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Original Articles: Gastroenterology: Inflammatory Bowel Disease

Clinical Practice Survey of Repeat Endoscopy in Pediatric Inflammatory Bowel Disease in North America

Moses, Jonathan; Sandberg, Kelly; Winberry, Gabriel; Riera, Diana§; DeLozier, Sarah||; Gupta, Sandeep K.; Reilly, Norelle#; Park, KT∗∗; Picoraro, Joseph#

Author Information
Journal of Pediatric Gastroenterology and Nutrition: July 2021 - Volume 73 - Issue 1 - p 61-66
doi: 10.1097/MPG.0000000000003100
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Abstract

What Is Known/What Is New

What Is Known

  • Treatment endpoints in the clinical care of inflammatory bowel disease patients have shifted from clinical remission to endoscopic remission.
  • Adoption of this practice has not been well documented in the care of pediatric inflammatory bowel disease patients, given the unique barriers to repeat endoscopy.

What Is New

  • Sixty-five percent of survey respondents utilize repeat endoscopy to assess for endoscopic remission as part of their routine clinical care.
  • Fewer years in practice demonstrated a higher likelihood to repeat endoscopy.

Inflammatory bowel disease (IBD) is a chronic, relapsing disorder encompassing Crohn disease and ulcerative colitis (UC), which requires continuous monitoring using clinical symptoms, laboratory markers, and endoscopic evaluation, among other routine assessments (1,2). Management of IBD patients has shifted from the use of clinical symptoms to guide management to a “treat to target” approach, involving the assessment of endoscopic remission (3). Data from adult IBD populations demonstrates that achieving endoscopic remission translates to fewer hospitalizations, fewer surgeries, longer time spent in remission, and higher quality of life (4–6). Data in pediatrics are less robust, but initial data show similar benefits (7).

Assessment for endoscopic remission requires repeat endoscopic evaluation, which is a major paradigm shift from the use of clinical symptoms to monitor patients and execute therapeutic decisions (3). Increased use of endoscopy could lead to increased cost of care and increased cumulative procedural risk to the patient (8). Unique considerations for pediatric IBD patients include the concerns for repeated anesthesia exposure in younger patients and the central role of parents in the shared decision-making process to perform repeat endoscopy. Recent recommendations from the European Society of Pediatric Gastroenterology, Hepatology, and Nutrition (ESPGHAN) advocate for the practice of repeat endoscopic evaluation (9). Given these barriers and lack of robust pediatric data, it is, however, unclear how often this practice is being employed by practicing pediatric gastroenterologists.

The primary aim of our study was to assess the use of repeat endoscopy to assess for endoscopic remission in pediatric IBD patients following initiation or changes in medical therapy. Our secondary aim was to examine the impact of provider characteristics on the practice of repeat endoscopy in pediatric IBD.

METHODS

Survey Design

The North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition (NASPGHAN) Clinical Care and Quality Committee (CCQ) created a working group to design a cross-sectional survey to assess the practice patterns of pediatric gastroenterologists and nurse practitioners in clinical practice regarding use of repeat endoscopy after the start or change of medical therapy for pediatric IBD patients. The committee members deliberated on the framework of the survey with final decision on content agreed upon by group consensus. The final survey contained 17 content questions and 4 optional post survey questions, with a completion time averaging 5 to 7 minutes. Baseline characteristics collected from each respondent included medical degree, years in practice, primary practice setting, involvement in the ImproveCareNow (ICN) network (www.improvecarenow.org), geographic location, number of IBD patients in the respondent's department/practice, number of IBD patients seen by the respondent, and presence of a pediatric IBD center (defined as a multidisciplinary team with dedicated time to care for pediatric IBD patients).

