What Is Known
- Pediatric colonoscopy/lower gastrointestinal endoscopy is an important diagnostic and therapeutic tool.
- Recurrent abdominal pain and isolated rectal bleeding are frequent reasons for referral and endoscopy.
What Is New
- A proportion of patients with a normal colonoscopy/lower gastrointestinal endoscopy could potentially have avoided the procedure in the first instance.
- Patients with recurrent abdominal pain in the absence of concerning features should avoid undergoing endoscopy.
- Patients with isolated rectal bleeding should have a trial of conservative management before undergoing endoscopy.
The first reports of pediatric colonoscopy date back to the 1970s (1,2). Since then, pediatric colonoscopy has been undertaken for the investigation of a variety of indications. In a large multicenter study in the USA of approximately 6700 pediatric colonoscopies and 2000 sigmoidoscopies, the indications were abdominal pain (31%), hematochezia (31%), diarrhea (24%), weight loss (10%), and anemia (4%) (3). The findings were as follows: normal (41%), other (stricture/stenosis, tumor, anatomic deformity, Crohn disease, colitis, fissure/fistula/melanosis) (27%), mucosal abnormality (including pouchitis and proctitis) (21%), polyp (9%), and multiple polyps (2%). Others have reported similar normal rates of 38% to 45% (4–6). Pediatric colonoscopy is not without risk and complication rates have been up to 1.1% with perforation rates of 0.01% to 0.11% with no reported deaths (4,5,7,8).
Although pediatric colonoscopy has been important in the diagnosis of inflammatory bowel disease (IBD), polyposis syndromes, graft versus host disease (GVHD), and vascular malformations, its use in evaluating other indications such as isolated rectal bleeding and recurrent abdominal pain in the absence of concerning features has not been well described (9,10). Thus, we have undertaken an audit of our lower gastrointestinal endoscopy (LGIE)/colonoscopy experience during a 10-year period to evaluate its usefulness in assessing otherwise normal children with these symptoms. A secondary aim of this audit was to determine whether unnecessary LGIE/colonoscopy could be avoided in light of increased pressure on waiting lists for colonoscopies.
A retrospective analysis of patients at The Children's Hospital at Westmead who had been booked for colonoscopy from 1st January 2001 to 31st December 2010 was performed and included all patients undergoing LGIE/colonoscopy henceforth referred to as colonoscopy. During this period, a total of 999 colonoscopies were performed by 6 endoscopists. Our hospital is 1 of 3 in the state of NSW (New South Wales) (population approximately 7.6 million (11)) with tertiary referral pediatric gastroenterology services. Patients were reviewed in clinic or on an inpatient service before being booked for colonoscopy. The following data were collected: age, date of colonoscopy, sex, consultant physician, indication for colonoscopy, additional procedures at the time of colonoscopy, macroscopic and microscopic findings, diagnosis, and complications. Indication for the procedure was recorded by the consultant endoscopist just before the procedure as part of ongoing peer review audit (12). The distance reached and completeness of colonoscopy was also recorded. There were 5 major indications for colonoscopy: suspected IBD, IBD restaging/follow-up, recurrent abdominal pain, isolated rectal bleeding, and a miscellaneous category including suspected polyps, suspected GVHD, chronic diarrhea, anemia, suspected colitis but not IBD, hematemesis, and melena. If patients with abdominal pain, rectal bleeding, chronic diarrhea, or anemia were suspected of having IBD, they were categorized as having suspected IBD. Patients with isolated abdominal pain were categorized under the recurrent abdominal pain indication and those with rectal bleeding alone with fresh, bright red blood without anemia were categorized under the isolated rectal bleeding indication. Those with isolated rectal bleeding were distinct from the group with hematemesis and melena or life-threatening gastrointestinal hemorrhage. Those with isolated rectal bleeding with a history of constipation would have a trial of laxatives before having a colonoscopy. Patients who were suspected of having polyps based on family history without rectal bleeding were categorized as suspected polyps and assigned to the miscellaneous category.
