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Original Article: Gastroenterology: Inflammatory Bowel Disease

Global Variation in Use of Enteral Nutrition for Pediatric Crohn Disease

Lawley, Morgan; Wu, Jessica W.∗,†; Navas-López, Victor M.; Huynh, Hien Q.; Carroll, Matthew W.; Chen, Min∗,†; Medvedev, Pavel; Day, Andrew S.§; Hussey, Séamus||; Sigall-Boneh, Rotem; Levine, Arie; Wine, Eytan∗,#

Author Information
Journal of Pediatric Gastroenterology and Nutrition: August 2018 - Volume 67 - Issue 2 - p e22-e29
doi: 10.1097/MPG.0000000000001946


What Is Known

  • Exclusive enteral nutrition is an effective treatment for pediatric Crohn disease but is challenging to complete.
  • A detailed description of how exclusive enteral nutrition is used could identify gaps and opportunities to optimize use of exclusive enteral nutrition.

What Is New

  • There is considerable variation in use of exclusive enteral nutrition across the world and between practitioners including duration, patient selection, allowing intake of other foods, and available resources.
  • Major barriers to use of exclusive enteral nutrition remain, including poor adherence and lack of support.
  • Sharing specific approaches to exclusive enteral nutrition can remove barriers and offer opportunities to optimize and improve use of exclusive enteral nutrition.

Around the world, there is a concerning increase in prevalence and incidence of inflammatory bowel diseases (IBD), especially in the pediatric population (1–4). Patients with Crohn disease (CD) have reported a decreased quality of life with major impacts on pediatric patients, including impaired growth and psychological effects (5).

Enteral nutrition (EN), typically provided exclusively (EEN), involves replacing a patient's normal diet with a liquid-based formula for several weeks and has been successfully used for both induction of remission and maintenance therapy in pediatric CD (6,7). EEN induces remission in up to 85% of patients, improves nutritional rehabilitation, and promotes mucosal healing (6–10). Furthermore, EEN is as effective as corticosteroids (or more) in mild-moderate pediatric CD, without the risk of side effects associated with steroids (11–14). EEN has been shown to be superior to partial enteral nutrition (PEN) in induction of remission, emphasizing the importance of exclusivity (15,16).

There are major differences, however, in the frequency of EEN use in different regions and variation across practice methods (17). Much of this variation relates to the difficulties in completing this therapy, given the monotonous nature of the diet and restriction in eating solid food. Practitioners have found practical ways to alleviate these challenges, but the literature is lacking in evidence-based advice on how to best manage an EEN program (18). The aim of this survey was to identify variation in practice and share experience in administering EEN, to promote further research, and contribute to progress towards optimization of therapy, especially through sharing tips and tools of support.



A survey was constructed through consultation with experts in the field, as there was no validated questionnaire available (complete survey: Table S1, in the Supplemental Digital Content, SDC, The survey remained open for 4 months and was disseminated by personal invitation to the Paediatric IBD Porto Group of ESPGHAN, the Canadian Children's IBD Network, and selective experts in the field; it was also sent twice to members of the Pediatric Gastrointestinal-Bulletin Board (PEDGI-BB); only pediatric practitioners were approached. Responders were encouraged to involve others in their group, including dietitians and nurses. Study data were collected and managed using REDCap (19) electronic data capture tools hosted and supported by the Women and Children's Health Research Institute at the University of Alberta between April and July 2016.

Survey Analysis

Data were exported from REDCap to Microsoft Excel and analysis of responses was completed using basic descriptive statistics. Only surveys more than 80% complete were included in the analyses. An overall assessment was followed by sub-group analyses, where responses were characterized by participant country and profession (IBD-focused pediatric gastroenterologist [PGE-IBD]; general pediatric gastroenterologist [PGE-all]; pediatric gastroenterology dietitian [PGD]; other), as self-defined by participants. Parameters included patient features (preferred age, disease location, and timing); EEN use (duration, formula type, route, concentration, exclusivity, allowed “cheats”); EEN program (team members, patient education and support, barriers, protocols, financial coverage); transition off and maintenance of EN.


Participant Characteristics

Of the 199 surveys initiated, only 146 participants from 26 different countries completed more than 80% of the survey and were included in the analysis. Eighty-nine participants were from Europe (including UK and Israel), 41 from North America, and 16 from elsewhere. For the purposes of sub-group analyses, responses were divided into 5 geographical regions (Table 1). Due to the large number of participants from 2 countries, Spain and the UK, and differences in health-care system structure, these 2 countries were analyzed separately, whereas “Europe-Other” (E-O) indicated continental Europe and Israel, with the exclusion of Spain. Regions with low representation were not included in subanalyses.

Breakdown of responses by region

Sixty-five percent of participants were general, non-IBD-focused pediatric gastroenterologists, 21% were IBD-focused, and 10% were dietitians, which formed the categories of sub-group analyses by profession (Table 2). Interestingly, non-IBD-focused and IBD-focused gastroenterologists saw a similar number of IBD patients per week (7.97 ± 7.7 vs 8 ± 8.2). Center size and years of experience treating IBD did not indicate differences in practice methods and are, therefore, not shown.

Breakdown of responses by profession

Exclusive Enteral Nutrition Indications

Participants indicated that they would use EEN as first-line treatment most commonly for ileocolonic CD (Paris L3) (20) and distal small bowel CD+/− limited cecal disease (L1; 91% and 88%, respectively). Fifty-two percent indicated EEN use for isolated colonic disease (L2). Its use was low (<31%) if the patient presented with significant perianal disease, and there was minimal use for select cases of ulcerative colitis (6%). European countries had much higher rates of EEN use for L2 than North American countries (UK 73%, Spain 65%, E-O 61% vs Canada 33%, USA 26%; Table S2, Most (82%) indicated EEN use beyond initial diagnosis; 44% used EN at initial diagnosis and occasionally when changing other therapies during a flare and 38% used EN at initial diagnosis and with every flare (if responded in the past). Fifteen percentage used EEN only at initial diagnosis (Fig. S1,; no regional effect). Details on age of use of EEN are included in the SDC, and Fig. S2,

Choice, Quantity, and Concentration of Enteral Nutrition Formulas

Polymeric formulas were the dominant category (88%) of formula choice. A concentration of 1 kcal/mL was often recommended (63%), followed by 1.5 kcal/mL (30%; Fig. S3, The majority of respondents in Canada (52%) used 1.5 kcal/mL, whereas most in other countries used 1 kcal/mL (UK 55%, US 58%, Spain 60%, and E-O 78%). Most gastroenterologists (61% PGE-all, 71% PGE-IBD) used 1 kcal/ml formula, whereas dietitians were split 50% of 50% between 1 kcal/ml and 1.5 kcal/mL. Data on caloric targets and choice of formula are included in the SDC,

Forty percentage of respondents allow their patients to try a few options and let them choose the formula; 38% consider switching formula if the patient is not managing; and 18% always use the same formula with no flexibility. Dietitians had more flexibility in formula use with 57% always letting their patients try a few formulas, and none always used the same formula. Twenty-two percentage and 19% of PGE-all and PGE-IBD, respectively, always use the same formula with no flexibility.

Duration, Route, and Exclusivity of Enteral Nutrition Administration

Eight weeks were the most common duration for EEN therapy (57%), followed by 6 weeks (31%; Fig. 1). A majority of respondents from Canada, US, and Spain treated for 8 weeks (53%, 63%, and 85%, respectively). UK and E-O favoured a shorter duration, with 73% and 57% treating for 6 weeks, respectively. Oral administration was the preferable route, with 66% always starting oral, switching to nasogastric (NG) only if not tolerated. Nine percent always start NG and switch to oral only if the patient is unwilling/unable, and 24% present both options for the patient/family to decide.

Recommended exclusive enteral nutrition duration: overall (A), by region (B), and by profession (C). EEN = exclusive enteral nutrition, E-O = Europe-Other (excludes UK and Spain), Peds GE = pediatric gastroenterologist.

Most (63%) did not allow any other intake other than water. Spain (88%) and E-O (86%), as well as UK (55%), were more likely to be completely exclusive with EEN and not allow any other intake besides water. US (74%) and Canada (57%) were more likely to allow other intake (referred to as “cheats”). Dietitians generally allowed cheats more frequently, allowing other intake in addition to water 71% of the time, whereas gastroenterologists were more “exclusive,” with 31% PGE-all and 26% PGE-IBD allowing any intake other than water (Fig. 2). The most common allowed cheats were candy and chewing gum only (16%) and clear fluids only (12%). From written text responses to the survey, fluids, candy, and gum were again most commonly allowed, and in some cases, items such as flavoring or an occasional piece of bread/toast were allowed (see a detailed list of allowed cheats and “tips” in Table S3,

Exclusive enteral nutrition exclusivity and allowable “cheats.” (A) Proportion of participants allowing intake other than formula and water (“cheats”). (B) Of those who allowed cheats, percentage of calories from EN. (C) Percent allowed cheats by region. (D) Percent allowed cheats by profession. E List and frequencies of common allowable cheats. EEN = exclusive enteral nutrition, EN = enteral nutrition, E-O = Europe-Other (excludes UK and Spain), Peds GE = pediatric gastroenterologist.

Exclusive Enteral Nutrition Program Features: Members, Protocols, and Patient Education

The majority (62%) of respondents did not provide a handout for patient education and support, although 43% indicated that they practice as a group in a uniform way. Participants from US indicated more independence around EEN teaching protocols, with 53% of respondents “doing their own thing” (vs Spain 25%, Canada 9%, E-O 8%, UK 0%; Table S4,; see examples of approaches from 5 centers in Table S5, Most programs (73%) had support from a dietitian, often with an important role, as EEN teaching was done by the dietitian 49% of the time. Fifty percent of programs also had support from nursing staff (Fig. 3A). Remarkably, EEN programs in Spain were a “one person show” (with no dietitian or nursing support) 70% of the time. Other regions almost always had a dietitian supporting the program (Canada and UK 100%, US 95%, E-O 92%, Spain 18%). In 39% of cases, EEN teaching was done by the gastroenterologist. Spain's more individualized practice was also reflected in the results for EEN education, where 95% of teaching was done by the gastroenterologist. Outside of Spain, the majority of EEN teaching was done by dietitians (54% in E-O, 66% in Canada, 73% in UK, and 74% in US; Fig. 3B).

Support, teaching resources, and barriers in EEN programs. (A) Support staff available for EEN programs by region. (B) Clinicians responsible for teaching EEN by region. (C) Major barriers to EEN by region. EEN = exclusive enteral nutrition, E-O = Europe-Other (excludes UK and Spain). Chi-square analysis: Significant difference in proportions between groups ( P < 0.05; ∗∗∗ P < 0.001).

Running an Exclusive Enteral Nutrition Program: Availability and Barriers

The majority (86%) of patients had access to support after starting therapy. Thirty-one percentage had a designated contact email address or phone number, 21% called the clinic and whoever was available tried to assist, for 19% there was a dedicated person usually available on the phone (“hotline”), and for 16% there was a dedicated person who was usually available in person. For 10%, it was dealt with on a case-by-case basis.

The largest barrier (58%) reported was poor adherence because of monotony (taste fatigue; Fig. 3C) followed by poor adherence because of palatability (42%). The majority of respondents in every region except the UK reported poor adherence because of monotony, whereas 55% in the UK reported no barriers. Most (81%) were satisfied with the way their EN program is running.

Additional results are detailed in the SDC,; further comments and tips are in Table S8,


EEN is an effective tool in the management of pediatric CD, but it can be a challenging therapy to adhere to. Although some detail on running EEN programs are available, there is wide variation in the use of EEN, including indication, age, route, duration, formula choice, exclusivity, and patient support with little evidence on how to best succeed. The rationale for this survey and manuscript was to fill this void and provide a detailed account on how EEN programs are administered across the globe. Given that, as detailed here, there are substantial barriers to EEN, sharing the “tricks and tips” we have each developed will provide essential resources and ideas, identify research and collaboration opportunities, and also afford resources for advocacy and improve patient care.

Several guidelines for the management of pediatric CD recommend EEN as an induction therapy (9,21,22). A consensus questionnaire in Japan found that many physicians (82%) recommended EEN for newly diagnosed children (23). The results of the present study show that clinicians across the world are using EEN for treatment of pediatric CD and for diverse indications. The Consensus guidelines of ECCO/ESPGHAN support the use of EEN for luminal disease, regardless of the location of disease (9). However, the use of EEN treatment often varies with location of the disease, with a high proportion using EEN for Paris L1 and L3 (20). A previous study by Stewart et al (24) found similar results in use of EEN in North America. Our comparison of regions found differences between the North American countries and the European countries. Although most results were similar, the European countries had much higher rates of EEN use for colonic disease than Canada and US.

A study from the Netherlands found that nonadherent children were significantly older than adherent ones (15.5 vs 13.4 years, P = 0.04) (25). Our finding of a decrease in EEN use in the older pediatric population (>17) could be in part because of an anticipated non-adherence in these patients, especially as it is at this age that patients are becoming more independent, although this was not directly addressed in the present study. It is also possible, however, that patients at this age are being treated more similarly to adults or by adult practitioners, where use of EEN has not been shown to have the same efficacy as in pediatrics, possibly because of nonadherence to treatment (26,27).

Most of the respondents to our survey reported using polymeric formulas, likely given that studies have not found any advantage to elemental formulas (6,9,21). Polymeric formulas have been suggested to be more palatable, as well as generally less expensive, which may explain the higher use reported (6,22). Differing from our results, Ishige et al (23) reported higher use of elemental formulas by Japanese physicians. For formula concentration, most reported using 1 kcal/mL, however, the majority in Canada indicated using 1.5 kcal/mL. Use of a higher concentration formula may improve tolerance by reducing formula volume, at the expense of a denser formula.