Survey Distribution

Recruitment took place via 3 email-based platforms: “Peds GI Bulletin Board” listserv (approximately 2700 members), ICN listerv (285 physician members registered), and Association of Pediatric Gastroenterology and Nutrition Nurses (APGNN) listserv (approximately 443 members). The Qualtrics web-based platform (Provo, UT) was used to conduct the survey. Given the known overlap in members between the listservs, we utilized IP address mapping to ensure we received only 1 response per participant. Institutional Review Board approval was obtained at University Hospitals in Cleveland, OH (approval date of March 3, 2020; STUDY20191387). The survey was released on March 30, 2020 to all listservs. Email reminders for the ICN listserv included 2 follow-up reminder emails, along with 1 advertisement of the survey as part of the monthly newsletter to encourage completion of the survey. A single email reminder was sent to the Peds GI listerv 4 weeks after the initial email.

Statistical Analysis

Survey responses were reported as frequencies and percentages. Analyses were conducted comparing participants who utilized repeat endoscopy with those who did not. Comparisons were conducted using chi-square tests or Fisher exact test as appropriate. Participants in both groups were asked to justify their rationales by multiple choice and open-ended response. At the end of the survey, an optional quiz was given in which participants could voluntarily participate.

RESULTS

Baseline Characteristics

A total of 238 unique respondents participated in the survey with a completion rate of 93.3% (Table 1). Total possible respondents were approximately 2300 between the “Peds GI Bulletin Board,” the ICN listserv, and the APGNN listserv, accounting for potential overlap in members of each listserv, for a response rate of 11%. Respondents were physicians (95%) or nurse practitioners (5%). They were located primarily in the United States and Canada (86%), and their location within the United States was diversely distributed, with their primary department or practice locations as being mostly urban (75%).

TABLE 1 - Baseline characteristics of North American survey respondents and analysis of respondents based on repeat endoscopy
Overall Repeat endoscopy, N = 134 No repeat endoscopy, N = 67 P value
Years you have been in practice 0.012
 1 to 5 years 58 (28) 43 (32) 12 (18)
 6 to 10 years 43 (21) 33 (25) 10 (15)
 11 to 15 years 34 (17) 21 (16) 13 (19)
 Greater than 15 years 70 (34) 37 (28) 32 (48)
Practice setting 0.849
 Academic 155 (76) 102 (76) 50 (75)
 Large health system practice (ie, Kaiser) 34 (17) 23 (17) 11 (16)
 Private practice 16 (8) 9 (7) 6 (9)
ImproveCareNow involvement 1.000
 No 59 (29) 39 (29) 20 (30)
 Yes 146 (71) 95 (71) 47 (70)
Region of United States 0.783
 East 53 (27) 34 (27) 18 (27)
 Midwest 65 (33) 40 (31) 25 (37)
 South 49 (25) 34 (27) 14 (21)
 West 30 (15) 20 (16) 10 (15)
Description of Primary Practice Setting 0.365
 Rural 5 (2) 3 (2) 2 (3)
 Suburban 52 (26) 30 (23) 21 (31)
 Urban 145 (72) 100 (75) 44 (66)
Overall volume of IBD patients (department) 0.067
 0 to 100 24 (12) 13 (10) 11 (16)
 101 to 200 40 (20) 26 (20) 13 (19)
 201 to 300 46 (23) 25 (19) 21 (31)
 301 to 400 27 (13) 22 (17) 5 (7)
 More than 400 65 (32) 47 (35) 17 (25)
Number of IBD patients you are primary provider 0.308
 0 to 10 28 (14) 16 (12) 11 (16)
 11 to 50 95 (47) 66 (49) 28 (42)
 51 to 150 64 (32) 39 (29) 25 (37)
 More than 150 16 (8) 13 (10) 3 (4)
Presence of multidisciplinary IBD center 0.096
 No 75 (37) 44 (33) 31 (46)
 Yes 127 (63) 89 (67) 36 (54)
IBD = inflammatory bowel disease.
Overall P value = 0.012; “1–5 years” versus “greater than 15 years,” P value = 0.008; “6–10 years” versus “greater than 15 years,” P value = 0.024; rest of comparisons were nonsignificant.

