EHD-04046; No of Pages 5 Early Human Development xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Best practice guidelines
Malrotation and intestinal atresias Stephen D. Adams, Michael P. Stanton ⁎ Department of Paediatric Surgery, University Hospitals Southampton NHS Trust, Tremona Road, Southampton SO16 6YD, United Kingdom
a r t i c l e
i n f o
a b s t r a c t This review encompasses four congenital conditions which present with symptoms of bowel obstruction in the neonatal period. The antenatal and postnatal features of malrotation, jejuno-ileal atresia, duodenal atresia and colonic atresia are discussed. Each condition is outlined including the classification, epidemiology, aetiology and presentation, and a summary of the surgical management is described. © 2014 Elsevier Ltd. All rights reserved.
Available online xxxx Keywords: Malrotation Volvulus Duodenal atresia Jejuno-ileal atresia Colonic atresia
Contents 1. Introduction . . . . . 2. Malrotation . . . . . 3. Jejuno-ileal atresia . . 4. Duodenal atresia . . . 5. Colonic atresia . . . . 6. Key guidelines . . . . 7. Research directions . . Conflict of interest statement References . . . . . . . .
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1. Introduction Bowel obstruction due to malrotation or bowel atresia occurs in around 6 per 10,000 live born infants. This article reviews the major congenital obstructive pathologies, presenting a summary of the condition in each case and a guide to management. 2. Malrotation Malrotation is a congenital anomaly of intestinal position and may lead to volvulus of the mid-gut around a narrow-based mesentery. The importance of considering this diagnosis cannot be overemphasised when an infant presents with bilious vomiting, as left untreated, mid-gut infarction rapidly occurs. Malrotation presents in around 1 in 2500 live born infants (under 1 year of age), however as an anatomic entity it is much more common than this, occurring in 0.2%–1% of the normal population. ⁎ Corresponding author. Tel.: +44 2381 206489; fax: +44 2381 204750. E-mail address: [email protected] (M.P. Stanton).
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Normal intestinal rotation is established initially by physiological herniation of the embryonic intestinal loop into the umbilical cord in the 4th gestational week, associated with a 90° anti-clockwise rotation. The mid-gut returns to the peritoneal cavity by the 8–10th week. As it does so, it rotates a further 180°, completing a total of 270° anticlockwise rotation, such that the duodenal–jejunal (DJ) comes to lie on the left of the midline and the caecum in the right iliac fossa. This standard description has been challenged by more recent experimental evidence [1]. The relative rotation is likely to be due to rapid differential growth, the most important feature of which is development of the duodenal loop. It may be that the return of the rest of the intestine occurs by a more passive mechanism, rather than being driven by rotation. The classical picture of malrotation results from an error in the normal process outlined. The commonest end-result is that of the caecum lying to the left of the midline, the DJ flexure lying to the right of the midline, narrow mesentery which lacks fixation, and peritoneal (Ladd's) bands passing from the caecum to the right side across the duodenum. There is much discussion of Ladd's bands in the literature, these being the result of the caecum's attempts at peritoneal fixation. They may be present but only occasionally give rise to duodenal
http://dx.doi.org/10.1016/j.earlhumdev.2014.09.017 0378-3782/© 2014 Elsevier Ltd. All rights reserved.
Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
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S.D. Adams, M.P. Stanton / Early Human Development xxx (2014) xxx–xxx
obstruction. The primary concern is that mid-gut volvulus may occur following twisting of the narrow mesentery and thus threaten the venous outflow and subsequently the arterial inflow to the intestine. Other rotational anomalies are described — non-rotation is seen in the context of abdominal wall defects and congenital diaphragmatic hernia. The duodenum passes straight inferiorly on the right side; the colon lies on the left. Reverse rotation is described where the duodenum passes in front of the superior mesenteric artery, with the colon lying in front of the mesentery. Internal small bowel hernias are also considered a subgroup of rotational anomalies. There is a high rate of associated anomalies reported in infants with malrotation. Type IIIb small bowel atresia may be a secondary outcome of antenatal volvulus. Other common associations include cardiac anomalies, ano-rectal malformation, duodenal web and trisomy 21. Non-rotation is almost ubiquitous in children with abdominal wall defects or congenital diaphragmatic hernia. Interestingly, the association of volvulus is rather less with this group, perhaps due to the contribution of post-operative (or congenital) bowel adhesions. Intestinal rotation anomalies are seen in association with heterotaxia. It is debated whether elective investigation and surgical correction of malrotation are merited in the context of heterotaxia, in particular when significant cardiac anomalies may be present. Recent evidence suggests that the morbidity from an elective procedure, when the infants cardiac status is relatively stable, may be low, however, the overall risk of volvulus appears to be low and screening in all cases may be misleading. The most common clinical presentation is with bile vomiting during the first month of life (N50% cases); this may be accompanied by abdominal distension or bleeding per rectum as a late sign. Presentation subsequent to this age becomes more varied and may include episodic vomiting (often non-bilious), recurrent abdominal pain or simply failure to thrive, all of which may have been attributed to gastrooesophageal reflux [2]. The diagnosis of malrotation is usually made by means of an upper GI contrast examination. Plain radiographs in cases of established volvulus typically show air in the stomach and proximal duodenum and a gasless appearance beyond. If the presentation is of an infant with peritonitis, then immediate laparotomy is mandated without the luxury of contrast examination first. Otherwise, plain XRs can be normal and do not exclude malrotation. The hallmark feature on upper GI contrast examination is a duodeno-jejunal flexure that does not pass to the left of the spinous process of the 2nd lumbar vertebra, together with a lowlying pylorus. If volvulus is present this may show as complete obstruction (‘bird-beak’) at the level of the proximal to mid-duodenum or indeed as a ‘cork-screw’ type appearance as the small bowel passes from posterior to anterior (Fig. 1). Ultrasonographic features have been described, in particular reversal of the position of the superior mesenteric artery and vein, although this modality would not be considered reliable enough to exclude malrotation when clinically suspected. Occasionally malrotation may be detected incidentally, for example on CT scan. For truly incidental older children (N2 years), some authors describe avoiding operation and advise urgent investigation and treatment should any gastro-intestinal symptoms occur. The authors' practice is to recommend semi-urgent surgical correction. The surgical procedure to correct malrotation was described by William Ladd in 1936 and still remains in widespread use. The premise is to de-rotate the mid-gut if it is twisted, straighten the duodenum, widen the mesenteric root and place the intestine in a stable position. To minimise the risk of recurrent volvulus, the small bowel is placed on the right side of the peritoneal cavity and the colon to the left. The caecum is positioned in the left upper quadrant thus an incidental appendicectomy may be performed to avoid future diagnostic confusion; inversion appendicectomy is the authors' preference but this step remains controversial. The operating surgeon may be faced with the situation of volvulus and total mid-gut infarction at initial laparotomy. If mid-gut resection is under taken at this stage, the infant is committed to short-gut syndrome with
Fig. 1. Radiograph from an upper GI contrast examination demonstrating classical appearances of malrotation with volvulus of the mid-gut. The DJ flexure lies to the right and there is a corkscrew appearance beyond.