Candy, gum, and clear fluids were the most commonly reported “cheats” in our study, both in the structured and free response sections. By region, Spain and E-O were much more likely to be truly exclusive with EEN and not allow any other intake (besides water). Practitioners from Canada and US were more likely to allow other intake. This may reflect differing perceptions regarding the mechanism of response, exclusion of food versus consumption of formula. It is interesting to note that this is not necessarily supported by the most recent evidence, which suggests that excluding table food rather than the amount of formula consumed may be more crucial for the microbiological and inflammatory effects (15,28), as well as use of specific diets, such as the CD exclusion diet (CDED) (29). By profession, dietitians differed from gastroenterologists and were much more likely to allow other intake. This may be a result of dietitians having to deal with patients’ difficulties in maintaining the liquid diet or with differences in perception as to how dietary therapy works.

Most regions indicated a high amount of support from dietitians, as well as nurses, whereas respondents from Spain indicated no support. For regions other than Spain, this is similar to results of a 2010 study of physician attitudes and practices of EEN in North America, which found that 74% of physicians reported involvement of a dietitian in administration of EEN, and a nurse by 65% (24). In comparison, the present results for Canada and US (Canada 100%, US 95% support from dietitian; Canada 95%, US 63% support from nurse) suggest a positive shift towards more support for EEN programs, although the small numbers from the US may be misleading. The previous study also found that education was more likely to be in the inpatient setting, (24) whereas this study found that overall, as well as in Canada and US, the out-patient setting was favoured. We hope that our global findings will assist regions with less support for EEN programs to advocate for their patients and align their practice with other regions, especially as dietetic contacts have been associated with higher remission rates (30).

The largest barriers reported in our survey were poor adherence because of monotony and palatability, especially in the US and E-O (Fig. 3C). These results were similar to a previous study describing attitudes of EEN in North America that found compliance issues to be the main disadvantage to EEN and the main barrier to increased use of EEN (24). We found that dietitians have more flexibility in regard to use of different formulas, and speculate this may be a result of dietitians spending more time with the patients managing diet and possibly having a different experience with the patient than the physician. If we want to reduce barriers, improve adherence, and hopefully increase success of treatment, it may be necessary to improve the palatability of the formulas and create more variety. Review of comments from our survey found palatability and variety to be dominant themes for what responders would most like to see improve in EEN care. A few comments indicated that the improvement they would mostly like to see would be a diet including solid foods (such as CDED, eg) (29). If this could be accomplished, and even a handful of foods were allowed, with evidence on their ability to aid in reaching remission, it could have a significant impact on improving the quality of life of patients requiring EEN therapy. Regionally, another major barrier in US and Canada was cost to patients. This is likely a result of EEN not being covered by the public health care system or by commercial health insurance or only being covered when given by NG, whereas the majority from European countries are covered by the public health care.


Most responses were from Westernized/developed countries and, therefore, do not give a good idea of variation in practices of developing countries or countries with varifying cultures. Furthermore, the distribution of the survey is expected to have primarily reached physicians who would be more likely to use EEN or those who completed the survey were more likely to use EEN. This almost certainly introduces a selection bias to our results and limits the ability to generalize findings from our survey to all settings. Responses from dietitians were low in number and may create some bias in that comparison. Another limitation is that the findings are based on personal responses and not actual data, so responses are likely to be driven by more motivated practitioners. Although our study identifies key variations in EEN care, interpretation of findings should be done with caution.

Take Home Message and Future Directions

The primary aim of this study was to identify variation in the practice methods of EEN use in the management of pediatric CD. We have identified varying perceptions regarding therapy. The majority of centers using EEN (with the exception of Spain) had access to dietitians, who were often responsible for patient education, follow-up, and support. Complementary educational materials appear to be used by a minority of centers, suggesting that there is much that can still be done to improve patient education and support. A comment provided that has the potential to reduce barriers to treatment is the development of a motivational app. A future survey could gauge patient interest in an idea such as this.

EEN is an excellent management therapy for pediatric CD that avoids the negative side effects of steroids. We have demonstrated high variation in implementation despite the presence of guidelines (9). This variation offers opportunities to compare practice and optimize outcomes of this challenging treatment, especially in relation to the identified barriers (Table S5, Future research providing evidence on mechanism(s) of action and development of evidence-based guidelines on treatment methods are required to optimize this therapy and further increase its use over steroids.


We would like to thank all the practitioners who contributed their experience and comments to this survey and appreciate the efforts put into their work. Special thanks to the Women and Children's Health Research Institute (WCHRI) at the University of Alberta for allowing us to use the REDCap platform for this project.


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Crohn disease; exclusive enteral nutrition; survey; variation in care

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