Focusing on the respondents in North America, length of physicians’ practice duration was distributed across a range of 1 year to more than 15 years (Table 1). The majority (76%) practiced in an academic setting. Most respondents (71%) reported their center as involved in the ICN Network. Number of IBD patients in the department or practice ranged from 0 to 100 (12%) to more than 400 (32%), reflecting diversity in practices (Table 1). Of the total IBD patients, respondents typically reported being the primary provider for 11 to 50 patients (47%) or 51 to 150 patients (32%). The majority of respondents (63%) have a pediatric IBD center at their institution (as defined above).

Endoscopy Protocols

Sixty-five percent of overall respondents stated they utilize repeat endoscopy after initiation or change in primary medication for their pediatric IBD patients. Standard protocols in the department for repeat endoscopy were reported by only 25% of respondents. Amongst respondents reporting no standard protocols in the department, about half (56%) reported repeating endoscopy as individuals. The most common time frames for repeat endoscopy based on department protocol was 9 to 12 months (46%) following initiation or change of medication. Amongst those who reported repeating endoscopy independent of departmental protocol, the time frame was most frequently 9 to 12 months (52%).

Within the category of “Years you have been in practice” in Table 1, we found a significant difference in the overall years in practice (P = 0.012). Examining this further, we found those who answered “1–5 years” and “6–10 years” performed repeat endoscopy significantly more than those who answered “greater than 15 years” (“1–5 years” vs “greater than 15 years,” P value = 0.008; “6–10 years” vs “greater than 15 years,” P value = 0.024). No significant differences were detected among the respondents based on practice setting, ICN involvement, geographic location, region of the United States, description of practice setting, overall volume of IBD patients, number of IBD patients treated by the individual, although presence of a multidisciplinary IBD Center approached, but did not reach, statistical significance (P = 0.069) (Table 1).

Assessment of Motivation to Repeat Endoscopy

Amongst the respondents who reported repeating endoscopy to assess for endoscopic remission, the most common reasons for this were: “symptoms are not sufficient to follow IBD patients” (83%), “liked to know the depth of their patient's remission” (71%), and “to reduce the risk of irreversible bowel damage” (62%) (Fig. 1). Amongst the respondents who did not repeat endoscopy to assess for endoscopic remission, the most common reasons were that: respondents “perform endoscopy based on clinical, biomarker, and/or imaging trends” (81%), and “a combination of clinical activity, biomarkers, and/or imaging accurately determines treatment efficacy” (60%) (Fig. 2). When given rank-order selections of commonly established barriers to repeat endoscopy for endoscopic remission evaluation, respondents’ most frequent responses were “lack of pediatric specific guideline,” and “need for further pediatric specific data on benefits of mucosal healing” (Table 2).

F1
FIGURE 1:
Respondent rationale for utilizing repeat endoscopy when assessing for endoscopic remission.
F2
FIGURE 2:
Respondent rationale for not utilizing repeat endoscopy when assessing for endoscopic remission in routine care.
TABLE 2 - Rank-order responses to “What would enable you or your routine care to regularly repeat endoscopy for endoscopic remission?”
Criteria Mean ranking Rank order
Pediatric-specific guideline 1.87 1
Further pediatric-specific data on benefits of mucosal healing 1.97 2
Shared decision-making tool to talk with/educate patients 3.02 3
Further pediatric-specific data on the safety of repeat endoscopy 3.52 4
Improved integration of endoscopy pictures in the electronic medical record 5.03 5
Other 5.60 6
N = 60.

