3 Nutritional Challenges in Special Conditions and Diseases Koletzko B, et al. (eds): Pediatric Nutrition in Practice. World Rev Nutr Diet. Basel, Karger, 2015, vol 113, pp 239–243 DOI: 10.1159/000360345
3.18 Enteral Nutrition for Paediatric Inflammatory Bowel Disease Marialena Mouzaki Anne Marie Griffiths
Key Messages • Exclusive enteral nutrition (EEN) is an alternative to drug therapy in inducing remission in active Crohn disease • In the treatment of active Crohn disease either elemental or polymeric formulae should be provided as the sole source of nutrition for 6–8 weeks • Supplementary enteral nutrition will facilitate weight gain and linear growth and may help maintain clinical remission • Further research is needed to clarify the mechanisms of action of EEN as primary therapy © 2015 S. Karger AG, Basel
Introduction
Enteral feeding of formulated food can be used to correct or prevent malnutrition in inflammatory bowel disease [1]. Exclusive enteral nutrition (EEN) implies the use of an artificial formula for
the provision of 100% of daily energy as well as macro- and micronutrient requirements in lieu of a regular diet. EEN is an alternative to corticosteroids for active Crohn disease, employed more often in children than adults, and more widely in Europe than in North America [2]. Its efficacy is supported by data from randomized controlled trials versus corticosteroids, and from comparative trials of different formulae [3]. The mechanism of action remains conjectural but may involve alteration in the enteric microflora [4]. Treatment algorithms for Crohn disease are changing. Corticosteroids alleviate symptoms but seldom heal the intestine. In Europe, EEN is endorsed as the primary therapy of new-onset Crohn disease, with thiopurines introduced early for maintenance therapy. Recent guidelines have been put forth to enhance the use of enteral nutrition in the management of paediatric Crohn disease in North America [5]. The support of a multidisciplinary team of nurses and dieticians is essential [5, 6]. This chapter focuses on the use of EEN as the primary therapy of intestinal inflammation and aims to provide a practical guide for its implementation.
3
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
Key Words Enteral nutrition · Inflammatory bowel disease · Growth · Treatment
Evidence of Efficacy Most data concerning the efficacy of EEN in treating active Crohn disease relate to clinical endpoints. Response to EEN has been associated with endoscopic healing in uncontrolled studies. In a recent controlled trial among 35 children treated for active Crohn disease, clinical response was associated with endoscopic improvement in 77% with EEN, but in only 33% with steroids [7]. Patient Selection Roughly 50–60% of Crohn disease patients treated with EEN achieve clinical remission [3]. The response depends on the patient population. Recentonset disease may be more responsive [3], perhaps contributing to the superior response rates reported in small trials conducted exclusively among children and summarized in a meta-analysis of outcomes in paediatric trials [8]. Although controversial, predominantly small intestinal inflammation is considered more likely to respond to EEN, compared with isolated Crohn colitis [6, 9]. This may be a reflection of the fact that Crohn colitis is particularly difficult to control. European and American guidelines advocate in favour of EEN use, irrespective of disease location [5, 10]. EEN is not used to treat ulcerative colitis. Therapeutic Regimens Exclusive versus Supplementary Enteral Nutrition To be successful, EEN should be the sole source of nutrition. Allowance of regular food during treatment of active disease compromises its efficacy [11] and may induce satiety and intolerance of the amounts of prescribed formula. Screening for micronutrient deficiencies (e.g. vitamin D) should guide the need for supplementation. The micronutrient content of the formula, as well as its mucosal healing effects, is also expected to assist in the correction of nutritional imbalances [12].
240
Mode of Administration Liquid diets may be sipped orally or administered via a silastic nasogastric feeding tube (NG tube; size: 6 or 8 Fr). Most children learn to insert the NG tube and administer the formula overnight. The tube is removed each morning to facilitate daytime activities. When use over a period of months is contemplated, an indwelling gastrostomy tube may be inserted. Target Volume and Calories EEN should provide 100% of the patient’s estimated caloric and protein requirements. These are calculated using normal predictive equations (e.g. Schofield, WHO equation, etc.; summarized in the clinical guidelines by the NASPGHAN Committee on Inflammatory Bowel Disease) [5]. In the setting of malnutrition, ideal body weight (the weight for the patient’s age that corresponds to the same percentile on the growth chart as their height percentile) should be used instead of actual weight to prevent underfeeding. An activity factor should be added for the estimation of total energy requirements. Maintenance fluid volumes do not have to be provided exclusively via EEN as consumption of clear fluids is also allowed. When using NG feeding, infusion rates should be increased in a stepwise manner considering tolerance. The duration of infusion is gradually decreased. A sample protocol for the gradual increase to full feeds is given in table 1. Most young patients aim to complete the infusion over 10–14 h. Choice of Formula Polymeric, peptide-based and amino acid-based formulae have all been used to treat active Crohn disease [3]. There is general agreement that the protein content of liquid diets does not influence their efficacy [3]. Dietary lipids, however, can modulate inflammation by a variety of mechanisms which influence cellular production of cytokines and eicosanoids [3, 13]. While the amount and type of fat may modulate inflammatory pathways, the therapeutic success achieved
Mouzaki Griffiths Koletzko B, et al. (eds): Pediatric Nutrition in Practice. World Rev Nutr Diet. Basel, Karger, 2015, vol 113, pp 239–243 DOI: 10.1159/000360345
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
Treatment of Active Crohn Disease
Table 1. Proposed protocol for the initiation of EEN
Initial rate of feeds
Start with half of the target hourly volume and give continuously over 24 h
Increasing feeds
Increase by 10 ml/h every 3 – 6 h, depending on symptoms
Cycling feeds
Decrease the overall feed duration by 2 – 3 h every day; the rate is determined by the total volume to be given over the desired number of hours
Final goal of feeds
The maximum rate is usually 6 – 8 ml/kg/h; the final duration of feeding is 10 – 14 h
Table 2. Sample protocol for reintroduction of solid foods
Examples
1–4
Grains; low fibre
White flour bread, crackers, pasta, rice Hot cereal: cream of wheat Cold cereal (low fat, low fibre)
5–9
Meat, fish and alternatives; low fibre, low fat
Plain (not fried, not processed) lamb, veal, beef, pork, chicken, turkey Fish (low fat) Tofu Eggs
10 – 14
Fruits and vegetables; low fibre, low fat
Raw fruits without skin/seeds Canned fruits without skin/seeds Cooked vegetables without skin/seeds
15 – 17
Dairy; low fat
Milk, yogurt, cheese
18
Regular diet
Slowly increasing fat and fibre content based on tolerance
with a variety of both polymeric (usually highfat) and elemental (usually low-fat) formulae suggests that efficacy does not depend solely on fat content. For those determined to drink the liquid diet, a polymeric formula must be used because of its greater palatability. If the formula is to be administered by NG tube, its palatability becomes unimportant. Given the influence of fat content on efficacy, a conventional elemental liquid diet (low fat content) may offer some therapeutic advan-
3
tage. The treatment benefit of a low-fat compared with a conventional polymeric diet is admittedly small [3]. Duration of EEN The required duration of EEN has not been well defined. Improvements in clinical and laboratory parameters occur quickly, often by 2 weeks, but the optimal time for achievement of mucosal healing has not been established. Most gastroenterologists suggest continuing the therapy for a
Enteral Nutrition for Paediatric Inflammatory Bowel Disease
Koletzko B, et al. (eds): Pediatric Nutrition in Practice. World Rev Nutr Diet. Basel, Karger, 2015, vol 113, pp 239–243 DOI: 10.1159/000360345
241
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
Day of Type of food introduction
minimum of 6 weeks, longer if ideal weight has not been reached yet. Reintroduction of Solid Food Foods are usually reintroduced gradually. It may be prudent, particularly if there are intestinal strictures, to offer a low-fibre diet initially following completion of the enteral nutrition regimen. A sample order of food reintroduction is given in table 2.
Facilitation of Linear Growth
Impairment of linear growth commonly complicates Crohn disease. The major contributing factors are the direct growth-inhibiting effects of proinflammatory cytokines produced by the inflamed intestine and chronic undernutrition [14]. Inappropriate use of chronic corticosteroid therapy will also impede linear growth. Other treatment strategies, which induce mucosal healing, will be associated with reduced cytokine production and will facilitate growth as long as the control of inflammation can be sustained. Resumption of normal linear growth is a marker of therapeutic success. Conversely, if a child merely gains weight but does not grow normally in height, it can be assumed that the inflamed intestine is not healing, and that other anti-inflammatory interventions must be adopted.
Maintenance of Clinical Remission
Symptoms tend to recur following the cessation of enteral nutrition. In most studies, 60–70% of patients experience a symptomatic relapse within 12 months of enteral nutrition [3]. Two nutritional strategies can be considered to maintain remission: firstly, ‘cyclical EEN’, meaning administration of a liquid diet and avoidance of regular food 1 month out of 4, or, secondly, ‘supplementary enteral nutrition’. The latter, which has been employed primarily if nocturnal NG feeding is used, involves continuation of such feeding 4–5 times weekly as supplement to an unrestricted ad libitum daytime diet [15]. In Europe, the most common strategy to maintain clinical remission following EEN is institution of immunomodulatory drugs.
Conclusions
• Exacerbations of Crohn disease, particularly involving the small intestine, may be treated with 4–6 weeks of EEN • Use of palatable polymeric formulae may avoid the need for nocturnal NG infusion • Because relapse is common following cessation of enteral nutrition, strategies to maintain remission must be planned • Sustained, normal linear growth is a marker of success of therapy
References
242
3 Zachos M, Tondeur M, Griffiths AM: Enteral nutritional therapy for induction of remission in Crohn’s disease. Cochrane Database Syst Rev 2007;1:CD000542. 4 Leach ST, Mitchell HM, Eng WR, Zhang L, Day AS: Sustained modulation of intestinal bacteria by exclusive enteral nutrition used to treat children with Crohn’s disease. Aliment Pharmacol Ther 2008;28:724–733.
5 Critch J, Day AS, Otley A, et al: Use of enteral nutrition for the control of intestinal inflammation in pediatric Crohn disease. J Pediatr Gastroenterol Nutr 2012;54:298–305. 6 Buchanan E, Gaunt WW, Cardigan T, et al: The use of exclusive enteral nutrition for induction of remission in children with Crohn’s disease demonstrates that disease phenotype does not influence clinical remission. Aliment Pharmacol Ther 2009;30:501–507.
Mouzaki Griffiths Koletzko B, et al. (eds): Pediatric Nutrition in Practice. World Rev Nutr Diet. Basel, Karger, 2015, vol 113, pp 239–243 DOI: 10.1159/000360345
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
1 Voitk AJ, Echave V, Feller JH, et al: Experience with elemental diet in the treatment of inflammatory bowel disease: is this primary therapy? Arch Surg 1973; 107:329–333. 2 Levine A, Milo T, Buller H, Markowitz J: Consensus and controversy in the management of pediatric Crohn disease: an international survey. J Pediatr Gastroenterol Nutr 2003;36:464–469.
7 Borrelli O, Cordischi L, Cirulli M, et al: Polymeric diet alone versus corticosteroids in the treatment of active pediatric Crohn’s disease: a randomized controlled open-label trial. Clin Gastroenterol Hepatol 2006;4:744–753. 8 Heuschkel RB, Menache CC, Megerian JT, Baird AE: Enteral nutrition and corticosteroids in the treatment of acute Crohn’s disease in children. J Pediatr Gastroenterol Nutr 2000;31:8–15. 9 Afzal NA, Davies S, Paintin M, ArnaudBattandier F, Walker-Smith JA, Murch S, Heuschkel R, Fell J: Colonic Crohn’s disease in children does not respond well to treatment with enteral nutrition if the ileum is not involved. Dig Dis Sci 2005;50:1471–1475.
10 Sandhu BK, Fell JM, Beattie RM, Mitton SG, Wilson DC, Jenkins H; IBD Working Group of the British Society of Paediatric Gastroenterology, Hepatology, and Nutrition: Guidelines for the management of inflammatory bowel disease in children in the United Kingdom. J Pediatr Gastroenterol Nutr 2010;50(suppl 1): S1–S13. 11 Johnson T, Macdonald S, Hill SM, Thomas A, Murphy MS: Treatment of active Crohn’s disease in children using partial enteral nutrition with liquid formula: a randomized controlled trial. Gut 2006;55:356–361. 12 Gerasimidis K, Talwar D, Duncan A, Moyes P, Buchanan E, Hassan K, O’Reilly D, McGrogan P, Edwards CA: Impact of exclusive enteral nutrition on body composition and circulating micronutrients in plasma and erythrocytes of children with active Crohn’s disease. Inflamm Bowel Dis 2012;18:1672–1681.
