between study group and control groups. The χ2 test was used for statistical comparison.
US techniques
Neonates underwent US using 3–9 MHz (Philips iU22, Philips Healthcare, Bothell, WA, USA) and 5–12 MHz transducers (Philips EPIQ7C, Philips Healthcare, Bothell, WA, USA). They were kept quiet by making them suck on a pacifier while the examinations were carried out. We measured the colon diameter at the left kidney’s transverse level (Fig. 2). We also measured the diameter of the smallest small bowel of the abdomen. Subsequently, we evaluated the presence of micro small bowel and the presence of gas in the colon and small bowel. The micro small bowel was defined as the small bowel diameter < 0.6 cm. Gas-negative colon was defined as the absence of gas in the measured colon (Video 1). A gas-negative small bowel was defined as the absence of gas in the micro small bowel on an ultrasound image (Fig. 3) (Video 2). US was performed by one operator with > 10 years of experience with paediatric US. Two other paediatric radiologists with > 5 years of experience performed all measurements and evaluations offline. Differences in opinions were resolved through discussions, when necessary.
Fig. 2.
Transection US images of the colon. (a) Schematic diagram of colon position on ultrasound. The letter ‘C’ in the lumen represents the likely location of the colon. Sto: stomach, SP: spine, LK: left kidney, AO: abdominal aorta, ICV: inferior cava vena (b) descending colon (arrow) without gas in a 2-day-old female neonate with SBA. The colon is small and without gas. (c) descending colon (arrow) without gas in a 1-day-old female neonate with an annular pancreas. There is little fluid and no gas in the colon. (d) descending colon (arrow) with gas in a 2-day-old female healthy neonate. There is some fluid and a little gas in the colon
Fig. 3.
US shows the small bowel. (a) Gas negative in the small bowel. A 1-day-old female neonate with SBA. The micro small bowel has no gas or content (arrow). (b) Gas negative in the small bowel. A 1-day-old female neonate with an annular pancreas. The micro small bowel has no gas or content (arrow). (c) Gas in the small bowel. A 2-day-old male healthy neonate. So much gas in the micro small bowel (arrow)
Statistical analysis
Data are presented as medians and interquartile ranges (IQRs). The nonparametric Wilcoxon test for paired data was used to test the difference between the study group and the other groups. The chi-squared and fisher exact tests were used to assess categoric data (neonatal sex, preterm or term, presence of micro small bowel, gas in small bowel and colon or not). The kruskal-wallis test was used to test the difference of ages between three groups. Receiver operating characteristic (ROC) curves were constructed to assess colon diameter and yielded the most accurate SBA diagnosis. Fifteen neonates with SBA and 31 without SBA were included in the ROC analysis. The optimal cut-off points for SBA prediction were identified from the highest Youden index. Areas under the ROC curves with 95% confidence intervals were calculated for the colon diameter. The cut-off value’s sensitivity and specificity for the colon diameter were calculated. We evaluated the sensitivities and specificities of other US SBA abdominal findings (presence of micro small bowel and the presence or absence of gas in the small bowel and colon), in combination with the preceding criteria for colon diameter, to assess the diagnostic accuracy added with measurement of the colon size. Statistical analysis was performed with IBM SPSS version 26.0 (IBM Corp. New York, USA). A two-tailed P-value < 0.05 indicates a statistically significant difference.
Results
US abdominal findings
Clinical characteristics (including preterm or term, male or female, and ages) between the study group and other groups showed no significant difference (P > 0.05) (Table 1). The colonic diameter in the study group of 0.5 cm (IQR, 0.5–0.6 cm) was significantly smaller than that in the group without SBA (0.9 cm; IQR, 0.8–1.2 cm; P < 0.001) and in the control group (1.2 cm; IQR, 0.8–1.35 cm; P < 0.001) (Fig. 4). The micro small bowel was found in all 15 neonates with SBA; there was no gas in the micro small bowel and colon for all of them. Among neonates in the group without SBA, the micro small bowel was visualised in 80.0% (12 of 15), including annular pancreas (n = 5), intestinal stenosis (n = 3), congenital megacolon (n = 1), gastroesophageal reflux (n = 1), and neonatal vomiting (n = 2). The proportion of gas-negativity in the small bowel was approximately 40.0% (6 of 15), including annular pancreas (n = 2), intestinal stenosis (n = 2), congenital megacolon (n = 1), and neonatal vomiting (n = 1). The proportion of gas-negativity in the colon was approximately 26.0% (4 of 15), including annular pancreas (n = 1), intestinal stenosis (n = 2), and anal atresia (n = 1). In the control group, the micro small bowel was noticeable in 68.8% (11 of 16); there were gas-negative small bowels in 25.0% (4 of 16) of the cases. Only one neonate, aged 4 h postnatal (the youngest), had a gas-negative colon. There was no significant difference in the presence of micro small bowel between the study group and the group without SBA (P = 0.224). Neonates in the study group had more micro small bowels than those in the control group (P = 0.043). There were significant differences in the gas-negative colon and small bowel between the study group and other groups (P < 0.001); neonates in the study group had less gas in the colon and distal small bowel (Table 2).
Fig. 4.
The nonparametric Wilcoxon test for paired data was used to test the difference in colonic diameter between the study group and the other groups
Table 2.
Comparison of US findings of small bowel and colon in the three groups
| US Finding | Study group ( n = 15 ) | Study group without SBA ( n = 15 ) | Control group ( n = 16 ) | P value |
|---|---|---|---|---|
| Colon diameter (IQR) | 0.5 cm (0.5–0.6 cm) | 0.9 cm (0.8-1.2 cm) | 1.2 cm (0.8-1.35 cm) | < 0.001†; 0.001‡ |
| Micro small bowel (<0.6 cm) | 15 (100%) | 12 (80%) | 11 (68.8%) | 0.224†; 0.043‡ |
| Gas negative in small bowel | 15 (100%) | 6 (40%) | 4 (25%) | < 0.001†; 0.001‡ |
| Gas negative in colon | 15 (100%) | 4 (26.0%) | 1 (6.3%) | < 0.001†; 0.001‡ |
IQR, interquartile ranges
† The P value concerns statistical comparison between study group and study group without SBA. The χ2 test was used for statistical comparison
‡ The P value concerns statistical comparison between study group and control group. The χ2 test was used for statistical comparison
Cut-off value and accuracy
According to the ROC analysis, the optimal cut-off value of the colon was defined as 0.65 cm (area under the ROC curve, 0.924). This criterion showed 90.3% (28 of 31) sensitivity, 86.7% (13 of 15) specificity, and 89.1% (41 of 46) accuracy. When the colonic diameter was 0.85 cm, the criterion showed a 71.0% (22 of 31) sensitivity and a 100% (15 of 15) specificity. Combining the colonic diameter and the micro small bowel produced a sensitivity of 93.5% (29 of 31), a specificity of 86.7% (13 of 15), and an accuracy of 91.3% (42 of 46). Combining the colon diameter and gas-negativity in the small bowel showed a sensitivity of 87.1% (27 of 31), a specificity of 100% (15 of 15), and an accuracy of 91.3% (42 of 46) (Table 3). Combining the colonic diameter and gas-negativity provided a sensitivity of 93.5% (27 of 31), a specificity of 100% (15 of 15), and an accuracy of 91.3% (42 of 46). Combining the colon diameter and colonic gas-negativity showed the best performance in SBA US diagnosis, with the highest area under the curve (AUC) (Fig. 5).
Table 3.
Diagnostic performance of the combination of each US findings for SBA.
| US Finding of abdomen | True-Positive Findings in Patients with SBA (n = 15) | True-Negative Findings in Neonate Without SBA (n = 31) | Sensitivity (%) | Specificity (%) | Accuracy (%) | 95% CI | AUC |
|---|---|---|---|---|---|---|---|
| Colon diameter | 13 | 28 | 0.903 | 0.867 | 0.8913 | 0.8466-1 | 0.9237 |
| Colon diameter and micro small bowel | 13 | 29 | 0.935 | 0.867 | 0.9130 | 0.8648-1 | 0.9366 |
| Colon diameter and gas negative in small bowel | 15 | 27 | 0.871 | 1.0 | 0.91304 | 0.9268-1 | 0.9699 |
| Colon diameter and gas negative in colon | 15 | 27 | 0.871 | 1.0 | 0.91304 | 0.9305-1 | 0.9720 |
CI, confidence interval; AUC, area under the curve
Fig. 5.
Using ROC analysis to find a combination of colon diameter with the other criteria
Discussion
Only a few ultrasound studies have focused on the neonatal intestine, possibly because it can be interfered by intestinal gas and stool mass. However, many intestinal diseases can be diagnosed by US even with interference [11–14]. US has become an important diagnostic method in many children’s diseases, including intussusception [15], intestinal malrotation [16, 17], and intestinal polyp [18]. US is important to neonates in diagnosing necrotising enterocolitis [19]. The proximal intestine is often dilated for neonates with SBA, filling with amniotic fluid or milk. In contrast, to avoid aspiration and relieve pain, clinicians usually carry out gastrointestinal decompression for neonates when an intestinal obstruction is suspected, which leads to the production of more intestinal gas, relieves the dilation state, and disturbs doctors from finding the dilated bowel. The distal SBA intestine was not affected by swallowing and gastrointestinal decompression. Since no amniotic fluid and milk were passed, the distal intestine (including the colon and a part of the small bowel) remained in a state of reduction for a long time. It only has a little meconium content and is without any gas. These characteristics are easily detected on ultrasound and can be used to distinguish other types of intestinal obstruction. Briefly, the present study examined the distal small bowel and colon characteristics to determine the accuracy of the SBA diagnosis.
The microcolon has been recognised and proposed by surgeons for nearly 100 years [20]. It has now become an important basis for contrast enema in diagnosing SBA; however, it was barely mentioned on the US. Although Hao [10] reviewed the ultrasonographic findings of 19 neonates with SBA and confirmed that US could detect microcolon without gas, the study did not provide the criteria of microcolon and the data on false-negative and -positive rates. To ensure consistency, we selected a transverse view of the left kidney showing the short colonic axis for measurement. This area was chosen because the anatomic locations of the descending colon are more constant and hardly disturbed by intestinal gas at the specified section. Finding a colon requires some experience and patience. Gentle pressure is applied, if necessary, to avoid the influence of crying. Furthermore, there is a need to avoid treating dilated small bowel as colon. In this study, five neonates had an unclear or unexplored colon. In addition to the high display rate (93.0%, 67/71), the colonic diameter of the study group was significantly smaller than that of the other two groups, indicating that the colonic diameter has a more intuitive value in SBA diagnosis. Combined with the cut-off value of the ROC curve, we believe that the ultrasonic colon with a diameter of < 0.65 cm has the maximum predictive value for SBA, called ultrasonic microcolon. On ultrasound, SBA can be ruled out when the colon diameter is > 0.85 cm.
We postulated that distal micro small bowel might be a secondary change of the SBA due to prolonged complete obstruction. But it is difficult to assess and make repeatable measurements. Because these distal micro small bowel perform small, peristalsis slower, have no fixed location, and are often obscured by dilated intestines. For atresia of or near the ileocecal junction, the micro small bowel may be absent or difficult to find [7]. We performed a periumbilical scan to find the section with the smallest intestine and the least intestinal gas for analysis. The diameter was < 0.6 cm and without wriggle, defined as the micro small bowel. Moreover, all neonates with SBA not only had micro small bowel but were also gas-negative. However, the micro small bowel was also present in the study group without SBA and the control group. It may be because the neonates have not accumulated food in the intestinal tract soon after birth. In particular, some neonates with heavy intestinal stenosis in the study group without SBA have a high proportion of micro small bowel.
Gas-negativity in the distal intestine is an essential diagnostic basis for SBA. Excluding few individuals has a biliary fistula [21]. In the study group without SBA, neonates without colonic gas were mostly patients with severe intestinal obstruction. In the control group, there was only one case of a 4-hour-old new-born, the youngest neonate, with a gas-negative colon. The gas in the intestinal lumen had not moved to the colon because the neonate did not eat much after birth. This shows that the absence of gas in the colon could be physiological during the first 4 h of their life. Since the amount of gas can be changed over time, finding a micro-small bowel without gas requires more experience, it cannot be an independent SBA diagnosis. Similarly, we did not find a time point for detecting false-positive gas negativities in the small bowel.
The current findings do not justify using colonic ultrasound as a substitute for contrast enema in diagnosing SBA; however, our study provides clinicians and neonates with more options. For neonates with suspected SBA, US can be done first; if SBA can be diagnosed, contrast enema administration may be cancelled. The difference in diagnostic accuracy between US and contrast enema requires further clarification.