Post Survey Quiz Results

Most respondents (73%) opted to take the optional quiz at the end of the survey; the content for the quiz was based on published data. Of these, 60% correctly identified the rate of 15% to 40% active endoscopic disease in the presence of clinical remission, based on current published pediatric data. Seventy-two percent correctly agreed there is insufficient data regarding long-term neurodevelopmental effects of repeated procedural sedation in children. Fifty-five percent correctly identified circumstances under which endoscopy should be performed in children based on the recently published ESPGHAN guidelines (9). Finally, 98% correctly answered that patients with Crohn disease and ulcerative colitis who achieve endoscopic remission are less likely to undergo surgery.

DISCUSSION

Using a cross-sectional survey distributed to practicing pediatric gastroenterology providers, we found overall 65% of respondents repeat endoscopy to assess for endoscopic remission in their clinical practice. In addition, amongst those who had no standard departmental protocol, half reported utilization of repeat endoscopy.

“Treat to target” strategy was formally proposed by the International Organization for the Study of Inflammatory Bowel Disease in 2015 with the initiative “Selecting Therapeutic Targets in Inflammatory Bowel Disease” (STRIDE) (3). One of the therapeutic targets of the STRIDE initiative was the absence of ulcerations on endoscopy performed 6 to 9 months after the start of therapy. In our survey, we found the most common time-frame for repeat endoscopy to assess for endoscopic remission was 9 to 12 months. This suggests pediatric gastroenterologists may use adult guidelines in the management of pediatric IBD patients. It is worth noting that 9 to 12 months was the most common time frame in those respondents with and without a departmental protocol, suggesting there may be a different standard in North American centers.

Use of endoscopy in pediatric IBD has been shown to affect patient management, with a rate of up to 48% of repeat endoscopy leading to a management change, most commonly of medication (10). More recently, ESPGHAN published pediatric-specific guidelines on the use of endoscopy in pediatric IBD (9). This included recommendations for endoscopy for the following: before major treatment changes (escalating or de-escalating), in Crohn disease to ensure mucosal healing during clinical remission, and in UC to ensure mucosal healing during clinical remission only if fecal calprotectin is elevated. We did not specifically query our respondents about their practice based on the diagnosis (Crohn disease or UC) but found the majority who do not repeat endoscopy reportedly making treatment decisions based on clinical, biomarker, and/or imaging trends (Fig. 2). This practice could be in line with the ESPGHAN recommendations for UC patients, assuming this included fecal calprotectin as the biomarker utilized. In pediatric UC patients treated with infliximab, a Pediatric Ulcerative Colitis Activity Index of <10 may be sufficient to avoid routine endoscopic evaluation (11). A recent practice survey performed by the Porto IBD Group of ESPGHAN reported full endoscopic work-up is performed in 87% of Crohn disease and 84% UC patients before major treatment changes (12). Although these rates are related specifically to repeat endoscopy before treatment and change and not to assess for endoscopic healing, they likely reflect adoption by a European cohort of the recent ESPGHAN guidelines.

Adult data has demonstrated improved outcomes for patients who achieve endoscopic remission, specifically related to lower need for colectomy in UC and higher rates of steroid-free clinical remission in both Crohn disease and UC (4,5). Endoscopic remission has also been associated with a lower rate of hospitalization for patients with Crohn disease (6). Recent prospective data has shown that endoscopic remission combined with clinical remission has been associated with decreased risk of disease progression in Crohn disease over a median of 3 years’ follow-up (13). Furthermore, a recent cohort demonstrated that complete endoscopic healing predicts better long-term outcomes than partial endoscopic healing, which required repeat endoscopy after initiation of therapy (14). Although there is data demonstrating the benefit of improved long-term outcomes over 3 years when patients achieve early endoscopic remission, robust data on the benefit of endoscopic remission in pediatric IBD is lacking and our survey supported this as a barrier to using repeat endoscopy in this population (15). “Further pediatric specific data on benefits of mucosal healing” ranked highly as a need to justify routine repeat endoscopy in clinical practice (Table 2).