A colonoscopy for a new diagnosis of IBD was considered complete if the colonoscope reached the terminal ileum (TI). For the indication of fresh rectal bleeding, if distal pathology was found that could account for fresh rectal bleeding, for example, a solitary polyp, anal fissures not identified in clinic, or nodular lymphoid hyperplasia (not IBD), then a colonoscopy past this point was considered not indicated, but this was at the discretion of the endoscopist. For recurrent abdominal pain, colonoscopy to the cecum or TI was considered complete. For any indication, reasons for an incomplete colonoscopy included severe colitis with risk of perforation, poor bowel preparation, technical difficulties preventing progression, and completion not indicated as with cloacogenic polyps or familial adenomatous polyposis (FAP) with multiple polyps found distally in a family with FAP with or without genetic confirmation of the diagnosis. If the patient had a rectal stump or ileoanal anastomosis with J-pouch, this was recorded. If IBD, other inflammatory disorders, or GVHD was suspected, biopsies were routinely taken. In those with rectal bleeding with a macroscopically normal colonoscopy without diarrhea, biopsies were not routinely taken, although practice varies between endoscopists.
The diagnosis of Crohn disease included granulomatous disease, segmental disease, deep wall inflammation, fistulae, and upper gastrointestinal tract disease. The diagnosis of ulcerative colitis included continuous inflammation from the rectum with mucosal inflammation. If the patient had a J-pouch and was found to have pouchitis, this was classified as such. Those patients who did not fit the definition for Crohn disease or ulcerative colitis were classified as IBD-U (unclassified). A normal diagnosis was defined as follows: no microscopic or macroscopic changes; nonspecific macroscopic changes but normal or nonspecific microscopic findings; and anal fissures. Patients with a diagnosis made on the upper endoscopy with a normal colonoscopy were not allocated to the normal category but to a category with a diagnosis. The data are depicted in figure and chart format. Statistical analysis employing Fisher exact test was done using GraphPad Software (GraphPad Software Inc, La Jolla, CA).
The audit received ethics approval from The Children's Hospital at Westmead.
A total of 999 procedures were included. The 5 main indications for colonoscopy included diagnosis of possible IBD 449 (45%), follow-up or restaging IBD 151 (15%), isolated rectal bleeding 197 (20%), recurrent abdominal pain without other clinical features 46 (5%), and a miscellaneous category which included possible polyps 40 (4%), GVHD 32 (3%), chronic diarrhea not IBD 26 (2.6%), and other miscellaneous 58, (5.8%). There were 559 (56%) males. Figure 1 displays the age ranges and sex of those undergoing colonoscopy. Almost half of all colonoscopies (450/999 or 45%) were performed in those ages 11 to 15 years. For all indications, the median age was 11 years. Numbers are very small in the 16 to 18 age group as patients are not accepted in a pediatric service over the age of 16 for initial presentation and only long-term patients with chronic medical conditions are followed until school leaving (approximately 18 years). In those who underwent colonoscopy for a new diagnosis of IBD, in the age ranges 0 to 5 years, 6 to 10 years, 11 to 15 years, and 16 to 18 years there were 57, 101, 252, and 39 colonoscopies, respectively, with a median age of 11.6 years. In those with rectal bleeding, in the age ranges 0 to 5 years, 6 to 10 years, 11 to 15 years, and 16 to 18 years there were 75, 63, 58, and 1 colonoscopies, respectively, with a median age was 8.2 years.
The cecum and/or TI were reached in 521 of 999 (52%) and ascending colon in a further 6%. There were 3 rectal stump examinations and 9 patients with J-pouch inflammation leaving 466 of 999 (47%) incomplete procedures in patients in whom a full colonoscopy was possible. Reasons for failure to complete the procedure included 104 moderate to severe colitis in which risk was deemed too high, 142 thought not indicated by the senior endoscopist, 56 poor bowel preparation, 11 technical failure, and 153 no reason. There was no relation between completion rates and abnormal or normal findings at colonoscopy except in the group who were undergoing colonoscopy for the diagnosis of suspected IBD.