Our study had some limitations. Firstly, although our study spanned 2 years, we did not have enough cases, including the control group of normal new-borns, because they rarely received routine abdominal ultrasounds. More clinical data need to be accumulated for comparison in differentiating colonic diameter between SBA and other diseases, including meconium ileus, even if no case was gathered in this study. Secondly, it is challenging to determine accurately the amount of micro small bowels, and the amount of gas in it can change over time. The results may vary depending on the doctor’s experience. Thirdly, considering the benefits of timely gastrointestinal decompression, we could not require eliminating gastrointestinal decompression in suspicious SBA neonates before US. Therefore, proximal bowel dilation was not analysed in this study. However, contrast enema or upper gastrointestinal contrast cannot be performed before an ultrasound examination is still required.
Conclusion
A colon < 0.65 cm in diameter should be called a microcolon; combining US combined with gas-negativity is an essential diagnostic basis for SBA.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Acknowledgements
Not applicable.
Abbreviations
- SBA
small bowel atresia
- US
ultrasonography
- IQR
interquartile ranges
- ROC
receiver operating characteristic
Author contribution
Ying Huang designed the study. Hao Ju wrote the main manuscript text. Shu Feng prepared figures and tables. All authors reviewed the manuscript.
Funding
This study was supported by grants from the Guide Project for Key Research and Development Foundation of Liaoning Province (No. 2019JH8/10300008), 345 Talent Project and Liaoning BaiQianWan Talents Program.
Data availability
All data generated or analysed during this study are included in this published article and its supplementary information files.
Declarations
Ethics Appapprovald Conconsent Participate
The need for written informed consent was waived by the Shengjing hospital ethics committee due to the retrospective nature of the study. All methods were carried out per relevant guidelines and regulations. The Shengjing hospital ethics committee approved all experimental protocols.
Consent for Publication
The written informed consent was obtained from all the Legally authorized representatives of the patients and participants for the publication of identifiable data.
Competing interests
The authors declare no conflict of interest, financial or otherwise.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Hemming V, Rankin J. Small intestinal atresia in a defined population: occurrence,prenatal diagnosis and survival. Prenat Diagn. 2007;27:1205–11. doi: 10.1002/pd.1886. [DOI] [PubMed] [Google Scholar]
- 2.Shinar S, Agrawal S, Ryu M, Van Mieghem T, Daneman A, Ryan G, et al (2020) Fetal Meconium Peritonitis Prenatal Findings and Postnatal Outcome: A Case Series, Systematic Review, and Meta-Analysis. Ultraschall Med. Jun 23. English.10.1055/a-1194-4363. [DOI] [PubMed]
- 3.Virgone C, D’antonio F, Khalil A, Jonh R, Manzoli L, Giuliani S. Accuracy of prenatal ultrasound in detecting jejunal and ileal atresia: systematic review and meta-analysis. Ultrasound Obstet Gynecol. 2015;45(5):523–9. doi: 10.1002/uog.14651. [DOI] [PubMed] [Google Scholar]
- 4.Morris G, Kennedy A, Jr, Cochran W. Small Bowel Congenital Anomalies: a Review and Update. Curr Gastroenterol Rep Apr. 2016;18(4):16. doi: 10.1007/s11894-016-0490-4. [DOI] [PubMed] [Google Scholar]
- 5.Carroll AG, Kavanagh RG, Ni Leidhin C, Cullinan NM, Lavelle LP, Malone DE. Comparative Effectiveness of Imaging Modalities for the Diagnosis of Intestinal Obstruction in Neonates and Infants: A Critically Appraised Topic. Acad Radiol. 2016;23(5):559–68. doi: 10.1016/j.acra.2015.12.014. [DOI] [PubMed] [Google Scholar]
- 6.Yan J, Sun J, Wu R, Tan SS, Chen Y, Peng Y, et al. Barium enema findings in total colonic aganglionosis: a single-center, retrospective study. BMC Pediatr Oct. 2020;31(1):499. doi: 10.1186/s12887-020-02403-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Cserni T, Magyar A, Németh T, Paran TS, Csízy I, Józsa T. Atresia of the ileocecal junction with agenesis of the ileocecal valve and vermiform appendix: report of a case. Surg Today. 2006;36(12):1126–8. doi: 10.1007/s00595-006-3302-x. [DOI] [PubMed] [Google Scholar]
- 8.Duarte JOM, Pereira PMLP, Sobral ASG, de Oliveira JPR, Rita HJB, de Sousa E, Costa JA. Rectal perforation after barium enema: A case report. Clin Case Rep Nov. 2019;22(12):2565–7. doi: 10.1002/ccr3.2563. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Kim HS, Je BK, Cha SH, Choi BM, Lee KY, Lee SH. Renal excretion of water-soluble contrast media after enema in the neonatal period. Pediatr Neonatol. 2014;55(4):256–61. doi: 10.1016/j.pedneo.2013.07.012. [DOI] [PubMed] [Google Scholar]
- 10.Hao J, Zhang Y, Tianyu L, Bo S, Shu F, Feng S, et al. Preliminary Investigation of the Diagnosis of Neonatal Congenital Small Bowel Atresia by Ultrasound. Biomed Res Int Sep. 2019;29;2019:7097159. doi: 10.1155/2019/7097159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Bollegala N, Griller N, Bannerman H, Habal M, Nguyen GC. Ultrasound vs Endoscopy, Surgery, or Pathology for the Diagnosis of Small Bowel Crohn’s Disease and its Complications. Inflamm Bowel Dis Jul. 2019;17(8):1313–38. doi: 10.1093/ibd/izy392. [DOI] [PubMed] [Google Scholar]
- 12.Haas K, Rubesova E, Bass D. (2016) Role of imaging in the evaluation of inflammatory bowel disease: How much is too much? World J Radiol. Feb 28;8(2):124-31. 10.4329/wjr.v8.i2.124. [DOI] [PMC free article] [PubMed]
- 13.Taylor SA, Mallett S, Bhatnagar G, Baldwin-Cleland R, Bloom S, Gupta A, et al. METRIC study investigators. Diagnostic accuracy of magnetic resonance enterography and small bowel ultrasound for the extent and activity of newly diagnosed and relapsed Crohn’s disease (METRIC): a multicentre trial. Lancet Gastroenterol Hepatol Aug. 2018;3(8):548–58. doi: 10.1016/S2468-1253(18)30161-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Liu Z, Guo J, Wang S, Zhao Y, Liu Z, Li J, et al. Evaluation of Transabdominal Ultrasound with Oral Cellulose-Based Contrast Agent in the Detection and Surveillance of Gastric Ulcer. Ultrasound Med Biol. 2017;43(7):1364–71. doi: 10.1016/j.ultrasmedbio.2017.02.008. [DOI] [PubMed] [Google Scholar]
- 15.Zhang Y, Bai YZ, Li SX, Liu SJ, Ren WD, Zheng LQ. Sonographic findings predictive of the need for surgical management in pediatric patients with small bowel intussusceptions. Langenbecks Arch Surg Oct. 2011;396(7):1035–40. doi: 10.1007/s00423-011-0742-6. [DOI] [PubMed] [Google Scholar]
- 16.Zhang W, Sun H, Luo F. The efficiency of sonography in diagnosing volvulus in neonates with suspected intestinal malrotation. Med (Baltimore) Oct. 2017;96(42):e8287. doi: 10.1097/MD.0000000000008287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Garel J, Daneman A, Rialon K, Zani A, Fecteau A, Piero A. The role of sonography for depiction of a whirlpool sign unrelated to midgut malrotation in neonates. Pediatr Radiol. 2020;50(1):46–56. doi: 10.1007/s00247-019-04508-z. [DOI] [PubMed] [Google Scholar]
- 18.Zhang Y, Li SX, Xie LM, Shi B, Ju H, Bai YZ, Zhang SC. Sonographic diagnosis of juvenile polyps in children. Ultrasound Med Biol Sep. 2012;38(9):1529–33. doi: 10.1016/j.ultrasmedbio.2012.05.018. [DOI] [PubMed] [Google Scholar]
- 19.Kim JH. Role of Abdominal US in Diagnosis of NEC. Clin Perinatol. 2019;46(1):119–27. doi: 10.1016/j.clp.2018.10.006. [DOI] [PubMed] [Google Scholar]
- 20.Greig DM. Congenital Microcolon. Edinb Med J Apr. 1925;32(4):175–206. [PMC free article] [PubMed] [Google Scholar]
- 21.Puvabanditsin S, Botwinick M, Chen CW, Joshi A, Mehta R. Biliary Tract Abnormalities as a Cause of Distal Bowel Gas in Neonatal Duodenal Atresia. Case Rep Surg Jun. 2018;26;2018:8041427. doi: 10.1155/2018/8041427. [DOI] [PMC free article] [PubMed] [Google Scholar]
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Supplementary Materials
Data Availability Statement
All data generated or analysed during this study are included in this published article and its supplementary information files.