The highest ranked reason given for the use of repeat endoscopy was “symptoms are not sufficient to follow IBD patients”; conversely, we found the majority of respondents who do not repeat endoscopy selected using clinical, biochemical markers, and/or imaging as sufficient to manage pediatric IBD patients. Clearly, there is a range of treatment paradigms in pediatric IBD and wide variation in diagnosis and treatment has been described previously (16). In a single center pediatric cohort, 45% to 67% achieved endoscopic remission, and of those who did not have endoscopic remission, 84% underwent escalation of therapy (17). In this cohort, up to 30% of patients in clinical remission had active disease on endoscopy. This finding was further reinforced with data from the ImageKids study demonstrating 11% to 43% of patients with active inflammation on endoscopy and/or MR enterography were in clinical remission (18). In addition, validated clinical activity indices to assess disease severity have poor correlation with disease severity when assessed by endoscopy (19). These data suggest direct examination by repeat endoscopy will help give a clearer picture of a patient's remission, as compared with using clinical, biochemical, and/or imaging alone. In addition, we found a significant difference between those in practice for the longest period of time (more than 15 years) and the 2 shorter periods of time (1–5 and 6–10 years). As the paradigm of clinical endpoints has evolved in the management of IBD, there has been a shift from using clinical symptoms to drive major therapeutic decisions to using endoscopic assessment (3). This lag time to adopt new practices in medicine has been highlighted in research demonstrating the slow adoption of new clinical practices by physicians, possibly related to the difficulty with “unlearning” common practices and shifting to new ones (20).

A strength of our survey is the novel nature of the data, as this is the first reported experience on the use of repeat endoscopy to assess for endoscopic remission in a predominantly North American cohort. The goal of this study was to capture the global practice patterns when deciding on whether or not to perform repeat endoscopy; however, we were not able to better understand unique clinical scenarios that may be presented to the practicing clinician on a day-to-day basis. Limitations of the data include our response rate of 11% of the total population solicited via the 3 listservs. In addition, those who responded to the survey may have been more motivated to complete the survey, and therefore, have a favorable view on the practice of repeat endoscopy. Another limitation would be the generalizability of this data as most respondents were a part of ICN, an academic center and had an IBD center of excellence in place. Given the low number of responses from non-United States sites, the risk of nonresponse bias is high and the analysis and conclusions of the study were focused to represent the primarily North American cohort of respondents. In addition, assessment of local resources was not part of the survey and could be considered for future studies assessing practice patterns. Finally, the survey was distributed to the listservs during the coronavirus disease-2019 (COVID-19) pandemic. Although it is difficult to quantify how this may have affected the response rate, this may have been a contributing factor to the lower response rate.

CONCLUSIONS

We found a high rate of repeat endoscopy to assess for endoscopic remission as a part of routine clinical practice in pediatric IBD in a primarily North American cohort. Major barriers identified to this practice included perceived lack of pediatric-specific guidelines and long-term data demonstrating clear benefit of this approach. Multicenter, prospective studies to assess for long-term benefit of endoscopic remission in pediatric patients are urgently needed.

Acknowledgments

We would like to thank the ImproveCareNow Network for reviewing the study design and allowing access to their listserv for the survey.