Findings at colonoscopy are depicted in Figure 2. Thirty-nine percent (390/999) of all colonoscopies, which included 51 with anal fissures, were normal. From 2001 to 2005, there were 177 normal colonoscopies out of 448 (40%) and from 2006 to 2010 there were 213 normal colonoscopies out of 551 (39%). Our preliminary data show that in the era after this audit was completed (2011–2014), there was a decline in normal rates of colonoscopy (data not shown). The percentage of normal colonoscopies done for suspected IBD from 2001 to 2005 was 62 of 177 (35%) and for 2006 to 2010 was 81 of 213 (38%). In all those with a normal colonoscopy, 342 of 390 (88%) had biopsies taken. Fifty-three of the 390 normal procedures would have been difficult to avoid—in other words there was a compelling indication for undertaking the procedure (13 for investigation of anemia, 9 for a family history of FAP, 5 for hematemesis and melena, 2 for suspected GVHD, 1 for autoimmune enteropathy, and 23 in which IBD was suspected in a child with a strong family history of IBD). Six hundred nine (61%) colonoscopies were abnormal (Fig. 2), the majority of whom had a diagnosis of IBD. Twenty-four patients had polyposis syndromes (12 FAP, 10 Peutz-Jeghers syndrome, 1 juvenile polyposis syndrome, and 1 other) but no diagnosis of colon cancer was made.
Diagnosis of IBD was the commonest indication for colonoscopy accounting for 449 of 999 (45%) of colonoscopies. Colonoscopy for suspected IBD confirmed the diagnosis in 282 of 449 (63%) but was normal in 143 of 449 (32%) (Fig. 3). Of the 143 with a normal colonoscopy, 4 were anal fissures and excluded from further analysis as they had a diagnosis, leaving 139. One hundred three of 139 normal colonoscopies underwent screening nuclear labeled white cell scan before colonoscopy, of which 52 (50%) were positive suggesting a possible diagnosis of IBD (but false-positive tests due to minor Peyer patch uptake of the tracer). In total, there were 62 of 139 (45%) with a combination of either abnormal white cell scans or abnormal inflammatory markers or both abnormal white cell scans and inflammatory markers. In 37 of 139 (27%), both white cell scans and inflammatory markers were normal. In the remaining 40 of 139 (29%), 6 had normal white cell scans with missing data on inflammatory markers, 13 had no white cell scan with normal inflammatory markers, and 21 had no white cell scans with missing data on inflammatory markers. Twenty-three of the 143 (16%) had a family history (18 of IBD and 5 other autoimmune diseases). There were an additional 151 out of 999 (15%) of colonoscopies conducted for patients with known IBD who required follow-up colonoscopy. Forty-six of 999 (5%) of colonoscopies performed for recurrent abdominal pain in an otherwise well child were all normal with a completion rate to the cecum and beyond of 72%.
Isolated rectal bleeding was one of the commonest indications for colonoscopy performed in 197 of 999 (20%). The final diagnosis after colonoscopy for isolated rectal bleeding was normal in 141 of 197 colonoscopies or 72%, of whom 46 (23%) had anal fissures not detected at initial consultation. There was no relation between completion rates and those with abnormal or normal findings. Only 56 (28%) were abnormal with juvenile polyps found in 39 (20%), IBD in 6 (3%), 3 vascular malformations, 3 rectal prolapse with cloacogenic polyps, 2 cow milk protein intolerance, and 1 each of portal hypertensive colonopathy, anal stenosis, and self-inflicted injury. Of the 39 colonoscopies in which juvenile polyps were found, 2 patients had 2 colonoscopies for a total of 37 patients. A solitary polyp was found in 36 patients and 2 polyps in 1 patient. One juvenile polyp was found in the transverse colon but the remaining 36 patients had left-sided polyps. None of the patients who underwent colonoscopy for rectal bleeding were found to have a polyposis syndrome.
After colonoscopy, there were 13 abdominal plain films obtained for clinical concern but only 2 perforations during the 10-year period for a rate of 0.2%. Both patients had severe Crohn disease, 1 was previously diagnosed and having his or her disease restaged and another for diagnosis of suspected IBD. There were no deaths.
Pediatric LGIE/colonoscopy is undertaken for a diverse range of gastrointestinal problems. A significant percentage of patients undergoing this procedure, however, either do not have pathology identified or have a trivial cause of symptoms and thus the procedure is potentially avoidable with a more conservative management approach and more stringent screening procedures before the procedure.
One of the commonest indications for colonoscopies is the investigation of isolated rectal bleeding, which accounted for 20% of all colonoscopies. This is similar to other studies, which have found that 11% to 28% of colonoscopies were done to investigate rectal bleeding (5,7,8). In 72% of our colonoscopies for this indication, the colon was normal. One study reported a normal rate of 20% for those undergoing colonoscopy for rectal bleeding (13). The present study, however, included patients with other associated features such as 52% abdominal pain and 28% diarrhea, whereas our study assessed isolated rectal bleeding. An older study of sigmoidoscopies for minor lower gastrointestinal bleeding reported a normal rate of 40% (14); however, those with anal fissures were already excluded from this study. Our study is unique as we assessed rectal bleeding in the absence of associated features and determined the value of colonoscopy in yielding a diagnosis.
A possibility for our high normal rate in those with rectal bleeding is likely related to the low threshold for undertaking a procedure in a child presenting with rectal bleeding and the difficulty in observing anal fissures in the clinic setting in small children. Indeed, for the indication of rectal bleeding, the group ages 0 to 5 years was the largest age group to undergo a colonoscopy. Although pediatric colonoscopy completion rates to the TI have been reported to be 65% to 83% (5,15,16), we did not find evidence that lower completion rates influenced findings at colonoscopy for rectal bleeding. It is unlikely that failure to complete the colonoscopy to cecum or TI will explain our high percentage of normal findings as right-sided lesions are not likely to cause trivial rectal bleeding and only 4 patients during the 10 years returned for a second colonoscopy for rectal bleeding in which the initial procedure was normal (with no significant pathology found on repeat colonoscopy). Moreover, the risk of malignancy is very low in this age group, and thus reducing the necessity for complete examination of the colon. The age-adjusted incidence rate in children and adolescents with cancer from the Surveillance, Epidemiology, and End Results database in the USA was extremely low at 0.38 per million (17). Importantly, there were no significant changes from 1973 to 2005. Although there are reports of adenomatous changes in polyps (9,18,19), it seems unlikely in the absence of any changes in the incidence over time that colonoscopy and removal of dysplastic lesions had much, if any impact on this. In a review of 77 patients with colorectal cancer ages 7 to 19 years, 76 of 77 had more than 1 symptom of colorectal cancer and 77% were anemic at presentation (20). In our series, there was 1 child undergoing surveillance for a cancer syndrome who had a tubulovillous adenoma and no cases of colon cancer.
We did not encounter any polyposis syndromes in those undergoing colonoscopy for isolated rectal bleeding. When all indications were, however, considered, 2 patients with polyposis syndromes were found accounting for 4% of those with polyps. Others have reported multiple polyps in 2% of those who had undergone colonoscopy for any indication (3). Juvenile polyposis syndrome is rare and occurs in 1 in every 100,000 persons (21). Fox et al (10) describe a retrospective study of 192 children in the USA with juvenile polyps, of which 117 (60.9%) had solitary polyps and 75 (39%) had multiple polyps. In 10 of 23 (43.5%) mothers of patients with multiple polyps, genetic testing was positive for juvenile polyposis syndrome. Hood et al (22) describe a retrospective study of 93 patients in the USA with juvenile polyps, of which 62 of 93 (66.7%) were single, 15 of 93 (16.1%) had multiple polyps defined as 2 to 4 juvenile polyps limited to the colon, and 16 of 93 (17.2%) had juvenile polyposis syndrome. In those with single juvenile polyps, 98% were in the rectosigmoid. When their data from all juvenile polyps were considered, the distribution of polyps was as follows: rectosigmoid (64%), left colon (14.8%), transverse colon (11.4%), and right colon (11.8%). In those with juvenile polyposis syndrome, anemia (≤105 g/L) was more common than for multiple or single juvenile polyps. Therefore, we propose that a reasonable management approach for the patient presenting with mild rectal bleeding without a family history of polyposis syndromes or clinical features such as anemia is a trial of laxatives before proceeding to colonoscopy, regardless of whether they have a history of constipation. Although we did not collect data on the number of patients who failed a trial of laxatives before proceeding to colonoscopy, this measure may avoid colonoscopy in up to 2 of 3 patients with this indication. A case could also be made for not proceeding to full colonoscopy in patients with solitary juvenile polyps in the rectosigmoid region.
Our most common indication for a colonoscopy was for the diagnosis of IBD, which accounted for 45% of this series. A diagnosis of IBD was made in 63% and in 32% the procedure was normal with higher completion rates in those with normal colonoscopies. We believe that this normal rate is high, although Mamula et al (5) found 42% (25/60) with chronic colitis, 13% (8/60) with acute colitis, and 45% (27/60) with normal colons. In our audit, it was interesting that in those with suspected IBD, 50% had a normal white cell scan and 27% had both normal white cell scans and normal inflammatory markers, yet these individuals underwent a colonoscopy. In 45% there were abnormal white cell scans, raised inflammatory markers, or both, which likely influenced the decision to proceed with the colonoscopy. It may be that parental anxiety contributed to undertaking colonoscopy in this group; however, this was difficult to determine in a retrospective audit. Indeed, 35% to 38% of normal colonoscopies were done for suspected IBD. This audit was conducted before the era of fecal calprotectin, which for the diagnosis of pediatric IBD, has a high pooled sensitivity of 0.978 and moderate specificity 0.682 (23). Preprocedure screening with fecal calprotectin would likely reduce the normal colonoscopy rate for suspected cases of IBD.
Colonoscopies performed for recurrent abdominal pain in the absence of any other symptoms were normal with completion rates being highest in this group. Although there were only 46 procedures done to investigate recurrent abdominal pain, this suggests that there is little utility for colonoscopy for this indication. In a retrospective study of 243 children with abdominal pain referred to a gastroenterology clinic, 121 (49.8%) were found to have organic disease and 122 (50.2%) were found to have pain-predominant functional gastrointestinal disorders (24). A colonoscopy was done in 21 of 122 (17%) of those patients with functional pain, of which 2 of 21 (9.5%) had abnormal findings (rare fork crypts, lymphoid hyperplasia). Amazingly, they found the average cost of working up functional abdominal pain including laboratory tests, imaging, and endoscopy was $6104.30 (USD) per patient. Recurrent abdominal pain is often a reason for referral to a gastroenterologist and parents pressure physicians for further investigation such as endoscopic examination. The data, however, indicate that colonoscopy does not usually yield a diagnosis in isolated recurrent abdominal pain and moreover a negative colonoscopy has not been shown to improve outcomes in those with functional pain (25).
One of the main limitations of the present study is that it was done retrospectively. It proved difficult to tease out whether parental pressure or attitudes of the endoscopist led to the relatively high rate of normal procedures. Indeed, although there is a general consensus among our endoscopists to reduce unnecessary colonoscopies, individual practice can be variable as no strict protocols exist and other factors apart from medical can influence the decision to undertake a colonoscopy. A more compelling question not completely answered by such an audit is whether completing the procedure to the TI or doing it in the first place had any bearing on the outcome in many submitted to colonoscopy, although the data do not suggest that our completion rates influenced whether pathology was found. The data also question the utility of colonoscopy in the majority of patients with mild rectal bleeding alone. Finally, a prospective study incorporating fecal calprotectin would be useful to determine whether this reduces the normal rate in patients with suspected IBD.
Absence of pathology is a common finding in pediatric colonoscopy. Thirty-nine percent of colonoscopies in this series were normal. Many of these could have been avoided by eliminating colonoscopy in patients with recurrent abdominal pain in the absence of other clinical features, conservative management with laxatives, and taking a “wait and see” approach in patients with the passage of small amounts of fresh blood per rectum typical of anal fissures, and fecal calprotectin measurement in patients with suspected IBD.
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