Abstract
Introduction
Contrast enemas are often made prior to stoma reversal in order to detect distal intestinal strictures distal of the stoma. If untreated these strictures can cause obstruction which might necessitate redo-surgery. However, the value of contrast enemas is unclear. Therefore, we aim to evaluate the contrast enema's diagnostic accuracy in detecting strictures in children with a stoma.
Methods
Young children (≤3 years) treated with a stoma between 1998 and 2018 were retrospectively included. The STARD criteria were followed. Patients treated for anorectal malformations and those that died before stoma reversal were excluded. Surgical identification of strictures during reversal or redo-surgery within three months was used as gold standard. Sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV) and area under the curve (AUC) reflected diagnostic accuracy.
Results
In 224 included children, strictures were found during reversal in 10% of which 95% in patients treated for necrotizing enterocolitis. Contrast enema was performed in 68% of all patients and detected 92% of the strictures. In the overall cohort, the sensitivity was 100%, specificity 98%, PPV 88% and NPV 100% whilst the AUC was 0.98. In patients treated for NEC, the sensitivity was 100%, specificity 97%, PPV 88% and NPV 100% whilst the AUC was 0.98.
Conclusion
Strictures prior to stoma reversal seem to be mainly identified in patients treated for NEC and not in other diseases necessitating a stoma. Moreover, the contrast enema shows excellent diagnostic accuracy in detecting these strictures. For this reason we advise to only perform contrast enemas in patients treated for NEC.
Level of Evidence
II
Keywords
1. Introduction
In young children (age ≤ 3 years), a small bowel stoma or colostomy might be necessary in the treatment of congenital intestinal diseases or abdominal sepsis [
[1]
,[2]
]. Such diseases include necrotizing enterocolitis (NEC), intestinal atresia, Hirschsprung disease, gastroschisis, meconium ileus or peritonitis and focal intestinal perforation. These stomas come with an increased risk of morbidity, considering both stoma creation and reversal, major stoma related morbidity (Clavien-Dindo grade ≥ III) occurs in 39% of the children [[3]
]. Before surgical reversal of the stoma some surgeons ask for a contrast enema, either antegrade via the mucous fistula or retrograde via the anus, of the intestinal tract distal of the stoma in order to detect intestinal strictures.Intestinal strictures can occur owing to unrecognized and untreated atresias or result after ischemic or inflammatory intestinal injury which for instance can occur in patients who experienced NEC [
[4]
]. Post-NEC strictures are a common cause of strictures in these patients reported in 20–30% of the patients following surgical treatment [5
, 6
, 7
, 8
]. If these strictures are not found and treated during stoma reversal, these can result in intestinal obstruction, passage problems and redo-surgery.Previously the diagnostic yield of the contrast enema has been doubted specifically in small bowel stomas [
[9]
]. This study included only four patients with a stricture and excluded colostomies. Therefore, a larger, more inclusive cohort is needed to determine if the contrast enema is useful, and if so in which group of patients.This study aims to evaluate the diagnostic accuracy of a contrast enema in identifying intestinal strictures distal of the stoma in young children (< 3 years of age) prior to stoma reversal.
2. Methods
2.1 Patients and management
All consecutive young children (≤3 years of age) with an intestinal stoma (jejunostomy, ileostomy or colostomy) created between 1998 and 2018 at our tertiary university medical center were retrospectively identified from a surgical administrative database. Patients treated for anorectal malformations were excluded because the indication for a contrast enema in these patients is fistula identification rather than identifying strictures [
[10]
]. Moreover, patients that died before stoma reversal were excluded. The medical ethical committee of the Academic Medical Center in Amsterdam reviewed and approved the study protocol (reference: W18_233#18.278). Patients and parents received an opt-out letter for consent. Following consent, patient records were checked for eligibility. Data was retrieved and stored in an electronic database (Castor EDC). The STARD criteria were followed [[11]
].2.2 Data extraction
We (RES, LES) extracted information concerning: diagnosis leading to stoma formation, if stoma was formed as primary treatment or secondary owing to complications, if patients underwent contrast enema, if the enema was performed via the stoma (antegrade) or anus (retrograde), if complications (allergic reaction or perforation) occurred during or following contrast enema, if strictures were seen on contrast enema, time from contrast enema until stoma reversal, if a stricture was identified during stoma reversal, if a stricture was identified during redo-surgery within three months following stoma reversal and time from reversal to identification of this missed strictures. Lastly the follow up since primary surgery was collected. In case of doubt an experienced pediatric surgeon (JD) was consulted.
2.3 Current practice of the contrast enema
At our institute a contrast enema prior to stoma reversal is performed ideally within four weeks before stoma reversal. Omnipaque© is used as contrast. The Foley catheter size is chosen based on the size of the stoma. A balloon might be inflated during the exam to prevent leakage of contrast, given no contraindications for inflating a balloon is present. The enema is preferably performed antegrade via the mucous fistula but in some cases, e.g. anterograde filling is suboptimal or does not reach the rectum, the enema is performed retrograde via the anus. Contrast enemas are performed and evaluated by specialized pediatric radiologists at our institute.
2.4 Outcome measures
The primary outcome was the diagnostic accuracy of the contrast enema in finding a stricture distal of the stoma. The results of the contrast enema were retrospectively collected. In case of doubt an experienced radiologist (JS) was consulted. If the images of the contrast enemas were no longer available and no definite conclusions could be made based on the written report, a contrast enema was deemed inconclusive. If the contrast enema was deemed inconclusive, this enema was not included in the analysis of the diagnostic accuracy. Identification and treatment during surgery of the strictures, either at stoma reversal or within three months following reversal, was used as the gold standard for intestinal strictures distal of the mucous fistula. In case of a missed second, more distal, stricture in a patient who received treatment for a first stricture, only the diagnostic results of the enema for the first stricture was taken into account. Secondary outcome measures were the incidence of intestinal strictures and the incidence of missed intestinal strictures which were identified during redo-surgery within three months of stoma reversal.
2.5 Statistical analysis
The diagnostic accuracy of the contrast enema was presented by means of the tests sensitivity, specificity, positive predictive value, negative predictive value and area under the curve (AUC) from the receiver operator curve (ROC) with 95%-confidence interval (95%-CI). This was evaluated for the whole cohort as well as for patients treated for necrotizing enterocolitis only. Descriptive characteristics were reported as median with interquartile range in case of non normally distributed variables or mean ± standard deviation (SD) in normally distributed variables. All analyses were performed with IBM SPSS statistics, version 23 (IBM Corp., Armonk, NY, United States).
3. Results
A total of 389 young children were treated with an intestinal stoma in our institute during the study period. A total of 165 patients were excluded of which 126 patients treated for anorectal malformations, 37 patients that died before stoma reversal and two patients who had stoma reversal in a different hospital leaving 224 patients to be included in our analysis. Patients in our cohort were treated for; necrotizing enterocolitis (NEC) (N = 94/224, 42%), Hirschsprung disease (N = 58/224, 26%), intestinal atresia (N = 30/224, 13%), meconium ileus (N = 21/224, 9%), meconium peritonitis (N = 10/224, 4%), gastroschisis with intestinal atresia (N = 7/224, 3%), focal intestinal perforation (FIP) (N = 5/224, 2%). The characteristics of all patients undergoing stoma reversal are presented in Table 1. The overall follow up was a median of 32 months (IQR: 10–95 months).
Table 1Characteristics of patients undergoing stoma reversal.
| N | Primary Stoma (%) | Colostomy (%) | Underwent enema (%) | Antegrade enema (%) | Strictures on enema prior to stoma reversal (%) | Strictures found during stoma reversal (%) | Strictures on enema prior to redo-surgery (%) | Strictures found during redo-surgery (%) | |
|---|---|---|---|---|---|---|---|---|---|
| NEC | 94 | 65 (69%) | 12 (13%) | 81 (86%) | 23(24%) | 22 (27%) | 20 (21%) | 2 (100%) | 2 (100%) |
| Hirschsprung disease | 57 | 55 (96%) | 19 (33%) | 20 (35%) | 9 (16%) | 1 (5%) | 0 | 0 | 0 |
| Intestinal atresia | 30 | 27 (90%) | 5 (19%) | 14 (47%) | 8 (27%) | 1(7%) | 1 (3%) | 1 (100%) | 1 (100%) |
| Meconium ileus | 21 | 20 (90%) | 1(5%) | 17 (81%) | 7 (33%) | 0 | 0 | 0 | 0 |
| Meconium peritonitis | 10 | 9 (90%) | 1 (10%) | 9 (90%) | 5 (50%) | 0 | 0 | 0 | 0 |
| Gastroschisis with intestinal atresia | 7 | 7 (100%) | 1 (14%) | 6 (86%) | 1 (14%) | 0 | 0 | 0 | 0 |
| FIP | 5 | 4 (80%) | 1 (20%) | 4 (90%) | 0 | 0 | 0 | 0 | 0 |
| Total | 224 | 187 (83%) | 40 (18%) | 151 (68%) | 53 (24%) | 24 (16%) | 21 (9%) | 3 (1%) | 3 (1%) |
1 % of all patients within this diagnosis.
2 % of the patients who underwent an enema.
3 In two patients reoperation within three months was necessary for treatment of a missed stricture.
4 One patient treated for a duodenal atresia reported two strictures, both detected on enema, which were treated in separate operations.
3.1 Gold standard strictures identified during surgery
Following our gold standard, 24 strictures were found and treated during either stoma reversal or redo-surgery in 23 patients which is 10% (N = 23/224) of the overall cohort. One patient treated with an intestinal atresia in the duodenum, complicated by a volvulus resulting in stoma formation owing to intestinal ischemia, had two strictures which were both identified by contrast enema but treated in two different operations. 96% (N = 22/23) of the patients who developed a stricture had a history of NEC. Out of all strictures, 88% (N = 21/24) were found during stoma reversal and 12% (N = 3/23) during redo-surgery within three months following stoma reversal. Three strictures were excluded from the analysis of the diagnostic accuracy of the contrast enema. Reasons for exclusion of these strictures were no enema performed prior to stoma reversal, an inconclusive enema and blockage of contrast by a primary stricture which resulted in a missed second, more distal, stricture during redo-surgery.
In the overall cohort 1% (N = 3/224) of the patients had to undergo redo-surgery following stoma reversal owing to a missed stricture. These were two patients treated for NEC and the previously described patient treated for a duodenal atresia with two separate strictures. In both NEC patients, the enema prior to reversal showed a stenosis which was not identified during reversal. Obstructive symptoms necessitated a repeated enema which again was suggestive of a stricture at the same sight. During redo-surgery both strictures were identified and treated.
The patients with strictures that were excluded from the analysis of the diagnostic accuracy of the enema and the patients with strictures that were missed at reversal but found during redo-surgery are discussed briefly in this article, a more extensive description of these patients can be found in Appendix A.
3.2 Usage rate and outcome of the contrast enema
Contrast enemas were performed in 68% (N = 151/224) of the patients prior to stoma reversal, in a median of 22 days (IQR: 8 – 33) before stoma reversal. The usage rate of the contrast enema was 70% (128/184) in patients treated with a small bowel stoma and 58% (N = 23/40) in patients treated with a colostomy. None of the enemas were complicated by an intestinal perforation or an allergic reaction to the contrast. Of the contrast enemas, 36% (N = 54/151) were preformed via the antegrade route, 53% (N = 80/151) retrograde, 5% (N = 8/151) both antegrade and retrograde and in 6% (N = 9/151) it was unclear. 88% (N = 21/24) of the gold standard, surgically proven, strictures were identified prior to surgery via the contrast enema. The other three strictures, were excluded from the analysis of the diagnostic accuracy of the contrast enema and have been described previously.
Table 2 shows the diagnostic accuracy of the contrast enema in the overall cohort. The contrast enema studies were suggestive of a stricture in 16% (N = 24/151) of the studies. Three of the enemas suggestive of a stricture were false positive. These patients will be discussed later. Taking these figures into account the contrast enema in the overall cohort shows a sensitivity of 100%, specificity of 98%, a positive predictive value of 88% and a negative predictive value of 100% whilst the AUC was 0.98 (95%-CI: 0.97–1.00). Of the patients with a positive contrast enema, 92% (N = 22/24) were treated for NEC whilst the other two patients were treated for an intestinal atresia and Hirschsprung disease. An enema suggestive of a stricture was seen in 17% (N = 22/128) of the studies in patients treated with a small bowel stoma. Of the enemas in patients treated with a colostomy this was 9% (N = 2/23). Both were patients treated for NEC and both strictures were found and resected during stoma reversal.
Table 2Predictive capabilities enema full cohort.
| Strictures at surgery | No strictures at surgery | Total row | |
|---|---|---|---|
| Enema positive | 21 | 3 | 24 |
| Enema negative | 0 | 127 | 127 |
| Total row | 21* (14%) | 130 | 151 |
| Sensitivity | 21 / 21 = 100% | PPV | 21 / 24 = 88% |
| Specificity | 127 / 130 = 98% | NPV | 127 / 127 = 100% |
1 Three cases of strictures were excluded, reasons for exclusion are described in the results.
Table 3 shows the diagnostic accuracy of the contrast enema when only taking into account the patients treated for NEC. It shows a sensitivity of 100%, specificity of 97%, a positive predictive value of 91% and a negative predictive value of 100% whilst the AUC was 0.98 (95%-CI: 0.96–1.00).
Table 3Predictive capabilities enema NEC patients.
| Strictures at surgery | No strictures at surgery | Total row | |
|---|---|---|---|
| Enema positive | 20*1 | 2 | 22 |
| Enema negative | 0 | 58 | 58 |
| Total row | 20⁎2 (25%) | 60 | 80⁎2 |
| Sensitivity | 20 / 20 = 100% | PPV | 20 / 22 = 91% |
| Specificity | 58 / 60 = 97% | NPV | 58 / 58 = 100% |
*1: In two patients reoperation within three months was necessary for treatment of the stricture *2: Two patients with a stricture (no enema & inconclusive enema) were excluded from the analysis.
3.3 False positive enemas, no stricture found during surgery
In three patients, two treated for NEC and one for Hirschsprung disease, a stricture was seen on contrast enema whilst no strictures was observed during stoma reversal or redo-surgery making the false positive rate 13% (N = 3/24) in the overall cohort and 9% (N = 2/22) in patients previously treated for NEC. In all of these patients with a false positive enema, the enema suggested of a stricture at the splenic flexure, yet no strictures were identified during surgery and no obstructive symptoms developed during follow up for which reason no redo-surgery was necessary. A more extensive description of these patients can be found in Appendix B.
4. Discussion
In this study of 224 young children treated with an intestinal stoma the incidence of a stricture was 10%. Out of these strictures, 12% were missed during stoma reversal but found during redo-surgery in 1% of the overall cohort. Out of all patients who develop a stricture, 96% had a history of NEC. The contrast enema prior to stoma reversal, which was performed in 68% of all patients and 86% of the patients treated for NEC, detected 88% of these strictures. The diagnostic accuracy of the contrast enema in the overall cohort shows a sensitivity of 100%, specificity of 98%, a positive predictive value of 88% and a negative predictive value of 100% whilst the AUC was 0.98. The diagnostic accuracy of the contrast enema in NEC patients shows a sensitivity of 100%, specificity of 97%, a positive predictive value of 91% and a negative predictive value of 100% whilst the AUC was 0.98. Three patients reported a false positive enema making the false positive rate 13% in the overall cohort and 9% in patients treated for NEC.
We and others show that the contrast enema is routinely used in many patients treated with a small bowel stoma although strictures are rarely identified [
[9]
]. Moreover, our result suggest that the contrast enema is also regularly (58%) performed in patients treated with a colostomy, which has not been shown in previous studies. All but one patient who developed a stricture were previously treated for NEC. The only strictures in a patient not treated for NEC was found in a complicated case of duodenal atresia with multiple sights of intestinal ischemia owing to a volvulus which was caused by an adhesion, which is a rare complication in these patients [[12]
]. Concluding from these results it seems that routine usage of a contrast enema in patients treated for meconium peritonitis, meconium ileus, Hirschsprung disease and focal intestinal perforation should not be recommended as it only increases exposure to ionizing radiation as well as costs.Since almost all strictures are found in patients treated for NEC, we would advise to only perform routine contrast enema prior to stoma reversal in all patients treated for NEC. We conclude this based on the high incidence of post-NEC strictures which develop in one in five patients as our results show. This incidence is similar to previous studies [
[5]
–[8]
]. With an AUC of 0.98 and zero false negative enemas, it seems that the enema has good diagnostic accuracy in detecting post-NEC strictures.There were two NEC patients who needed redo-surgery within days following stoma reversal owing to a missed, but enema proven, stricture. This seems to suggest that these strictures can become symptomatic if not treated. However, it is questionable if all post-NEC strictures identified on contrast enema would have become symptomatic if left untreated. This question can only truly be answered in a randomized controlled trial. Still, by looking at medically, nonsurgical, NEC patients, we might find an indication of the clinical consequence of not treating post-NEC strictures before obstructive symptoms. In patients medically treated for NEC, no stoma is created, or contrast enema is performed so only those strictures that become symptomatic are detected and treated. Still, post-NEC strictures are found in 20–30% of these patients, which is similar to surgically treated NEC patients [
[5]
,[6]
,[8]
]. If the contrast enema would have detected many clinically insignificant strictures, one would expect the incidences to differ more profoundly. The strictures in medically treated NEC patients seem to become symptomatic at 2–3 months following initial NEC, which is approximately the moment of stoma reversal in surgically treated NEC patients. If not treated, patients suffering from post-NEC strictures are reported to have failure to thrive [[5]
–[8]
]. Moreover, no complications of the treatment of post-NEC strictures have been reported, both in our cohort as in previous studies [[6]
–[8]
]. We therefore conclude that it does not seem that contrast enemas lead to an overdiagnosis of post-NEC strictures and that stricture resection seems a relatively safe treatment which can prevent the patient from experiencing failure to thrive and undergoing a re operation.Another hypothetically feasible way to evaluate the clinical relevance of an enema proven stenosis could be mucous fistula feeding. The clinical results of this procedure have been variable and complications, such as intestinal perforations caused by the refeeding catheter, have been described [
[13]
]. However, other studies have suggested that mucous fistula feeding could result in less complications, such as short bowel syndrome and anastomotic leakage [[14]
,[15]
]. In case of a contrast enema proven stenosis, this procedure might show if passage of stool is still possible. However, there is no study evaluating the diagnostic accuracy of mucous fistula feeding in detecting intestinal stenosis. Therefore, it is still hard to conclude the feasibility of this method compared to the contrast enema, although it could be a non invasive, costless and radiation free method.Our results are in contrast with the previous study which reported a post-NEC stricture incidence of only 5% and a high rate of false positive in these patients of 55% (N = 5/9) [
[9]
]. These figures resulted in a low predictive value of 44% in these patients. Since this study did not clearly describe the patients with a false negative enema, it is hard to conclude a reason for this difference. Yet the low incidence of post-NEC strictures will probably have had a large influence.Some surgeons might argue that most strictures can be detected during stoma reversal by clear examination without needing a contrast enema to indicate possible stenotic segments. However, during many stoma reversals the intestine is only partly observed. Inspection of the full intestinal tract would lengthen the duration of the surgery and increase the risk of iatrogenic damage to the intestine. Moreover, we show that at least in two patients the contrast enema did prove to show a stricture which, at stoma reversal, was not detected by our experienced pediatric surgeons whilst both strictures were found at the indicated sight during redo surgery.
In case of a stricture that completely closes the lumen of the intestine, the full tract of the intestine cannot be visualized by using a one-way, antegrade or retrograde, enema. This could lead to missing a second stricture, as we show in one of our patients. Since this stricture was later found on retrograde enema, it could well be that if we had combined antegrade and retrograde enema in this patient we would not have missed the second stricture. In our cohort, eight patients, of which five treated for NEC, received a combined antegrade and retrograde enema owing to uncertainty of full visualization of the intestinal tract. This resulted in the identification of three strictures, all in patients treated for NEC, which were all found and treated during stoma reversal. Therefore, it could be advisable to routinely combine these two enemas in case of incomplete or doubt of the visualization of the intestinal tract.
When evaluating the patients with a false positive contrast enema we noted that in all three patients the enema suggested a stricture at the splenic flexure. In adults, spasms at the in a healthy colon are described to mimic a fixed narrowing resulting in a pseudo-obstruction at or near the splenic flexure [
[16]
]. Although this might be an explanation of our finding, it is unclear if the same illusory image can occur in young children.Our advice only focusses on routinely performing contrast enema in all patients treated with a stoma, with the indication of detecting intestinal strictures prior to stoma reversal. The occurrence of certain complications, such as post-surgery enterocolitis following treatment for Hirschsprung's disease, might increase the likelihood of stenosis development therefore leading to the decision to perform a contrast enema. Moreover, there can certainly be other indications for making a contrast enema such as to determine the transition zone in Hirschsprung disease, to clear impacted meconium in case of meconium ileus and to identify an intestinal atresia which was missed during stoma formation [
17
, 18
, 19
, - Frongia G.
- Günther P.
- Schenk J.P.
- Strube K.
- Kessler M.
- Mehrabi A.
- et al.
Contrast enema for hirschsprung disease investigation: diagnostic accuracy and validity for subsequent diagnostic and surgical planning.
Eur J Pediatr Surg. 2016; 26 (Official Journal of Austrian Association of Pediatric Surgery [et al] = Zeitschrift fur Kinderchirurgie): 207-214
20
]. This is specifically the case in patients with multiple atresias at different sights in the intestinal tract, which occur in up to 23% of the jejunoileal atresias [[21]
]. In our cohort, none of the patients treated for isolated jejunoileal intestinal atresia as for a combined jejunoileal atresia with a gastroschisis had a positive enema nor a missed atresia during surgery. This could indicate that visual identification of these multiple atresias during stoma formation is reliable which in turn could mean a contrast enema prior to reversal is unnecessary.The most profound limitation of this study was its retrospective nature. Because of these reasons we could not evaluate why some patients did receive a contrast enema whilst others did not. It could be that the diagnostic accuracy of the contrast enema would have differed if all patients treated for NEC did receive a contrast enema. Along the same line the reports of contrast enemas are probably only a summary of the actual findings of the radiologists. Still, both the contrast enemas as the surgical procedures, were performed by experienced and specialized medical staff and their reports will have reflected their actual findings.
5. Conclusions
Distal intestinal strictures at stoma reversal seem to be identified almost exclusively in patients treated for necrotizing enterocolitis. This is caused by a high incidence of post-NEC strictures which occurs in one in five patients. The contrast enema seems to be capable to detect these strictures with an AUC of 0.98. We therefore conclude that it seems unwise to perform routine contrast enema in all infants prior to stoma reversal, except following treatment for necrotizing enterocolitis.
Funding
Not applicable.
Declaration of Competing Interest
None to report.
Appendix. Supplementary materials
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Article info
Publication history
Published online: June 25, 2022
Accepted:
June 20,
2022
Received in revised form:
June 5,
2022
Received:
March 20,
2022
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