REFERENCES

1. Feuerstein JD, Isaacs KL, Schneider Y, et al. AGA Clinical Practice Guidelines on the management of moderate to severe ulcerative colitis. Gastroenterology 2020; 158:1450–1461.
2. Ruemmele FM, Veres G, Kolho KL, et al. European Crohn's and Colitis Organisation, European Society of Pediatric Gastroenterology, Hepatology and Nutrition. Consensus guidelines of ECCO/ESPGHAN on the medical management of pediatric Crohn's disease. J Crohns Colitis 2014; 8:1179–1207.
3. Peyrin-Biroulet L, Sandborn W, Sands BE, et al. Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE): determining therapeutic goals for treat-to-target. Am J Gastroenterol 2015; 110:1324–1338.
4. Shah SC, Colombel JF, Sands BE, et al. Mucosal healing is associated with improved long-term outcomes of patients with ulcerative colitis: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 2016; 14:1245.e8–1255.e8.
5. Baert F, Moortgat L, Van Assche G, et al. Belgian Inflammatory Bowel Disease Research Group, North-Holland Gut Club. Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn's disease. Gastroenterology 2010; 138:463–468.
6. Schnitzler F, Fidder H, Ferrante M, et al. Mucosal healing predicts long-term outcome of maintenance therapy with infliximab in Crohn's disease. Inflamm Bowel Dis 2009; 15:1295–1301.
7. Nuti F, Civitelli F, Bloise S, et al. Prospective evaluation of the achievement of mucosal healing with anti-TNFα therapy in a Paediatric Crohn's Disease Cohort. J Crohns Colitis 2016; 10:5–12.
8. Ananthakrishnan AN, Korzenik JR, Hur C. Can mucosal healing be a cost-effective endpoint for biologic therapy in Crohn's disease? A decision analysis. Inflamm Bowel Dis 2013; 19:37–44.
9. Oliva S, Thomson M, de Ridder L, et al. Endoscopy in pediatric inflammatory bowel disease: a position paper on behalf of the Porto IBD Group of the European Society for Pediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr 2018; 67:414–430.
10. Thakkar K, Lucia CJ, Ferry GD, et al. Repeat endoscopy affects patient management in pediatric inflammatory bowel disease. Am J Gastroenterol 2009; 104:722–727.
11. Turner D, Griffiths AM, Veerman G, et al. Endoscopic and clinical variables that predict sustained remission in children with ulcerative colitis treated with infliximab. Clin Gastroenterol Hepatol 2013; 11:1460–1465.
12. Bronsky J, de Ridder L, Ruemmele FM, et al. Diagnostic and therapeutic approach in paediatric inflammatory bowel diseases: results from a Clinical Practice Survey. J Pediatr Gastroenterol Nutr 2019; 68:676–683.
13. Ungaro RC, Yzet C, Bossuyt P, et al. Deep remission at 1 year prevents progression of early Crohn's disease. Gastroenterology 2020; 159:139–147.
14. Yzet C, Diouf M, Le Mouel JP, et al. Complete endoscopic healing associated with better outcomes than partial endoscopic healing in patients with Crohn's disease. Clin Gastroenterol Hepatol 2020; 18:2256–2261.
15. Grovera Z, Burgessc C, Muird R, et al. Early mucosal healing with exclusive enteral nutrition is associated with improved outcomes in newly diagnosed children with luminal Crohn's disease. J Crohns Colitis 2016; 10:1159–1164.
16. Colletti RB, Baldassano RN, Milov DE, et al. Pediatric IBD Network for Research and Improvement. Variation in care in pediatric Crohn disease. J Pediatr Gastroenterol Nutr 2009; 49:297–303.
17. Santha SL, Shankar PR, Pan A, et al. Mucosal healing in clinical practice: a single-center pediatric IBD experience. Inflamm Bowel Dis 2017; 23:1447–1453.
18. Weinstein-Nakar I, Focht G, Church P, et al. ImageKids study group. Associations among mucosal and transmural healing and fecal level of calprotectin in children with Crohn's disease. Clin Gastroenterol Hepatol 2018; 16:1089.e4–1097.e4.
19. Falvey JD, Hoskin T, Meijer B, et al. Disease activity assessment in IBD: clinical indices and biomarkers fail to predict endoscopic remission. Inflamm Bowel Dis 2015; 21:824–831.
20. Gupta DM, Boland RJ, Aron DC. The Physician's experience of changing clinical practice: a struggle to unlearn. Implemt Sci 2017; 12:28.
Keywords:

Crohn disease; endoscopy; pediatric inflammatory bowel disease; ulcerative colitis

Copyright © 2021 by European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition