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Fluoroscopic Diagnosis of Malrotation: Technique, Challenges, and Trouble Shooting
ARTICLE IN PRESS Current Problems in Diagnostic Radiology 000 (2019) 1 13
Current Problems in Diagnostic Radiology journal homepage: www.cpdrjournal.com
Fluoroscopic Diagnosis of Malrotation: Technique, Challenges, and Trouble Shooting Sachin S. Kumbhar, MD*, Jing Qi, MD Medical College of Wisconsin, Milwaukee, WI
A B S T R A C T
A fluoroscopic upper gastrointestinal series is the most commonly used investigation for the diagnosis of malrotation and midgut volvulus. However, both false positive and false negative results can occur causing diagnostic confusion. Several physiologic states and pathologic conditions can mimic fluoroscopic appearance of malrotation. Proper fluoroscopic technique is essential to maximize diagnostic accuracy. In this pictorial essay, we discuss common diagnostic challenges in the diagnosis of malrotation and strategies radiologists can use to clarify the diagnosis in equivocal cases. © 2019 Elsevier Inc. All rights reserved.
Introduction Malrotation of the gastrointestinal (GI) tract is a congenital abnormality that predisposes patients to midgut volvulus, a potentially fatal condition.1 An upper GI fluoroscopic examination is commonly requested either on an urgent basis in children having bilious vomiting or in an outpatient setting in children with various abdominal symptoms. Several physiologic states can cause diagnostic confusion on upper GI series.2 It is important that the radiologists familiarize themselves with the optimal method of performing and interpreting a pediatric upper GI series to maximize diagnostic accuracy. In this review article, we discuss commonly encountered challenges in the diagnosis of malrotation and offer suggestions for troubleshooting. Definition, Embryology, and Etiopathogenesis Malrotation is a spectrum of disorders leading to abnormal position of the bowel in the abdomen due to abnormal embryologic bowel rotation.3 The gut in early embryonic period is a straight tube-like structure. As the gut lengthens during subsequent weeks, it also rotates 270° counterclockwise around the superior mesenteric artery (SMA) axis in several stages (Fig 1). Due to this rotation the cranial portion of the gut which forms the duodenum migrates to a location posterior to the SMA with the duodenojejunal junction (DJJ) to the left of SMA. The caudal portion of the gut which contains the cecum rotates counterclockwise from the left side of the abdomen
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. *Reprint requests: Sachin S. Kumbhar, MD, Medical College of Wisconsin, 8915 W Connell Ct, Milwaukee WI 53226. E-mail addresses: [email protected], [email protected] (S.S. Kumbhar). https://doi.org/10.1067/j.cpradiol.2019.10.002 0363-0188/© 2019 Elsevier Inc. All rights reserved.
in such a way that the cecum comes to rest in the right lower quadrant (RLQ).4 At completion of rotation, the ascending colon is fixed to the retroperitoneum on the right and the descending colon is fixed to the retroperitoneum on the left (Fig 2). Majority of the duodenum is also retroperitoneal.5 The small bowel mesentery has a wide root extending between 2 fixed points, the first being the DJJ in the left upper quadrant and the second being the ileocecal valve in the RLQ.6 The DJJ is suspended by the ligament of Trietz which is a peritoneal fold extending from the right esophageal crus of diaphragm and connective tissue around the coeliac artery and SMA.7 The ligament of Trietz is a surgically identifiable landmark and denotes the point where the small bowel becomes an intraperitoneal structure. Malrotation may affect small bowel or large bowel, or both.8 Any deviation from the normal pattern of intestinal rotation leads to an abnormal position of the DJJ and/or cecum. With decreased distance between the 2, the mesentery has a narrower root thus increasing the risk of twisting or volvulus.9 Abnormal rotation of the gut is also associated with peritoneal bands extending from the cecum to other structures which can cross the duodenum and cause obstruction.10
Clinical Features Malrotation affects about 1 in 500 live births. Vast majority of affected children present in the neonatal period, most commonly with bilious vomiting. Older children may present with nonspecific symptoms like intermittent vomiting, abdominal pain, and poor weight gain. Sometimes malrotation is an incidental finding on imaging done for other purposes.11 Malrotation is associated with several syndromes and disorders including but not limited to gastroschisis, congenital diaphragmatic hernia, omphalocele, and heterotaxy syndromes.10
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FIG 1. Diagrammatic representation of normal bowel rotation. The cephalad segment of the primitive gut including the duodenojejunal junction (D) rotates 270° anticlockwise around the superior mesenteric artery (straight arrow) to reach its normal location in the left abdomen (#). The caudal segment including the cecum (C) also rotates 270° anticlockwise to reach the right lower quadrant of the abdomen (*).
FIG 2. Normal anatomy at completion of rotation. The duodenojejunal junction (arrow) lies in the left upper quadrant and the cecum (*) is fixed to the retroperitoneum in the right lower quadrant. The third portion of the duodenum (double arrows) is located posterior to the superior mesenteric artery. Note that the mesentery has a wide root (arrowheads).
Normal Anatomy On a normal upper GI series, the proximal duodenum extends posteriorly from the pylorus, as seen on the lateral view, and extends toward the spine to its retroperitoneal location. The duodenum then crosses over to the left side of the spine and turns cranially to extend to the DJJ. The DJJ is identified on fluoroscopy as the cranial most and leftward most part of the bowel where it takes a definite inferior turn. A normally located DJJ should be to the left of the left-sided pedicle of the adjacent vertebral body (Fig 3). The DJJ
should be at the level of the duodenal bulb or higher on the frontal view and located posteriorly on the lateral projection.10,12,13 The proximal jejunal loops are usually located in the left upper quadrant and cecum in the RLQ. Upper GI Study Technique If the esophagus is to be evaluated, a left side down position should be used for the lateral view to avoid unintended gastric emptying. Esophageal evaluation in the right side down position
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FIG 3. Normal anatomy at upper GI study in a 6-year-old girl. (a) Frontal view of the abdomen demonstrates the duodenojejunal junction (arrow) located to the left of the left sided pedicle (arrowhead) and at the level of the duodenal bulb (double arrows). (b) Lateral view of the abdomen demonstrates a posterior location of the duodenojenjunal junction (arrow).