the possibility of intestinal transplantation. A difficult ethical consideration arises which should be managed with full discussion with the family to allow informed choice. If there is any question regarding viability, the bowel is returned to the abdominal cavity and a secondlook laparotomy can be performed at 24–48 h. A successful reversal of apparently established infarction of the mid-gut using postoperative systemic thrombolysis has been reported in 2 infants and appears to be a promising therapy [3]. Laparoscopic Ladd's procedure is now well-established, but may not be appropriate in the emergency setting. Complications of Ladd's procedure include adhesive small bowel obstruction (6%), incisional hernia, perforated viscus and recurrent volvulus (around 1% each). Malrotation still accounts for a significant proportion of children with short-gut syndrome. Mortality depends on whether bowel ischaemia is present and is approximately 3% [4].
3. Jejuno-ileal atresia Jejuno-ileal atresia (JIA) is the commonest type of intestinal atresia and accounts for around 1 in 5000 to 1 in 14,000 live births. Over one third of affected children are born prematurely, there is no sex predominance and usually there are no associated chromosomal abnormalities (b1%). Small bowel atresias are classified using Louw's classification (Table 1, Fig. 2) and the relative frequency spreads reasonably evenly between 4 groups. Type III is further subdivided (as per Grosfeld et al. [14]) to account for IIIb — the apple peel atresia which is present in 7% of JIAs. The apple peel deformity results in an atresia just beyond the DJ flexure, with the remaining small bowel coiled around the ileocolic artery. The superior mesenteric artery is absent beyond the origin of the middle colic vessel. Type IIIb and IV atresias are more commonly
Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
S.D. Adams, M.P. Stanton / Early Human Development xxx (2014) xxx–xxx Table 1 Louw's classification & Grosfeld's modification. Type of atresia
Description
I II III
Internal membrane, serosa in continuity, no mesenteric defect Serosal discontinuity, cord between proximal and distal ends Serosal discontinuity with mesenteric defect (subdivided by Grosfeld into a and b) Mesenteric defect only Apple peel deformity Multiple atresias
IIIa IIIb IV
associated with a significant loss of intestinal length. Jejunal atresias are more common than ileal and the more distal the atresia the less frequent the incidence [5]. Since the initial experiments of Louw and Barnard in the 1950s [15], it has been assumed that JIA results from a vascular insult late in foetal life. It has been accurately reproduced by ligation of mesenteric vessels in-utero in canine studies and analysis of the post-atretic intestinal content demonstrates bile salts, epithelial cells and ingested lanugo hair in humans [6]. Associated conditions may be related to the aetiology of the condition; JIA is present in approximately 10% of infants with gastroschisis and 10% of infants with JIA will also have cystic fibrosis. Routine screening for CF is now undertaken for all newborns in the UK, with an associated improvement in clinical outcome for infants diagnosed in the neonatal period [7]. Some centres suggest formal screening (genetic screen or sweat test) to produce higher sensitivity than is provided by the immuno-
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reactive trypsinogen as currently undertaken in the UK by the newborn screening blood spot test. Malrotation is present in 20% however volvulus is present in 25% at operation — if volvulus occurs antenatally then it may lead to intestinal loss and the development of an atresia (typically Type IIIb). Concurrent duodenal or colonic atresia may occur in up to 6%. Antenatal detection of JIA has been reported in approximately half of cases in some series. Multiple dilated loops (e.g. N 7 mm diameter), cystic mass, ascites or polyhydramnios may be seen. The combination of dilated bowel and polyhydramnios may be particularly suggestive. Foetal echogenic bowel can be a transient finding and postnatally the majority will not have intestinal pathology. Post-natal presenting features are bilious vomiting, abdominal distension and delayed passage of meconium. Normal coloured meconium may be present, but it is more usual for pale plugs to be passed or produced if rectal washouts are administered. The presentation can be similar to that of malrotation and mid-gut volvulus and must therefore be investigated as an emergency. Plain abdominal radiography alone is usually diagnostic, with swallowed air acting as a contrast medium (Fig. 3). In proximal atresias, a small number of dilated loops are seen with an absence of distal air. The presence of calcification implies pre-natal bowel perforation of the proximal atretic segment leading to meconium pseudocyst formation. An upper GI contrast can be utilised to exclude malrotation. Contrast enema may be required to differentiate distal atresia from meconium ileus, Hirschsprung disease or small left colon syndrome. Atresia is excluded if contrast refluxes into dilated gas-filled loops of bowel, with an unused appearance of the colon. Once the diagnosis is confirmed, nasogastric decompression and fluid resuscitation are instituted. The operative strategy depends on
I
II
IIIa
IIIb
IV
Fig. 2. Classification of bowel atresia. Adapted from Grosfeld JL et al. J Pediatr Surg 1979;14:368–75.
Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
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S.D. Adams, M.P. Stanton / Early Human Development xxx (2014) xxx–xxx
Fig. 3. Plain abdominal radiograph demonstrating multiple dilated bowel loops in keeping with an ileal atresia.
the operative findings, but resection of the dilated proximal end, and primary anastomosis to the distal portion, is usually undertaken. Multiple atresias may be anastomosed but will more commonly be provided with a covering stoma. Short-term parenteral nutrition (PN) is required in the majority whilst normal intestinal function resumes. The prognosis for JIA is generally related to the total length of the remaining intestine and the presence of an intact ileo-caecal valve. For example, infants with N100 cm of intestine are likely to require short-term PN only, whereas at b25 cm, long-term PN, intestinal lengthening procedures and consideration for liver/small bowel transplantation will be necessary. The two commonly used lengthening procedures are the serial transverse enteroplasty procedure (STEP) and longitudinal intestinal lengthening procedure (LILT). JIA accounts for 10% of the surgical causes of intestinal failure, with gastroschisis and necrotising enterocolitis making up the majority. Overall survival with JIA is expected to be N90%.
There is a slight male preponderance (1.4:1). Around 30% of children with DA will also have trisomy 21 and up to 25% with DA have structural cardiac defects. Conversely 8% of children with trisomy 21 will also have DA. Up to 10% of affected children will be malrotated and a proportion will have the VACTERL association or some of its component parts. Around 7% will have another intestinal atresia [9]. DA will often (44–51%) present antenatally with the sonographic finding of polyhydramnios leading to later scans and the detection of a ‘double bubble’ in the third trimester. This is explained by the presence of amniotic fluid in the stomach and proximal duodenum. The double bubble, containing swallowed air, without the presence of distal gas, is also the typical finding on a post-natal plain abdominal radiograph (Fig. 4). Infants present with vomiting in the first 48 h of life; this is bilious in 80% (post-ampullary). In the remaining 20% the vomit is not bilestained as the obstruction occurs proximal to the insertion of the common bile duct in the second part of the duodenum (pre-ampullary). The most important differential diagnosis at presentation is malrotation with mid-gut volvulus. Clues to differentiating malrotation and DA include the antenatal history and radiographic features such as a smooth outline to the most distal point of a double bubble (DA), rather than the ‘birds beak’ (suggestive of malrotation). However, any suspicion of this diagnosis mandates emergency investigation and/or operative intervention. Distal gas beyond the double bubble may be indicative of malrotation/volvulus, but can also occur in the rare anatomical variant of a bifid common bile duct (or even pancreatic duct) inserting into the proximal and distal duodenal segments. Initial management of DA is with nasogastric drainage, supportive treatment and examination/ investigation to assess for the presence of associated anomalies. Surgical correction is not usually an emergency. Operative intervention is usually with duodeno-duodenostomy, where the proximal and distal duodenal pouches are opened and joined, effectively bypassing the atretic segment. This procedure can be performed either open or laparoscopically. A duodenal membrane can be dealt with by means of a vertical duodenotomy, web resection
4. Duodenal atresia Duodenal atresia (DA) occurs in around 1 in 10,000 live births and represents up to 60% of intestinal atresias [7]. The aetiology of DA was originally thought to be quite different from the vascular theory which applies to other intestinal atresias; rather the duodenal lumen became occluded during epithelial proliferation and failed to re-canalise in the 2nd gestational month, as first proposed by Tandler in 1900. Since then, little more has been established regarding the pathogenesis of DA in humans. Recent research has focussed on the role of the fibroblast growth factor pathway in mice. An autosomal recessive phenotype of duodenal and colonic atresia can be produced in a murine model by knock-out of the fibroblast growth factor receptor 2b [8]. Classification is similar to other intestinal atresias, with Type I (membrane or web causing luminal obstruction) accounting for up to 90% of cases. Type I atresias or stenoses can lead to the ‘windsock’ anomaly — surgically relevant as the obstructing membrane distends distally leading to the external appearance of dilatation beyond the actual level of obstruction.
Fig. 4. Plain chest and abdominal radiograph demonstrating the ‘double bubble’ appearance suggestive of duodenal atresia. There is a rounded end to the proximal duodenal pouch and no distal gas.
Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
S.D. Adams, M.P. Stanton / Early Human Development xxx (2014) xxx–xxx
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and transverse closure. Duodeno-jejunostomy can be performed if duodeno-duodenostomy is not possible, but is associated with a greater risk of blind-loop syndrome. Operative findings can also demonstrate another causative or associated pathology — for example annular pancreas, malrotation or second distal intestinal atresia. Post-operatively, parenteral nutrition can usually be avoided and some centres advocate placement of a trans-anastomotic tube to facilitate early jejunal feed whilst normal gastro-duodenal function resumes [10]. There is an associated mortality rate of around 5% with DA; this is related to the high rate of associated anomalies. The long-term outcome is usually very good in terms of intestinal function. Rarely, gross dilatation of the proximal duodenum may develop over time, amenable either to re-anastomosis or tapering duodenoplasty. Pyloric atresia is a very rare anomaly showing autosomal recessive inheritance when associated with epidermolysis bullosa. The aetiology is also thought to be a failure of vacuolisation of the solid pyloric lumen. Membranous obstruction is more common than a true atresia and can be corrected by web excision or pyloroplasty. True atresia requires gastro-duodenostomy.
rectal biopsy before primary anastomosis is undertaken. The outcome of isolated CA cases is good in terms of bowel function as overall bowel length is usually not significantly reduced.
5. Colonic atresia
Further experimental evidence to outline the process of ‘rotation’ in the human foetus is likely to clarify our understanding of this condition. The vascular theory of JIA still relies on evidence from the 1950s. The fibroblast growth factor pathway, and its elimination in a murine model, may provide clues as to the aetiology. Research in the management of short-gut syndrome are currently directed at the optimal use of PN/minimising its side effects and assessing the outcome of bowel lengthening procedures and transplantation.
Colonic atresia (CA) is a rare anomaly making up 2–15% of intestinal atresias. CA is classified according to the same system as other bowel atresias as described by Louw [6] and is likely to share a common vascular aetiology. The estimated incidence varies between 1 in 10,000 and 1 in 66,000. The affected segment is more commonly the right colon than the left, and a type III atresia (mesenteric defect separating the blind ends) usually results. There is a slight predominance of males over females (4:3). There is a significant mortality associated with CA, estimated at 25% in one literature review [11]. However, this is likely to represent cases of significantly delayed diagnosis, and individual series reports 0% mortality. CA differs from other bowel atresias in terms of its associations. Hirschpsrung disease has been reported in association with CA in a small number of cases (b 20) [12]. It has been speculated that CA may arise from volvulus of the dilated colon proximal to the affected aganglionic segment. Alternatively, atresia in itself may prevent migration of enteric neurones. Although an unusual association, this should be considered if a primary repair is undertaken. The small number of reported cases does not allow firm conclusions to be drawn regarding location of the atresia and risk of associated aganglionosis. CA also occurs in association with gastroschisis and it has been postulated that constriction at the umbilical ring may be causative. Antenatal detection of distal bowel atresia in general may be suggested by the finding of bowel dilatation, but specific detection of CA has only been described once [13]. Polyhydramnios does not usually occur due to amniotic fluid absorption in the foetal proximal small bowel. Infants present in the first 48 h with typical features of distal intestinal obstruction — distension, failure to pass meconium and bilious vomiting. The proximal colon is often hugely dilated and thus palpable. This is particularly concerning as a closed loop colonic obstruction may form in the presence of a competent ileo-caecal valve. As with other atresias, correction of dehydration and naso-gastric decompression is initiated. Abdominal radiograph will demonstrate very dilated loops of bowel. Contrast enema may be confirmatory, although the degree of clinical distension, absence of meconium and findings on plain radiograph will often be sufficient to merit laparotomy. Two surgical approaches are described. Primary excision and anastomosis are possible, particularly when the right colon is affected. Alternatively, a staged approach, often preferred for left-sided atresia, with initial stoma formation and delayed repair may be undertaken. Although a rare association, it is important to exclude distal aganglionosis with
6. Key guidelines Bilious (dark green) vomiting in an infant should always be regarded as abnormal and a high level of suspicion should be held for malrotation initially; the presentation of malrotation can occasionally be confused with DA and JIA. Suspicion of trisomy 21 should be high in DA. JIA may be suspected antenatally in about half of cases by the presence of dilated bowel and polyhydramnios. Overall outcomes are good; a small proportion will have short-gut syndrome. Hirschsprung disease should be considered and excluded in cases of CA. 7. Research directions
Conflict of interest statement The authors declare that there are no relevant conflicts of interest regarding the preparation of this invited review article. References [1] Kluth D, Jaeschke-Melli S, Fiegel H. The embryology of gut rotation. Semin Pediatr Surg 2003;12(4):275–9. [2] Yanez R, Spitz L. Intestinal malrotation presenting outside the neonatal period. Arch Dis Child 1986;61:682–5. [3] Kiely EM, Pierro A, Pierce C, Cross K, De Coppi P. Clot dissolution: a novel treatment of midgut volvulus. Pediatrics 2012;129:e1601–4. [4] Gohary Y, Alagtal M, Gillick J. Long-term complications following operative intervention for intestinal malrotation: a 10-year review. Pediatr Surg Int 2010;26:203–6. [5] Calisti A, Olivieri C, Coletta R, Briganti V, Oriolo L, Giannino G. Jejunoileal atresia: factors affecting the outcome and long-term sequelae. J Clin Neonatol 2012;1(1): 38–41. [6] Louw JH. Jejunoileal atresia and stenosis. J Pediatr Surg 1966;1(1):8–23. [7] Best KE, Tennant PWG, Addor M-C, Bianchi F, Boyd P, Calzolari E, et al. Epidemiology of small intestinal atresia in Europe: a register-based study. Arch Dis Child Fetal Neonatal Ed 2012;97:F353–8. [8] Kanard RC, Fairbanks TJ, De Langhe SP, Sala FG, Del Moral PM, Lopez CA, et al. Fibroblast growth factor-10 serves a regulatory role in duodenal development. J Pediatr Surg 2005;40:313–6. [9] Choudhry MS, Rahman N, Boyd P, Lakhoo K. Duodenal atresia: associated anomalies, prenatal diagnosis and outcome. Pediatr Surg Int 2009;25:727–30. [10] Hall NJ, Drewett M, Wheeler RA, Griffiths DM, Kitteringham LJ, Burge DM. Transanastomotic tubes reduce the need for central venous access and parenteral nutrition in infants with congenital duodenal obstruction. Pediatr Surg Int 2011; 27:851–5. [11] Etensel B, Temir G, Karkiner A, Melek M, Edirne Y, Karaca I, et al. Atresia of the colon. J Pediatr Surg 2005;40(8):1258–68. [12] Seo T, Ando H, Watanabe Y, Harada T, Ito F, Kaneko K, et al. Colonic atresia and Hirschsprung's disease: importance of histologic examination of the distal bowel. J Pediatr Surg 2002;37(8):E19. [13] Anderson N, Malpas T, Robertson R. Prenatal diagnosis of colon atresia. Pediatr Radiol 1993;23(1):63–4. [14] Grosfeld JL, Ballantine TVN, Shoemaker R. Operative management of intestinal atresia and stenosis based on pathologic findings. J Pediatr Surg 1979;14(3):368–75. [15] Louw JH, Barnard CN. Congenital intestinal atresia. Lancet 1955;19:1065–7.
Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
Contents lists available at ScienceDirect
Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Best practice guidelines
Malrotation and intestinal atresias Stephen D. Adams, Michael P. Stanton ⁎ Department of Paediatric Surgery, University Hospitals Southampton NHS Trust, Tremona Road, Southampton SO16 6YD, United Kingdom
a r t i c l e
i n f o
a b s t r a c t This review encompasses four congenital conditions which present with symptoms of bowel obstruction in the neonatal period. The antenatal and postnatal features of malrotation, jejuno-ileal atresia, duodenal atresia and colonic atresia are discussed. Each condition is outlined including the classification, epidemiology, aetiology and presentation, and a summary of the surgical management is described. © 2014 Elsevier Ltd. All rights reserved.
Available online xxxx Keywords: Malrotation Volvulus Duodenal atresia Jejuno-ileal atresia Colonic atresia
Contents 1. Introduction . . . . . 2. Malrotation . . . . . 3. Jejuno-ileal atresia . . 4. Duodenal atresia . . . 5. Colonic atresia . . . . 6. Key guidelines . . . . 7. Research directions . . Conflict of interest statement References . . . . . . . .
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1. Introduction Bowel obstruction due to malrotation or bowel atresia occurs in around 6 per 10,000 live born infants. This article reviews the major congenital obstructive pathologies, presenting a summary of the condition in each case and a guide to management. 2. Malrotation Malrotation is a congenital anomaly of intestinal position and may lead to volvulus of the mid-gut around a narrow-based mesentery. The importance of considering this diagnosis cannot be overemphasised when an infant presents with bilious vomiting, as left untreated, mid-gut infarction rapidly occurs. Malrotation presents in around 1 in 2500 live born infants (under 1 year of age), however as an anatomic entity it is much more common than this, occurring in 0.2%–1% of the normal population. ⁎ Corresponding author. Tel.: +44 2381 206489; fax: +44 2381 204750. E-mail address: [email protected] (M.P. Stanton).
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Normal intestinal rotation is established initially by physiological herniation of the embryonic intestinal loop into the umbilical cord in the 4th gestational week, associated with a 90° anti-clockwise rotation. The mid-gut returns to the peritoneal cavity by the 8–10th week. As it does so, it rotates a further 180°, completing a total of 270° anticlockwise rotation, such that the duodenal–jejunal (DJ) comes to lie on the left of the midline and the caecum in the right iliac fossa. This standard description has been challenged by more recent experimental evidence [1]. The relative rotation is likely to be due to rapid differential growth, the most important feature of which is development of the duodenal loop. It may be that the return of the rest of the intestine occurs by a more passive mechanism, rather than being driven by rotation. The classical picture of malrotation results from an error in the normal process outlined. The commonest end-result is that of the caecum lying to the left of the midline, the DJ flexure lying to the right of the midline, narrow mesentery which lacks fixation, and peritoneal (Ladd's) bands passing from the caecum to the right side across the duodenum. There is much discussion of Ladd's bands in the literature, these being the result of the caecum's attempts at peritoneal fixation. They may be present but only occasionally give rise to duodenal
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Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
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obstruction. The primary concern is that mid-gut volvulus may occur following twisting of the narrow mesentery and thus threaten the venous outflow and subsequently the arterial inflow to the intestine. Other rotational anomalies are described — non-rotation is seen in the context of abdominal wall defects and congenital diaphragmatic hernia. The duodenum passes straight inferiorly on the right side; the colon lies on the left. Reverse rotation is described where the duodenum passes in front of the superior mesenteric artery, with the colon lying in front of the mesentery. Internal small bowel hernias are also considered a subgroup of rotational anomalies. There is a high rate of associated anomalies reported in infants with malrotation. Type IIIb small bowel atresia may be a secondary outcome of antenatal volvulus. Other common associations include cardiac anomalies, ano-rectal malformation, duodenal web and trisomy 21. Non-rotation is almost ubiquitous in children with abdominal wall defects or congenital diaphragmatic hernia. Interestingly, the association of volvulus is rather less with this group, perhaps due to the contribution of post-operative (or congenital) bowel adhesions. Intestinal rotation anomalies are seen in association with heterotaxia. It is debated whether elective investigation and surgical correction of malrotation are merited in the context of heterotaxia, in particular when significant cardiac anomalies may be present. Recent evidence suggests that the morbidity from an elective procedure, when the infants cardiac status is relatively stable, may be low, however, the overall risk of volvulus appears to be low and screening in all cases may be misleading. The most common clinical presentation is with bile vomiting during the first month of life (N50% cases); this may be accompanied by abdominal distension or bleeding per rectum as a late sign. Presentation subsequent to this age becomes more varied and may include episodic vomiting (often non-bilious), recurrent abdominal pain or simply failure to thrive, all of which may have been attributed to gastrooesophageal reflux [2]. The diagnosis of malrotation is usually made by means of an upper GI contrast examination. Plain radiographs in cases of established volvulus typically show air in the stomach and proximal duodenum and a gasless appearance beyond. If the presentation is of an infant with peritonitis, then immediate laparotomy is mandated without the luxury of contrast examination first. Otherwise, plain XRs can be normal and do not exclude malrotation. The hallmark feature on upper GI contrast examination is a duodeno-jejunal flexure that does not pass to the left of the spinous process of the 2nd lumbar vertebra, together with a lowlying pylorus. If volvulus is present this may show as complete obstruction (‘bird-beak’) at the level of the proximal to mid-duodenum or indeed as a ‘cork-screw’ type appearance as the small bowel passes from posterior to anterior (Fig. 1). Ultrasonographic features have been described, in particular reversal of the position of the superior mesenteric artery and vein, although this modality would not be considered reliable enough to exclude malrotation when clinically suspected. Occasionally malrotation may be detected incidentally, for example on CT scan. For truly incidental older children (N2 years), some authors describe avoiding operation and advise urgent investigation and treatment should any gastro-intestinal symptoms occur. The authors' practice is to recommend semi-urgent surgical correction. The surgical procedure to correct malrotation was described by William Ladd in 1936 and still remains in widespread use. The premise is to de-rotate the mid-gut if it is twisted, straighten the duodenum, widen the mesenteric root and place the intestine in a stable position. To minimise the risk of recurrent volvulus, the small bowel is placed on the right side of the peritoneal cavity and the colon to the left. The caecum is positioned in the left upper quadrant thus an incidental appendicectomy may be performed to avoid future diagnostic confusion; inversion appendicectomy is the authors' preference but this step remains controversial. The operating surgeon may be faced with the situation of volvulus and total mid-gut infarction at initial laparotomy. If mid-gut resection is under taken at this stage, the infant is committed to short-gut syndrome with
Fig. 1. Radiograph from an upper GI contrast examination demonstrating classical appearances of malrotation with volvulus of the mid-gut. The DJ flexure lies to the right and there is a corkscrew appearance beyond.
the possibility of intestinal transplantation. A difficult ethical consideration arises which should be managed with full discussion with the family to allow informed choice. If there is any question regarding viability, the bowel is returned to the abdominal cavity and a secondlook laparotomy can be performed at 24–48 h. A successful reversal of apparently established infarction of the mid-gut using postoperative systemic thrombolysis has been reported in 2 infants and appears to be a promising therapy [3]. Laparoscopic Ladd's procedure is now well-established, but may not be appropriate in the emergency setting. Complications of Ladd's procedure include adhesive small bowel obstruction (6%), incisional hernia, perforated viscus and recurrent volvulus (around 1% each). Malrotation still accounts for a significant proportion of children with short-gut syndrome. Mortality depends on whether bowel ischaemia is present and is approximately 3% [4].
3. Jejuno-ileal atresia Jejuno-ileal atresia (JIA) is the commonest type of intestinal atresia and accounts for around 1 in 5000 to 1 in 14,000 live births. Over one third of affected children are born prematurely, there is no sex predominance and usually there are no associated chromosomal abnormalities (b1%). Small bowel atresias are classified using Louw's classification (Table 1, Fig. 2) and the relative frequency spreads reasonably evenly between 4 groups. Type III is further subdivided (as per Grosfeld et al. [14]) to account for IIIb — the apple peel atresia which is present in 7% of JIAs. The apple peel deformity results in an atresia just beyond the DJ flexure, with the remaining small bowel coiled around the ileocolic artery. The superior mesenteric artery is absent beyond the origin of the middle colic vessel. Type IIIb and IV atresias are more commonly
Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
S.D. Adams, M.P. Stanton / Early Human Development xxx (2014) xxx–xxx Table 1 Louw's classification & Grosfeld's modification. Type of atresia
Description
I II III
Internal membrane, serosa in continuity, no mesenteric defect Serosal discontinuity, cord between proximal and distal ends Serosal discontinuity with mesenteric defect (subdivided by Grosfeld into a and b) Mesenteric defect only Apple peel deformity Multiple atresias
IIIa IIIb IV
associated with a significant loss of intestinal length. Jejunal atresias are more common than ileal and the more distal the atresia the less frequent the incidence [5]. Since the initial experiments of Louw and Barnard in the 1950s [15], it has been assumed that JIA results from a vascular insult late in foetal life. It has been accurately reproduced by ligation of mesenteric vessels in-utero in canine studies and analysis of the post-atretic intestinal content demonstrates bile salts, epithelial cells and ingested lanugo hair in humans [6]. Associated conditions may be related to the aetiology of the condition; JIA is present in approximately 10% of infants with gastroschisis and 10% of infants with JIA will also have cystic fibrosis. Routine screening for CF is now undertaken for all newborns in the UK, with an associated improvement in clinical outcome for infants diagnosed in the neonatal period [7]. Some centres suggest formal screening (genetic screen or sweat test) to produce higher sensitivity than is provided by the immuno-
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reactive trypsinogen as currently undertaken in the UK by the newborn screening blood spot test. Malrotation is present in 20% however volvulus is present in 25% at operation — if volvulus occurs antenatally then it may lead to intestinal loss and the development of an atresia (typically Type IIIb). Concurrent duodenal or colonic atresia may occur in up to 6%. Antenatal detection of JIA has been reported in approximately half of cases in some series. Multiple dilated loops (e.g. N 7 mm diameter), cystic mass, ascites or polyhydramnios may be seen. The combination of dilated bowel and polyhydramnios may be particularly suggestive. Foetal echogenic bowel can be a transient finding and postnatally the majority will not have intestinal pathology. Post-natal presenting features are bilious vomiting, abdominal distension and delayed passage of meconium. Normal coloured meconium may be present, but it is more usual for pale plugs to be passed or produced if rectal washouts are administered. The presentation can be similar to that of malrotation and mid-gut volvulus and must therefore be investigated as an emergency. Plain abdominal radiography alone is usually diagnostic, with swallowed air acting as a contrast medium (Fig. 3). In proximal atresias, a small number of dilated loops are seen with an absence of distal air. The presence of calcification implies pre-natal bowel perforation of the proximal atretic segment leading to meconium pseudocyst formation. An upper GI contrast can be utilised to exclude malrotation. Contrast enema may be required to differentiate distal atresia from meconium ileus, Hirschsprung disease or small left colon syndrome. Atresia is excluded if contrast refluxes into dilated gas-filled loops of bowel, with an unused appearance of the colon. Once the diagnosis is confirmed, nasogastric decompression and fluid resuscitation are instituted. The operative strategy depends on
I
II
IIIa
IIIb
IV
Fig. 2. Classification of bowel atresia. Adapted from Grosfeld JL et al. J Pediatr Surg 1979;14:368–75.
Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
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Fig. 3. Plain abdominal radiograph demonstrating multiple dilated bowel loops in keeping with an ileal atresia.
the operative findings, but resection of the dilated proximal end, and primary anastomosis to the distal portion, is usually undertaken. Multiple atresias may be anastomosed but will more commonly be provided with a covering stoma. Short-term parenteral nutrition (PN) is required in the majority whilst normal intestinal function resumes. The prognosis for JIA is generally related to the total length of the remaining intestine and the presence of an intact ileo-caecal valve. For example, infants with N100 cm of intestine are likely to require short-term PN only, whereas at b25 cm, long-term PN, intestinal lengthening procedures and consideration for liver/small bowel transplantation will be necessary. The two commonly used lengthening procedures are the serial transverse enteroplasty procedure (STEP) and longitudinal intestinal lengthening procedure (LILT). JIA accounts for 10% of the surgical causes of intestinal failure, with gastroschisis and necrotising enterocolitis making up the majority. Overall survival with JIA is expected to be N90%.
There is a slight male preponderance (1.4:1). Around 30% of children with DA will also have trisomy 21 and up to 25% with DA have structural cardiac defects. Conversely 8% of children with trisomy 21 will also have DA. Up to 10% of affected children will be malrotated and a proportion will have the VACTERL association or some of its component parts. Around 7% will have another intestinal atresia [9]. DA will often (44–51%) present antenatally with the sonographic finding of polyhydramnios leading to later scans and the detection of a ‘double bubble’ in the third trimester. This is explained by the presence of amniotic fluid in the stomach and proximal duodenum. The double bubble, containing swallowed air, without the presence of distal gas, is also the typical finding on a post-natal plain abdominal radiograph (Fig. 4). Infants present with vomiting in the first 48 h of life; this is bilious in 80% (post-ampullary). In the remaining 20% the vomit is not bilestained as the obstruction occurs proximal to the insertion of the common bile duct in the second part of the duodenum (pre-ampullary). The most important differential diagnosis at presentation is malrotation with mid-gut volvulus. Clues to differentiating malrotation and DA include the antenatal history and radiographic features such as a smooth outline to the most distal point of a double bubble (DA), rather than the ‘birds beak’ (suggestive of malrotation). However, any suspicion of this diagnosis mandates emergency investigation and/or operative intervention. Distal gas beyond the double bubble may be indicative of malrotation/volvulus, but can also occur in the rare anatomical variant of a bifid common bile duct (or even pancreatic duct) inserting into the proximal and distal duodenal segments. Initial management of DA is with nasogastric drainage, supportive treatment and examination/ investigation to assess for the presence of associated anomalies. Surgical correction is not usually an emergency. Operative intervention is usually with duodeno-duodenostomy, where the proximal and distal duodenal pouches are opened and joined, effectively bypassing the atretic segment. This procedure can be performed either open or laparoscopically. A duodenal membrane can be dealt with by means of a vertical duodenotomy, web resection
4. Duodenal atresia Duodenal atresia (DA) occurs in around 1 in 10,000 live births and represents up to 60% of intestinal atresias [7]. The aetiology of DA was originally thought to be quite different from the vascular theory which applies to other intestinal atresias; rather the duodenal lumen became occluded during epithelial proliferation and failed to re-canalise in the 2nd gestational month, as first proposed by Tandler in 1900. Since then, little more has been established regarding the pathogenesis of DA in humans. Recent research has focussed on the role of the fibroblast growth factor pathway in mice. An autosomal recessive phenotype of duodenal and colonic atresia can be produced in a murine model by knock-out of the fibroblast growth factor receptor 2b [8]. Classification is similar to other intestinal atresias, with Type I (membrane or web causing luminal obstruction) accounting for up to 90% of cases. Type I atresias or stenoses can lead to the ‘windsock’ anomaly — surgically relevant as the obstructing membrane distends distally leading to the external appearance of dilatation beyond the actual level of obstruction.
Fig. 4. Plain chest and abdominal radiograph demonstrating the ‘double bubble’ appearance suggestive of duodenal atresia. There is a rounded end to the proximal duodenal pouch and no distal gas.
Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
S.D. Adams, M.P. Stanton / Early Human Development xxx (2014) xxx–xxx
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and transverse closure. Duodeno-jejunostomy can be performed if duodeno-duodenostomy is not possible, but is associated with a greater risk of blind-loop syndrome. Operative findings can also demonstrate another causative or associated pathology — for example annular pancreas, malrotation or second distal intestinal atresia. Post-operatively, parenteral nutrition can usually be avoided and some centres advocate placement of a trans-anastomotic tube to facilitate early jejunal feed whilst normal gastro-duodenal function resumes [10]. There is an associated mortality rate of around 5% with DA; this is related to the high rate of associated anomalies. The long-term outcome is usually very good in terms of intestinal function. Rarely, gross dilatation of the proximal duodenum may develop over time, amenable either to re-anastomosis or tapering duodenoplasty. Pyloric atresia is a very rare anomaly showing autosomal recessive inheritance when associated with epidermolysis bullosa. The aetiology is also thought to be a failure of vacuolisation of the solid pyloric lumen. Membranous obstruction is more common than a true atresia and can be corrected by web excision or pyloroplasty. True atresia requires gastro-duodenostomy.
rectal biopsy before primary anastomosis is undertaken. The outcome of isolated CA cases is good in terms of bowel function as overall bowel length is usually not significantly reduced.
5. Colonic atresia
Further experimental evidence to outline the process of ‘rotation’ in the human foetus is likely to clarify our understanding of this condition. The vascular theory of JIA still relies on evidence from the 1950s. The fibroblast growth factor pathway, and its elimination in a murine model, may provide clues as to the aetiology. Research in the management of short-gut syndrome are currently directed at the optimal use of PN/minimising its side effects and assessing the outcome of bowel lengthening procedures and transplantation.
Colonic atresia (CA) is a rare anomaly making up 2–15% of intestinal atresias. CA is classified according to the same system as other bowel atresias as described by Louw [6] and is likely to share a common vascular aetiology. The estimated incidence varies between 1 in 10,000 and 1 in 66,000. The affected segment is more commonly the right colon than the left, and a type III atresia (mesenteric defect separating the blind ends) usually results. There is a slight predominance of males over females (4:3). There is a significant mortality associated with CA, estimated at 25% in one literature review [11]. However, this is likely to represent cases of significantly delayed diagnosis, and individual series reports 0% mortality. CA differs from other bowel atresias in terms of its associations. Hirschpsrung disease has been reported in association with CA in a small number of cases (b 20) [12]. It has been speculated that CA may arise from volvulus of the dilated colon proximal to the affected aganglionic segment. Alternatively, atresia in itself may prevent migration of enteric neurones. Although an unusual association, this should be considered if a primary repair is undertaken. The small number of reported cases does not allow firm conclusions to be drawn regarding location of the atresia and risk of associated aganglionosis. CA also occurs in association with gastroschisis and it has been postulated that constriction at the umbilical ring may be causative. Antenatal detection of distal bowel atresia in general may be suggested by the finding of bowel dilatation, but specific detection of CA has only been described once [13]. Polyhydramnios does not usually occur due to amniotic fluid absorption in the foetal proximal small bowel. Infants present in the first 48 h with typical features of distal intestinal obstruction — distension, failure to pass meconium and bilious vomiting. The proximal colon is often hugely dilated and thus palpable. This is particularly concerning as a closed loop colonic obstruction may form in the presence of a competent ileo-caecal valve. As with other atresias, correction of dehydration and naso-gastric decompression is initiated. Abdominal radiograph will demonstrate very dilated loops of bowel. Contrast enema may be confirmatory, although the degree of clinical distension, absence of meconium and findings on plain radiograph will often be sufficient to merit laparotomy. Two surgical approaches are described. Primary excision and anastomosis are possible, particularly when the right colon is affected. Alternatively, a staged approach, often preferred for left-sided atresia, with initial stoma formation and delayed repair may be undertaken. Although a rare association, it is important to exclude distal aganglionosis with
6. Key guidelines Bilious (dark green) vomiting in an infant should always be regarded as abnormal and a high level of suspicion should be held for malrotation initially; the presentation of malrotation can occasionally be confused with DA and JIA. Suspicion of trisomy 21 should be high in DA. JIA may be suspected antenatally in about half of cases by the presence of dilated bowel and polyhydramnios. Overall outcomes are good; a small proportion will have short-gut syndrome. Hirschsprung disease should be considered and excluded in cases of CA. 7. Research directions
Conflict of interest statement The authors declare that there are no relevant conflicts of interest regarding the preparation of this invited review article. References [1] Kluth D, Jaeschke-Melli S, Fiegel H. The embryology of gut rotation. Semin Pediatr Surg 2003;12(4):275–9. [2] Yanez R, Spitz L. Intestinal malrotation presenting outside the neonatal period. Arch Dis Child 1986;61:682–5. [3] Kiely EM, Pierro A, Pierce C, Cross K, De Coppi P. Clot dissolution: a novel treatment of midgut volvulus. Pediatrics 2012;129:e1601–4. [4] Gohary Y, Alagtal M, Gillick J. Long-term complications following operative intervention for intestinal malrotation: a 10-year review. Pediatr Surg Int 2010;26:203–6. [5] Calisti A, Olivieri C, Coletta R, Briganti V, Oriolo L, Giannino G. Jejunoileal atresia: factors affecting the outcome and long-term sequelae. J Clin Neonatol 2012;1(1): 38–41. [6] Louw JH. Jejunoileal atresia and stenosis. J Pediatr Surg 1966;1(1):8–23. [7] Best KE, Tennant PWG, Addor M-C, Bianchi F, Boyd P, Calzolari E, et al. Epidemiology of small intestinal atresia in Europe: a register-based study. Arch Dis Child Fetal Neonatal Ed 2012;97:F353–8. [8] Kanard RC, Fairbanks TJ, De Langhe SP, Sala FG, Del Moral PM, Lopez CA, et al. Fibroblast growth factor-10 serves a regulatory role in duodenal development. J Pediatr Surg 2005;40:313–6. [9] Choudhry MS, Rahman N, Boyd P, Lakhoo K. Duodenal atresia: associated anomalies, prenatal diagnosis and outcome. Pediatr Surg Int 2009;25:727–30. [10] Hall NJ, Drewett M, Wheeler RA, Griffiths DM, Kitteringham LJ, Burge DM. Transanastomotic tubes reduce the need for central venous access and parenteral nutrition in infants with congenital duodenal obstruction. Pediatr Surg Int 2011; 27:851–5. [11] Etensel B, Temir G, Karkiner A, Melek M, Edirne Y, Karaca I, et al. Atresia of the colon. J Pediatr Surg 2005;40(8):1258–68. [12] Seo T, Ando H, Watanabe Y, Harada T, Ito F, Kaneko K, et al. Colonic atresia and Hirschsprung's disease: importance of histologic examination of the distal bowel. J Pediatr Surg 2002;37(8):E19. [13] Anderson N, Malpas T, Robertson R. Prenatal diagnosis of colon atresia. Pediatr Radiol 1993;23(1):63–4. [14] Grosfeld JL, Ballantine TVN, Shoemaker R. Operative management of intestinal atresia and stenosis based on pathologic findings. J Pediatr Surg 1979;14(3):368–75. [15] Louw JH, Barnard CN. Congenital intestinal atresia. Lancet 1955;19:1065–7.
Please cite this article as: Adams SD, Stanton MP, Malrotation and intestinal atresias, Early Hum Dev (2014), http://dx.doi.org/10.1016/ j.earlhumdev.2014.09.017