FIG 4. Use of abdominal compression to demonstrate the duodenojejunal junction in a 2-year-old girl. (a) Frontal view of the abdomen demonstrates contrast in the duodenum (arrow) and the proximal jejunum (arrowhead). The duodenojejunal junction is obscured by contrast within the stomach. (b) Frontal view of the abdomen obtained immediately after release of abdominal compression demonstrates the duodenojejunal junction (arrow) by displacing the stomach.
may cause early emptying of contrast into the duodenum causing the first pass of contrast through the duodenum to be missed. Volume of contrast used should be kept to minimum necessary as excessive contrast in the stomach can obscure the DJJ. Patients referred from the inpatient or emergency services may already have a nasogastric (NG) tube placed. Delivery of contrast through the NG tube can allow more control over contrast volume. It should however be kept in mind that in younger children postpyloric enteric tubes can distort anatomy and displace the DJJ. 14
Once desired amount of contrast has reached the stomach the child should be positioned in right side down position to assess extension of duodenum to the retroperitoneum. The radiologist should be vigilant and ready to image quickly as in some patients there is prompt gastric emptying in this position. After the proximal duodenum is opacified the child should be placed in supine position to assess position of the DJJ in the frontal view. Continuous fluoroscopy while the child is moved from the lateral to supine position is beneficial to capture the first pass of contrast through the duodenum.
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FIG 5. Use of watchful waiting and second bolus to demonstrate the duodenojejunal junction in a 20-month-old girl. (a) Frontal view of the abdomen demonstrates contrast in the proximal jejunum (arrow). The duodenojejunal junction was missed due to rapid transit. (b) Image obtained after few minutes demonstrates further propagation of contrast within the jejunum with relative clearance of the jejunal loops overlying the expected location of the duodenojejunal junction. (c) Second bolus of contrast was allowed to pass the duodenum demonstrating the duodenojejunal junction (arrowhead).
If there is a delay in movement of contrast through the third portion of the duodenum to the left, a transient left posterior oblique positioning of the patient may aid forward movement of contrast. The child then can be quickly returned to the supine position to document the anatomy. Once the location of the DJJ on the frontal view is documented, a lateral view should also be obtained to demonstrate its posterior retroperitoneal location. If the DJJ is obscured by contrast in the stomach gentle palpation to displace the stomach may aid in visualization of the DJJ
(Fig 4). The first pass of contrast through the duodenum may sometimes be missed if the stomach empties too quickly. Opacification of proximal jejunal loops may then hinder identification of the DJJ. If this happens intermittent fluoroscopy over next several minutes may be beneficial. After the contrast disperses within the jejunum the child may again be positioned in the right side down position and a second bolus of contrast may be allowed to enter the duodenum. A densely opacified DJJ can be identified through overlapping loops of jejunum (Fig 5). If the position of the DJJ remains equivocal
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FIG 6. Malrotation in a 12-month-old boy with bilious emesis. The duodenojejunal junction (arrow) is located medial to the left-sided pedicle (arrowhead) and inferior to the level of the duodenal bulb (double arrows). Malrotation was confirmed at surgery.
FIG 7. Subtle malrotation in a 2-year-old boy with vomiting. (a, b) Frontal views of the abdomen demonstrate the duodenojejunal junction (arrow) at the level of the duodenal bulb (double arrows) and medial to the left sided pedicle (arrowhead). Malrotation without volvulus was found at surgery.
the study should be extended to determine the position of proximal jejunal loops and the cecum.
Fluoroscopic Findings Malrotation An upper GI series is the preferred imaging study to diagnosis malrotation with sensitivity of 93%-100%.15-17 Demonstration of an abnormal position of the DJJ is the most important fluoroscopic finding to clinch the diagnosis. Findings that suggest malrotation are (1) the DJJ projects medial to the left-sided pedicle; (2) DJJ is inferior to the duodenal bulb; (3) DJJ is located more anterior than usual suggesting an intraperitoneal location (Fig 6).10,12,13 While most patients with malrotation have an obviously abnormal location of the DJJ, findings in some patients can be subtle causing diagnostic challenge. The DJJ may overlap the left-
sided pedicle or maybe only slightly inferior to the level of the duodenal bulb (Fig 7). If the lateral view demonstrates an intraperitoneal location of the DJJ confidence in the diagnosis of malrotation can be increased. Another finding suggesting malrotation is proximal jejunal loops located in the right upper quadrant of the abdomen. Most patients with malrotation also have an abnormal cecal location. It should however be noted that neither of this feature is specific in isolation (Fig 8). The cecum can be normally located in patients with malrotation.18
Midgut Volvulus Upper GI series has a reported sensitivity of 54% for midgut volvulus.17 Characteristic finding of midgut volvulus is a “corkscrew” appearance of proximal small bowel (Fig 9).19 Corkscrew appearance may not be apparent in patients with complete bowel
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FIG 8. Malrotation in a 4-month-old girl with situs inversus. (a) Frontal view of the abdomen demonstrates stomach in the right upper quadrant. Entire duodenum and part of the proximal jejunum are in the left upper quadrant. The duodenojejunal junction was not clearly identified due to excessive duodenal tortuosity. The jejunum crosses the midline to the right (arrow). (b) Frontal view of the abdomen from contrast enema study demonstrates the cecum (arrow) and appendix (arrowhead) in the left lower quadrant. The large bowel is normally rotated for patient’s situs.
FIG 9. Midgut volvulus without complete obstruction in an 8-year-old boy. Frontal oblique image from upper GI study demonstrates the classic “corkscrew” (arrows) appearance of the proximal jejunum. Midgut volvulus was confirmed at surgery.
obstruction as contrast will not enter the twisted loops of bowel. A beak-like tapering of the bowel may be seen in patients with complete obstruction (Fig 10). Watchful waiting or gentle abdominal compression may facilitate a small amount of contrast to clear past the obstruction to demonstrate the corkscrew pattern of the volvulized bowel (Fig 11).20
Peritoneal Bands Malrotation sometimes presents with duodenal obstruction due to peritoneal bands. The proximal duodenum will be dilated (Fig 12). If obstruction is incomplete contrast may extend beyond the point of obstruction and delineate the duodenal anatomy. The duodenum
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FIG 10. Midgut volvulus with complete obstruction in a 1-month-old boy. Frontal view from upper GI study demonstrates proximal duodenal dilation with beak like tapering (arrow) at the level of obstruction. Midgut volvulus was confirmed at surgery.
FIG 11. Midgut volvulus in a 1-day-old boy. (a, b) Frontal image from upper GI study demonstrates proximal duodenal dilation (a) with obstruction at the level of third portion of the duodenum (arrow). Image obtained after several minutes (b) shows that contrast has cleared past the obstruction to opacify narrowed bowel loops with corkscrew-like appearance (arrowheads). Midgut volvulus was confirmed at surgery.
may have a Z-shaped appearance in the presence of bands. The location of DJJ is usually abnormal. Challenging Cases Both false positive and false negative cases can occur in the fluoroscopic diagnosis of malrotation. The main reason for inaccurate diagnosis
is overlap between subtle abnormal position of the DJJ in malrotation and mild displacement of the DJJ due to other causes. False positive rates can be as high as 15% while false negative rates can reach up to 6%.21,22 The DJJ may be slightly inferior to the level of the duodenal bulb in infants with normal bowel rotation (Fig 13). This finding, which is more common in infants born prematurely, is thought to be due to relatively lax peritoneal structures in infants.13
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FIG 12. Obstructing duodenal band in a 13-year-old girl. Frontal image from upper GI study demonstrates dilation of the duodenal bulb (arrow) with abrupt narrowing in the second portion (arrowhead) of the duodenum. Obstructing peritoneal bands with malrotation was found at surgery.
FIG 13. Slight inferior location of the duodenojejunal junction in a 1-day-old girl. Frontal image from upper GI study demonstrates the duodenojejunal junction (arrow) to the left of the left sided pedicle and slightly inferior to the level of the duodenal bulb (arrowhead).
The DJJ in children younger than 4 years can be easily displaced by various physiologic and pathologic processes that cause enlargement of abdominal organs or gastric/bowel distention (Fig 14).23 Conditions than can displace the DJJ include, but are not limited to, gastric distention, chronic bowel dilation, colonic distension, splenomegaly, enlarged left kidney, liver transplant, and presence of an enteric tube.2,14 The DJJ is relatively fixed in children older than 4 years of age. Variations in duodenal anatomy can also cause diagnostic confusion. Wandering duodenum consists of redundancy of the duodenum that appears as a tortuous course on fluoroscopy (Fig 15). The DJJ is in the normal location. In mobile duodenum, the post bulbar proximal duodenum forms a loop in the right abdomen instead of being fixed to the retroperitoneum before crossing over to the left side (Fig 16).12,24 Duodenum inversum is a congenital
anomaly in which second portion of the duodenum extends superiorly and posteriorly on the right side of the spine. It then crosses over to the left at a level more cephalad than expected (Fig 17). The DJJ is in normal location.25,26 Trouble Shooting Attention to proper fluoroscopic technique is a key to increase the diagnostic accuracy of malrotation. Documenting first pass of contrast through duodenum and demonstrating position of the DJJ on both frontal and lateral views are important components of the exam.13 If the DJJ projects slightly medially than expected, a review of patients’ positioning for the image might be helpful. True supine positioning with patient’s back flat against the table is important.
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FIG 14. Inferior displacement of the duodenojejunal junction in a 7-year-old girl with gastric bezoar. Frontal image from upper GI study demonstrates the duodenojejunal junction (arrow) to the left of the left sided pedicle and inferior to the level of the duodenal bulb (double arrows). The stomach is distended with a filling defect due to a trichobezoar (arrowhead). Normal rotation of the bowel was confirmed at surgery.
FIG 15. Wandering duodenum in a 5-month-old boy. Frontal image from upper GI study demonstrates a tortuous course of the third portion (arrowheads) of the duodenum. The duodenojejunal junction (arrow) is in normal position.
An oblique position can cause the DJJ to project over the spine and lead to a false positive result (Fig 18). Symmetric appearance of the lower ribs is a good indication of a true supine position. Subtle inferior position of the DJJ is another source of diagnostic confusion. Review of the scout film might reveal a potential cause of a displaced DJJ such as a distended stomach, dilated
bowel, or splenomegaly. If the scout film reveals gastric distention, aspiration of gastric contents through a NG tube may aid in the DJJ coming back to its normal location (Fig 19). Review of patient’s charts and prior imaging may help to identify other sources of false positive results such as enlarged kidney or liver transplant.2
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FIG 16. Mobile duodenum in a 6-year-old boy. Frontal image from upper GI study demonstrates the second portion of the duodenum forming a loop (arrowhead) in the right abdomen. The duodenojejunal junction (arrow) is in normal position.
FIG 17. Duodenum inversum in a 1-month-old boy. Frontal image from upper GI study demonstrates normal course of the second portion (double arrows) of the duodenum. The third portion (arrowheads) courses cranially in the right abdomen and then crosses the midline at a higher level than usual. The duodenojejunal junction (arrow) is normally located.
Manual compression of the abdomen to determine the mobility of the DJJ can be used in children with equivocal position of the DJJ. The DJJ can be manually displaced in children with normal bowel rotation up to 4 years of age. It will however return to a normal location after the compression is released. In patients with malrotation the DJJ position may remain abnormal after release of compression.20,23 Radiologists should be familiar with physiologic variations in duodenal anatomy like wandering duodenum and mobile duodenum. While some duodenal redundancy is normal, excessive redundancy should raise suspicion for malrotation especially in the presence of angularity or kinking. Presence of more than one loop of the duodenum on the right of the spine is also abnormal and indicative of malrotation.12
Another strategy that can be employed in equivocal cases is to extend the study to determine the location of proximal jejunum and cecum. Contrast enema may also be performed to determine cecal location.10 While a right upper quadrant position of proximal jejunum can be seen in malrotation, this finding in isolation is not specific. Position of the cecum is abnormal in up to 80% children with malrotation.12,18 However, there is overlap with physiologic variations in cecal position. Regardless, demonstration of an obviously abnormal cecal/colonic position will be helpful to clear diagnosis. If the exam remains equivocal, repeat exam on another day should be considered (Fig 20). A repeat exam is convenient, more cost effective and less invasive compared to surgery. Repeat exam
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FIG 18. Oblique position causing diagnostic confusion in a 1-year-old boy. Fluoroscopic image from upper GI study demonstrates the duodenojejunal junction (arrow) projecting over the spine in the midline. A review of the lower ribs reveals asymmetrical appearance indicating oblique positioning. A repeat upper GI study (same as in FIG 4) performed subsequently demonstrated normal location of the duodenojejunal junction.
FIG 19. Use of gastric decompression to demonstrate normal anatomy in a 2-day-old boy. Initial frontal image from upper GI study (a) demonstrates medial location of the duodenojejunal junction (arrow) overlying the left sided pedicle. Note that the stomach is distended. Air was aspirated through the nasogastric tube to decompress the stomach. Repeat frontal image (b) demonstrates normal location of the duodenojejunal junction (arrowhead) to the left of the left sided pedicle.
may be performed using an enteric tube which allows for more control over contrast volume and can achieve better duodenal distention with lesser gastric opacification. Conclusions An upper GI series is the most commonly performed radiological test for the diagnosis of malrotation and midgut volvulus. Unfortunately, several physiologic and pathologic conditions can have a fluoroscopic appearance similar to subtle cases of malrotation causing
diagnostic dilemma. Proper technique in performing the upper GI study is vital to maximize diagnostic yield. The radiologist should be familiar with physiologic variations in duodenal anatomy. Several strategies such as gastric decompression, abdominal compression, demonstrating cecal position, and repeat study can be used in equivocal cases. Conflict of Interest The authors declare that they have no conflict of interest.
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FIG 20. Use of repeat upper GI study to demonstrate normal anatomy in a 1-year-old boy. Initial frontal image from upper GI study (a) demonstrates medial location of the duodenojejunal junction (arrow). Delayed abdominal radiograph (not shown) demonstrated cecum in the right lower quadrant. Repeat upper GI study performed on a later day (b) demonstrates normal location of the duodenojejunal junction (arrowhead). Medial displacement of the duodenojejunal junction on the initial study was thought to be caused by gaseous distention of the splenic flexure (double arrows) of the colon (c).
References 1. Shalaby MS, Kuti K, Walker G. Intestinal malrotation and volvulus in infants and children. BMJ 2013;347:f6949. 2. Smitthimedhin A, Suarez A, Webb RL, et al. Mimics of malrotation on pediatric upper gastrointestinal series: a pictorial review. Abdom Radiol (NY) 2018;43:2246–54. 3. Pickhardt PJ, Bhalla S. Intestinal malrotation in adolescents and adults: spectrum of clinical and imaging features. AJR Am J Roentgenol 2002;179:1429–35. 4. Aslanabadi S, Ghalehgolab-Behbahan A, Jamshidi M, et al. Intestinal malrotations: a review and report of thirty cases. Folia Morphol (Warsz) 2007;66:277–82. 5. Coffin A, Boulay-Coletta I, Sebbag-Sfez D, et al. Radioanatomy of the retroperitoneal space. Diagn Interv Imaging 2015;96:171–86. 6. Okino Y, Kiyosue H, Mori H, et al. Root of the small-bowel mesentery: correlative anatomy and CT features of pathologic conditions. Radiographics 2001; 21:1475–90. 7. Meyers MA. Treitz redux: the ligament of Treitz revisited. Abdom Imaging 1995;20:421–4. 8. Long FR, Kramer SS, Markowitz RI, et al. Radiographic patterns of intestinal malrotation in children. Radiographics 1996;16:547–56. discussion 56-60. 9. Hamidi H, Obaidy Y, Maroof S. Intestinal malrotation and midgut volvulus. Radiol Case Rep 2016;11:271–4. 10. Strouse PJ. Disorders of intestinal rotation and fixation (“malrotation”). Pediatr Radiol 2004;34:837–51.
11. Rittenhouse DW, Pucci MJ, Brumbaugh JL, et al. Congenital variants of gastrointestinal rotation found at resection of hepatopancreatobiliary tumors: a case series with review of the literature. Case Rep Pancreat Cancer 2016;2:6–13. 12. Long FR, Kramer SS, Markowitz RI, et al. Intestinal malrotation in children: tutorial on radiographic diagnosis in difficult cases. Radiology 1996;198:775–80. 13. Applegate KE, Anderson JM, Klatte EC. Intestinal malrotation in children: a problem-solving approach to the upper gastrointestinal series. Radiographics 2006;26:1485–500. 14. Merten DF, Mumford L, Filston HC, et al. Radiological observations during transpyloric tube feeding in infants of low birth weight. Perforation of the duodenum and variations in normal duodenal anatomy. Radiology. 1980;136:67–75. 15. Lin JN, Lou CC, Wang KL. Intestinal malrotation and midgut volvulus: a 15-year review. J Formos Med Assoc 1995;94:178–81. 16. Torres AM, Ziegler MM. Malrotation of the intestine. World J Surg 1993;17:326–31. 17. Seashore JH, Touloukian RJ. Midgut volvulus. An ever-present threat. Arch Pediatr Adolesc Med 1994;148:43–6. 18. Slovis TL, Klein MD, Watts FB Jr. Incomplete rotation of the intestine with a normal cecal position. Surgery 1980;87:325–30. 19. Peterson CM, Anderson JS, Hara AK, et al. Volvulus of the gastrointestinal tract: appearances at multimodality imaging. Radiographics 2009;29:1281–93. 20. Lim-Dunham JE, Ben-Ami T, Yousefzadeh DK. Manual epigastric compression during upper gastrointestinal examination of neonates: value in diagnosis of intestinal malrotation and volvulus. AJR Am J Roentgenol 1999;173: 979–83.
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21. Dilley AV, Pereira J, Shi EC, et al. The radiologist says malrotation: does the surgeon operate? Pediatr Surg Int 2000;16:45–9. 22. Prasil P, Flageole H, Shaw KS, et al. Should malrotation in children be treated differently according to age? J Pediatr Surg 2000;35:756–8. 23. Katz ME, Siegel MJ, Shackelford GD, et al. The position and mobility of the duodenum in children. AJR Am J Roentgenol 1987;148:947–51.
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24. Marine MB, Karmazyn B. Imaging of malrotation in the neonate. Semin Ultrasound CT MR 2014;35:555–70. 25. Kim ME, Fallon SC, Bisset GS, et al. Duodenum inversum: a report and review of the literature. J Pediatr Surg 2013;48:e47–9. 26. Dogan MS, Doganay S, Koc G, et al. Duodenum Inversum: findings from an upper gastrointestinal series. Sultan Qaboos Univ Med J 2016;16:e379–80.
Current Problems in Diagnostic Radiology journal homepage: www.cpdrjournal.com
Fluoroscopic Diagnosis of Malrotation: Technique, Challenges, and Trouble Shooting Sachin S. Kumbhar, MD*, Jing Qi, MD Medical College of Wisconsin, Milwaukee, WI
A B S T R A C T
A fluoroscopic upper gastrointestinal series is the most commonly used investigation for the diagnosis of malrotation and midgut volvulus. However, both false positive and false negative results can occur causing diagnostic confusion. Several physiologic states and pathologic conditions can mimic fluoroscopic appearance of malrotation. Proper fluoroscopic technique is essential to maximize diagnostic accuracy. In this pictorial essay, we discuss common diagnostic challenges in the diagnosis of malrotation and strategies radiologists can use to clarify the diagnosis in equivocal cases. © 2019 Elsevier Inc. All rights reserved.
Introduction Malrotation of the gastrointestinal (GI) tract is a congenital abnormality that predisposes patients to midgut volvulus, a potentially fatal condition.1 An upper GI fluoroscopic examination is commonly requested either on an urgent basis in children having bilious vomiting or in an outpatient setting in children with various abdominal symptoms. Several physiologic states can cause diagnostic confusion on upper GI series.2 It is important that the radiologists familiarize themselves with the optimal method of performing and interpreting a pediatric upper GI series to maximize diagnostic accuracy. In this review article, we discuss commonly encountered challenges in the diagnosis of malrotation and offer suggestions for troubleshooting. Definition, Embryology, and Etiopathogenesis Malrotation is a spectrum of disorders leading to abnormal position of the bowel in the abdomen due to abnormal embryologic bowel rotation.3 The gut in early embryonic period is a straight tube-like structure. As the gut lengthens during subsequent weeks, it also rotates 270° counterclockwise around the superior mesenteric artery (SMA) axis in several stages (Fig 1). Due to this rotation the cranial portion of the gut which forms the duodenum migrates to a location posterior to the SMA with the duodenojejunal junction (DJJ) to the left of SMA. The caudal portion of the gut which contains the cecum rotates counterclockwise from the left side of the abdomen
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. *Reprint requests: Sachin S. Kumbhar, MD, Medical College of Wisconsin, 8915 W Connell Ct, Milwaukee WI 53226. E-mail addresses: [email protected], [email protected] (S.S. Kumbhar). https://doi.org/10.1067/j.cpradiol.2019.10.002 0363-0188/© 2019 Elsevier Inc. All rights reserved.
in such a way that the cecum comes to rest in the right lower quadrant (RLQ).4 At completion of rotation, the ascending colon is fixed to the retroperitoneum on the right and the descending colon is fixed to the retroperitoneum on the left (Fig 2). Majority of the duodenum is also retroperitoneal.5 The small bowel mesentery has a wide root extending between 2 fixed points, the first being the DJJ in the left upper quadrant and the second being the ileocecal valve in the RLQ.6 The DJJ is suspended by the ligament of Trietz which is a peritoneal fold extending from the right esophageal crus of diaphragm and connective tissue around the coeliac artery and SMA.7 The ligament of Trietz is a surgically identifiable landmark and denotes the point where the small bowel becomes an intraperitoneal structure. Malrotation may affect small bowel or large bowel, or both.8 Any deviation from the normal pattern of intestinal rotation leads to an abnormal position of the DJJ and/or cecum. With decreased distance between the 2, the mesentery has a narrower root thus increasing the risk of twisting or volvulus.9 Abnormal rotation of the gut is also associated with peritoneal bands extending from the cecum to other structures which can cross the duodenum and cause obstruction.10
Clinical Features Malrotation affects about 1 in 500 live births. Vast majority of affected children present in the neonatal period, most commonly with bilious vomiting. Older children may present with nonspecific symptoms like intermittent vomiting, abdominal pain, and poor weight gain. Sometimes malrotation is an incidental finding on imaging done for other purposes.11 Malrotation is associated with several syndromes and disorders including but not limited to gastroschisis, congenital diaphragmatic hernia, omphalocele, and heterotaxy syndromes.10
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FIG 1. Diagrammatic representation of normal bowel rotation. The cephalad segment of the primitive gut including the duodenojejunal junction (D) rotates 270° anticlockwise around the superior mesenteric artery (straight arrow) to reach its normal location in the left abdomen (#). The caudal segment including the cecum (C) also rotates 270° anticlockwise to reach the right lower quadrant of the abdomen (*).
FIG 2. Normal anatomy at completion of rotation. The duodenojejunal junction (arrow) lies in the left upper quadrant and the cecum (*) is fixed to the retroperitoneum in the right lower quadrant. The third portion of the duodenum (double arrows) is located posterior to the superior mesenteric artery. Note that the mesentery has a wide root (arrowheads).
Normal Anatomy On a normal upper GI series, the proximal duodenum extends posteriorly from the pylorus, as seen on the lateral view, and extends toward the spine to its retroperitoneal location. The duodenum then crosses over to the left side of the spine and turns cranially to extend to the DJJ. The DJJ is identified on fluoroscopy as the cranial most and leftward most part of the bowel where it takes a definite inferior turn. A normally located DJJ should be to the left of the left-sided pedicle of the adjacent vertebral body (Fig 3). The DJJ
should be at the level of the duodenal bulb or higher on the frontal view and located posteriorly on the lateral projection.10,12,13 The proximal jejunal loops are usually located in the left upper quadrant and cecum in the RLQ. Upper GI Study Technique If the esophagus is to be evaluated, a left side down position should be used for the lateral view to avoid unintended gastric emptying. Esophageal evaluation in the right side down position
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FIG 3. Normal anatomy at upper GI study in a 6-year-old girl. (a) Frontal view of the abdomen demonstrates the duodenojejunal junction (arrow) located to the left of the left sided pedicle (arrowhead) and at the level of the duodenal bulb (double arrows). (b) Lateral view of the abdomen demonstrates a posterior location of the duodenojenjunal junction (arrow).
FIG 4. Use of abdominal compression to demonstrate the duodenojejunal junction in a 2-year-old girl. (a) Frontal view of the abdomen demonstrates contrast in the duodenum (arrow) and the proximal jejunum (arrowhead). The duodenojejunal junction is obscured by contrast within the stomach. (b) Frontal view of the abdomen obtained immediately after release of abdominal compression demonstrates the duodenojejunal junction (arrow) by displacing the stomach.
may cause early emptying of contrast into the duodenum causing the first pass of contrast through the duodenum to be missed. Volume of contrast used should be kept to minimum necessary as excessive contrast in the stomach can obscure the DJJ. Patients referred from the inpatient or emergency services may already have a nasogastric (NG) tube placed. Delivery of contrast through the NG tube can allow more control over contrast volume. It should however be kept in mind that in younger children postpyloric enteric tubes can distort anatomy and displace the DJJ. 14
Once desired amount of contrast has reached the stomach the child should be positioned in right side down position to assess extension of duodenum to the retroperitoneum. The radiologist should be vigilant and ready to image quickly as in some patients there is prompt gastric emptying in this position. After the proximal duodenum is opacified the child should be placed in supine position to assess position of the DJJ in the frontal view. Continuous fluoroscopy while the child is moved from the lateral to supine position is beneficial to capture the first pass of contrast through the duodenum.
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FIG 5. Use of watchful waiting and second bolus to demonstrate the duodenojejunal junction in a 20-month-old girl. (a) Frontal view of the abdomen demonstrates contrast in the proximal jejunum (arrow). The duodenojejunal junction was missed due to rapid transit. (b) Image obtained after few minutes demonstrates further propagation of contrast within the jejunum with relative clearance of the jejunal loops overlying the expected location of the duodenojejunal junction. (c) Second bolus of contrast was allowed to pass the duodenum demonstrating the duodenojejunal junction (arrowhead).
If there is a delay in movement of contrast through the third portion of the duodenum to the left, a transient left posterior oblique positioning of the patient may aid forward movement of contrast. The child then can be quickly returned to the supine position to document the anatomy. Once the location of the DJJ on the frontal view is documented, a lateral view should also be obtained to demonstrate its posterior retroperitoneal location. If the DJJ is obscured by contrast in the stomach gentle palpation to displace the stomach may aid in visualization of the DJJ
(Fig 4). The first pass of contrast through the duodenum may sometimes be missed if the stomach empties too quickly. Opacification of proximal jejunal loops may then hinder identification of the DJJ. If this happens intermittent fluoroscopy over next several minutes may be beneficial. After the contrast disperses within the jejunum the child may again be positioned in the right side down position and a second bolus of contrast may be allowed to enter the duodenum. A densely opacified DJJ can be identified through overlapping loops of jejunum (Fig 5). If the position of the DJJ remains equivocal
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FIG 6. Malrotation in a 12-month-old boy with bilious emesis. The duodenojejunal junction (arrow) is located medial to the left-sided pedicle (arrowhead) and inferior to the level of the duodenal bulb (double arrows). Malrotation was confirmed at surgery.
FIG 7. Subtle malrotation in a 2-year-old boy with vomiting. (a, b) Frontal views of the abdomen demonstrate the duodenojejunal junction (arrow) at the level of the duodenal bulb (double arrows) and medial to the left sided pedicle (arrowhead). Malrotation without volvulus was found at surgery.
the study should be extended to determine the position of proximal jejunal loops and the cecum.
Fluoroscopic Findings Malrotation An upper GI series is the preferred imaging study to diagnosis malrotation with sensitivity of 93%-100%.15-17 Demonstration of an abnormal position of the DJJ is the most important fluoroscopic finding to clinch the diagnosis. Findings that suggest malrotation are (1) the DJJ projects medial to the left-sided pedicle; (2) DJJ is inferior to the duodenal bulb; (3) DJJ is located more anterior than usual suggesting an intraperitoneal location (Fig 6).10,12,13 While most patients with malrotation have an obviously abnormal location of the DJJ, findings in some patients can be subtle causing diagnostic challenge. The DJJ may overlap the left-
sided pedicle or maybe only slightly inferior to the level of the duodenal bulb (Fig 7). If the lateral view demonstrates an intraperitoneal location of the DJJ confidence in the diagnosis of malrotation can be increased. Another finding suggesting malrotation is proximal jejunal loops located in the right upper quadrant of the abdomen. Most patients with malrotation also have an abnormal cecal location. It should however be noted that neither of this feature is specific in isolation (Fig 8). The cecum can be normally located in patients with malrotation.18
Midgut Volvulus Upper GI series has a reported sensitivity of 54% for midgut volvulus.17 Characteristic finding of midgut volvulus is a “corkscrew” appearance of proximal small bowel (Fig 9).19 Corkscrew appearance may not be apparent in patients with complete bowel
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FIG 8. Malrotation in a 4-month-old girl with situs inversus. (a) Frontal view of the abdomen demonstrates stomach in the right upper quadrant. Entire duodenum and part of the proximal jejunum are in the left upper quadrant. The duodenojejunal junction was not clearly identified due to excessive duodenal tortuosity. The jejunum crosses the midline to the right (arrow). (b) Frontal view of the abdomen from contrast enema study demonstrates the cecum (arrow) and appendix (arrowhead) in the left lower quadrant. The large bowel is normally rotated for patient’s situs.
FIG 9. Midgut volvulus without complete obstruction in an 8-year-old boy. Frontal oblique image from upper GI study demonstrates the classic “corkscrew” (arrows) appearance of the proximal jejunum. Midgut volvulus was confirmed at surgery.
obstruction as contrast will not enter the twisted loops of bowel. A beak-like tapering of the bowel may be seen in patients with complete obstruction (Fig 10). Watchful waiting or gentle abdominal compression may facilitate a small amount of contrast to clear past the obstruction to demonstrate the corkscrew pattern of the volvulized bowel (Fig 11).20
Peritoneal Bands Malrotation sometimes presents with duodenal obstruction due to peritoneal bands. The proximal duodenum will be dilated (Fig 12). If obstruction is incomplete contrast may extend beyond the point of obstruction and delineate the duodenal anatomy. The duodenum
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FIG 10. Midgut volvulus with complete obstruction in a 1-month-old boy. Frontal view from upper GI study demonstrates proximal duodenal dilation with beak like tapering (arrow) at the level of obstruction. Midgut volvulus was confirmed at surgery.
FIG 11. Midgut volvulus in a 1-day-old boy. (a, b) Frontal image from upper GI study demonstrates proximal duodenal dilation (a) with obstruction at the level of third portion of the duodenum (arrow). Image obtained after several minutes (b) shows that contrast has cleared past the obstruction to opacify narrowed bowel loops with corkscrew-like appearance (arrowheads). Midgut volvulus was confirmed at surgery.
may have a Z-shaped appearance in the presence of bands. The location of DJJ is usually abnormal. Challenging Cases Both false positive and false negative cases can occur in the fluoroscopic diagnosis of malrotation. The main reason for inaccurate diagnosis
is overlap between subtle abnormal position of the DJJ in malrotation and mild displacement of the DJJ due to other causes. False positive rates can be as high as 15% while false negative rates can reach up to 6%.21,22 The DJJ may be slightly inferior to the level of the duodenal bulb in infants with normal bowel rotation (Fig 13). This finding, which is more common in infants born prematurely, is thought to be due to relatively lax peritoneal structures in infants.13
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FIG 12. Obstructing duodenal band in a 13-year-old girl. Frontal image from upper GI study demonstrates dilation of the duodenal bulb (arrow) with abrupt narrowing in the second portion (arrowhead) of the duodenum. Obstructing peritoneal bands with malrotation was found at surgery.
FIG 13. Slight inferior location of the duodenojejunal junction in a 1-day-old girl. Frontal image from upper GI study demonstrates the duodenojejunal junction (arrow) to the left of the left sided pedicle and slightly inferior to the level of the duodenal bulb (arrowhead).
The DJJ in children younger than 4 years can be easily displaced by various physiologic and pathologic processes that cause enlargement of abdominal organs or gastric/bowel distention (Fig 14).23 Conditions than can displace the DJJ include, but are not limited to, gastric distention, chronic bowel dilation, colonic distension, splenomegaly, enlarged left kidney, liver transplant, and presence of an enteric tube.2,14 The DJJ is relatively fixed in children older than 4 years of age. Variations in duodenal anatomy can also cause diagnostic confusion. Wandering duodenum consists of redundancy of the duodenum that appears as a tortuous course on fluoroscopy (Fig 15). The DJJ is in the normal location. In mobile duodenum, the post bulbar proximal duodenum forms a loop in the right abdomen instead of being fixed to the retroperitoneum before crossing over to the left side (Fig 16).12,24 Duodenum inversum is a congenital
anomaly in which second portion of the duodenum extends superiorly and posteriorly on the right side of the spine. It then crosses over to the left at a level more cephalad than expected (Fig 17). The DJJ is in normal location.25,26 Trouble Shooting Attention to proper fluoroscopic technique is a key to increase the diagnostic accuracy of malrotation. Documenting first pass of contrast through duodenum and demonstrating position of the DJJ on both frontal and lateral views are important components of the exam.13 If the DJJ projects slightly medially than expected, a review of patients’ positioning for the image might be helpful. True supine positioning with patient’s back flat against the table is important.
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FIG 14. Inferior displacement of the duodenojejunal junction in a 7-year-old girl with gastric bezoar. Frontal image from upper GI study demonstrates the duodenojejunal junction (arrow) to the left of the left sided pedicle and inferior to the level of the duodenal bulb (double arrows). The stomach is distended with a filling defect due to a trichobezoar (arrowhead). Normal rotation of the bowel was confirmed at surgery.
FIG 15. Wandering duodenum in a 5-month-old boy. Frontal image from upper GI study demonstrates a tortuous course of the third portion (arrowheads) of the duodenum. The duodenojejunal junction (arrow) is in normal position.
An oblique position can cause the DJJ to project over the spine and lead to a false positive result (Fig 18). Symmetric appearance of the lower ribs is a good indication of a true supine position. Subtle inferior position of the DJJ is another source of diagnostic confusion. Review of the scout film might reveal a potential cause of a displaced DJJ such as a distended stomach, dilated
bowel, or splenomegaly. If the scout film reveals gastric distention, aspiration of gastric contents through a NG tube may aid in the DJJ coming back to its normal location (Fig 19). Review of patient’s charts and prior imaging may help to identify other sources of false positive results such as enlarged kidney or liver transplant.2
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FIG 16. Mobile duodenum in a 6-year-old boy. Frontal image from upper GI study demonstrates the second portion of the duodenum forming a loop (arrowhead) in the right abdomen. The duodenojejunal junction (arrow) is in normal position.
FIG 17. Duodenum inversum in a 1-month-old boy. Frontal image from upper GI study demonstrates normal course of the second portion (double arrows) of the duodenum. The third portion (arrowheads) courses cranially in the right abdomen and then crosses the midline at a higher level than usual. The duodenojejunal junction (arrow) is normally located.
Manual compression of the abdomen to determine the mobility of the DJJ can be used in children with equivocal position of the DJJ. The DJJ can be manually displaced in children with normal bowel rotation up to 4 years of age. It will however return to a normal location after the compression is released. In patients with malrotation the DJJ position may remain abnormal after release of compression.20,23 Radiologists should be familiar with physiologic variations in duodenal anatomy like wandering duodenum and mobile duodenum. While some duodenal redundancy is normal, excessive redundancy should raise suspicion for malrotation especially in the presence of angularity or kinking. Presence of more than one loop of the duodenum on the right of the spine is also abnormal and indicative of malrotation.12
Another strategy that can be employed in equivocal cases is to extend the study to determine the location of proximal jejunum and cecum. Contrast enema may also be performed to determine cecal location.10 While a right upper quadrant position of proximal jejunum can be seen in malrotation, this finding in isolation is not specific. Position of the cecum is abnormal in up to 80% children with malrotation.12,18 However, there is overlap with physiologic variations in cecal position. Regardless, demonstration of an obviously abnormal cecal/colonic position will be helpful to clear diagnosis. If the exam remains equivocal, repeat exam on another day should be considered (Fig 20). A repeat exam is convenient, more cost effective and less invasive compared to surgery. Repeat exam
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FIG 18. Oblique position causing diagnostic confusion in a 1-year-old boy. Fluoroscopic image from upper GI study demonstrates the duodenojejunal junction (arrow) projecting over the spine in the midline. A review of the lower ribs reveals asymmetrical appearance indicating oblique positioning. A repeat upper GI study (same as in FIG 4) performed subsequently demonstrated normal location of the duodenojejunal junction.
FIG 19. Use of gastric decompression to demonstrate normal anatomy in a 2-day-old boy. Initial frontal image from upper GI study (a) demonstrates medial location of the duodenojejunal junction (arrow) overlying the left sided pedicle. Note that the stomach is distended. Air was aspirated through the nasogastric tube to decompress the stomach. Repeat frontal image (b) demonstrates normal location of the duodenojejunal junction (arrowhead) to the left of the left sided pedicle.
may be performed using an enteric tube which allows for more control over contrast volume and can achieve better duodenal distention with lesser gastric opacification. Conclusions An upper GI series is the most commonly performed radiological test for the diagnosis of malrotation and midgut volvulus. Unfortunately, several physiologic and pathologic conditions can have a fluoroscopic appearance similar to subtle cases of malrotation causing
diagnostic dilemma. Proper technique in performing the upper GI study is vital to maximize diagnostic yield. The radiologist should be familiar with physiologic variations in duodenal anatomy. Several strategies such as gastric decompression, abdominal compression, demonstrating cecal position, and repeat study can be used in equivocal cases. Conflict of Interest The authors declare that they have no conflict of interest.
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FIG 20. Use of repeat upper GI study to demonstrate normal anatomy in a 1-year-old boy. Initial frontal image from upper GI study (a) demonstrates medial location of the duodenojejunal junction (arrow). Delayed abdominal radiograph (not shown) demonstrated cecum in the right lower quadrant. Repeat upper GI study performed on a later day (b) demonstrates normal location of the duodenojejunal junction (arrowhead). Medial displacement of the duodenojejunal junction on the initial study was thought to be caused by gaseous distention of the splenic flexure (double arrows) of the colon (c).
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