13 Gassull MA, Fernández-Bañares F, Cabré E, Papo M, Giaffer MH, SánchezLombraña JL, Richart C, Malchow H, González-Huix F, Esteve M: Fat composition may be a clue to explain the primary therapeutic effect of enteral nutrition in Crohn’s disease: results of a double blind randomized multicentre European trial. Gut 2002;51:164–168. 14 Walters T, Griffiths A: Mechanisms of growth impairment in pediatric Crohn’s disease. Nat Rev Gastroenterol Hepatol 2009;6:513–523. 15 Wilschanski M, Sherman P, Pencharz P, Davis L, Corey M, Griffiths A: Supplementary enteral nutrition maintains remission in paediatric Crohn’s disease. Gut 1996;38:543–548.
Enteral Nutrition for Paediatric Inflammatory Bowel Disease
Koletzko B, et al. (eds): Pediatric Nutrition in Practice. World Rev Nutr Diet. Basel, Karger, 2015, vol 113, pp 239–243 DOI: 10.1159/000360345
243
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
3
3.18 Enteral Nutrition for Paediatric Inflammatory Bowel Disease Marialena Mouzaki Anne Marie Griffiths
Key Messages • Exclusive enteral nutrition (EEN) is an alternative to drug therapy in inducing remission in active Crohn disease • In the treatment of active Crohn disease either elemental or polymeric formulae should be provided as the sole source of nutrition for 6–8 weeks • Supplementary enteral nutrition will facilitate weight gain and linear growth and may help maintain clinical remission • Further research is needed to clarify the mechanisms of action of EEN as primary therapy © 2015 S. Karger AG, Basel
Introduction
Enteral feeding of formulated food can be used to correct or prevent malnutrition in inflammatory bowel disease [1]. Exclusive enteral nutrition (EEN) implies the use of an artificial formula for
the provision of 100% of daily energy as well as macro- and micronutrient requirements in lieu of a regular diet. EEN is an alternative to corticosteroids for active Crohn disease, employed more often in children than adults, and more widely in Europe than in North America [2]. Its efficacy is supported by data from randomized controlled trials versus corticosteroids, and from comparative trials of different formulae [3]. The mechanism of action remains conjectural but may involve alteration in the enteric microflora [4]. Treatment algorithms for Crohn disease are changing. Corticosteroids alleviate symptoms but seldom heal the intestine. In Europe, EEN is endorsed as the primary therapy of new-onset Crohn disease, with thiopurines introduced early for maintenance therapy. Recent guidelines have been put forth to enhance the use of enteral nutrition in the management of paediatric Crohn disease in North America [5]. The support of a multidisciplinary team of nurses and dieticians is essential [5, 6]. This chapter focuses on the use of EEN as the primary therapy of intestinal inflammation and aims to provide a practical guide for its implementation.
3
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
Key Words Enteral nutrition · Inflammatory bowel disease · Growth · Treatment
Evidence of Efficacy Most data concerning the efficacy of EEN in treating active Crohn disease relate to clinical endpoints. Response to EEN has been associated with endoscopic healing in uncontrolled studies. In a recent controlled trial among 35 children treated for active Crohn disease, clinical response was associated with endoscopic improvement in 77% with EEN, but in only 33% with steroids [7]. Patient Selection Roughly 50–60% of Crohn disease patients treated with EEN achieve clinical remission [3]. The response depends on the patient population. Recentonset disease may be more responsive [3], perhaps contributing to the superior response rates reported in small trials conducted exclusively among children and summarized in a meta-analysis of outcomes in paediatric trials [8]. Although controversial, predominantly small intestinal inflammation is considered more likely to respond to EEN, compared with isolated Crohn colitis [6, 9]. This may be a reflection of the fact that Crohn colitis is particularly difficult to control. European and American guidelines advocate in favour of EEN use, irrespective of disease location [5, 10]. EEN is not used to treat ulcerative colitis. Therapeutic Regimens Exclusive versus Supplementary Enteral Nutrition To be successful, EEN should be the sole source of nutrition. Allowance of regular food during treatment of active disease compromises its efficacy [11] and may induce satiety and intolerance of the amounts of prescribed formula. Screening for micronutrient deficiencies (e.g. vitamin D) should guide the need for supplementation. The micronutrient content of the formula, as well as its mucosal healing effects, is also expected to assist in the correction of nutritional imbalances [12].
240
Mode of Administration Liquid diets may be sipped orally or administered via a silastic nasogastric feeding tube (NG tube; size: 6 or 8 Fr). Most children learn to insert the NG tube and administer the formula overnight. The tube is removed each morning to facilitate daytime activities. When use over a period of months is contemplated, an indwelling gastrostomy tube may be inserted. Target Volume and Calories EEN should provide 100% of the patient’s estimated caloric and protein requirements. These are calculated using normal predictive equations (e.g. Schofield, WHO equation, etc.; summarized in the clinical guidelines by the NASPGHAN Committee on Inflammatory Bowel Disease) [5]. In the setting of malnutrition, ideal body weight (the weight for the patient’s age that corresponds to the same percentile on the growth chart as their height percentile) should be used instead of actual weight to prevent underfeeding. An activity factor should be added for the estimation of total energy requirements. Maintenance fluid volumes do not have to be provided exclusively via EEN as consumption of clear fluids is also allowed. When using NG feeding, infusion rates should be increased in a stepwise manner considering tolerance. The duration of infusion is gradually decreased. A sample protocol for the gradual increase to full feeds is given in table 1. Most young patients aim to complete the infusion over 10–14 h. Choice of Formula Polymeric, peptide-based and amino acid-based formulae have all been used to treat active Crohn disease [3]. There is general agreement that the protein content of liquid diets does not influence their efficacy [3]. Dietary lipids, however, can modulate inflammation by a variety of mechanisms which influence cellular production of cytokines and eicosanoids [3, 13]. While the amount and type of fat may modulate inflammatory pathways, the therapeutic success achieved
Mouzaki Griffiths Koletzko B, et al. (eds): Pediatric Nutrition in Practice. World Rev Nutr Diet. Basel, Karger, 2015, vol 113, pp 239–243 DOI: 10.1159/000360345
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
Treatment of Active Crohn Disease
Table 1. Proposed protocol for the initiation of EEN
Initial rate of feeds
Start with half of the target hourly volume and give continuously over 24 h
Increasing feeds
Increase by 10 ml/h every 3 – 6 h, depending on symptoms
Cycling feeds
Decrease the overall feed duration by 2 – 3 h every day; the rate is determined by the total volume to be given over the desired number of hours
Final goal of feeds
The maximum rate is usually 6 – 8 ml/kg/h; the final duration of feeding is 10 – 14 h
Table 2. Sample protocol for reintroduction of solid foods
Examples
1–4
Grains; low fibre
White flour bread, crackers, pasta, rice Hot cereal: cream of wheat Cold cereal (low fat, low fibre)
5–9
Meat, fish and alternatives; low fibre, low fat
Plain (not fried, not processed) lamb, veal, beef, pork, chicken, turkey Fish (low fat) Tofu Eggs
10 – 14
Fruits and vegetables; low fibre, low fat
Raw fruits without skin/seeds Canned fruits without skin/seeds Cooked vegetables without skin/seeds
15 – 17
Dairy; low fat
Milk, yogurt, cheese
18
Regular diet
Slowly increasing fat and fibre content based on tolerance
with a variety of both polymeric (usually highfat) and elemental (usually low-fat) formulae suggests that efficacy does not depend solely on fat content. For those determined to drink the liquid diet, a polymeric formula must be used because of its greater palatability. If the formula is to be administered by NG tube, its palatability becomes unimportant. Given the influence of fat content on efficacy, a conventional elemental liquid diet (low fat content) may offer some therapeutic advan-
3
tage. The treatment benefit of a low-fat compared with a conventional polymeric diet is admittedly small [3]. Duration of EEN The required duration of EEN has not been well defined. Improvements in clinical and laboratory parameters occur quickly, often by 2 weeks, but the optimal time for achievement of mucosal healing has not been established. Most gastroenterologists suggest continuing the therapy for a
Enteral Nutrition for Paediatric Inflammatory Bowel Disease
Koletzko B, et al. (eds): Pediatric Nutrition in Practice. World Rev Nutr Diet. Basel, Karger, 2015, vol 113, pp 239–243 DOI: 10.1159/000360345
241
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
Day of Type of food introduction
minimum of 6 weeks, longer if ideal weight has not been reached yet. Reintroduction of Solid Food Foods are usually reintroduced gradually. It may be prudent, particularly if there are intestinal strictures, to offer a low-fibre diet initially following completion of the enteral nutrition regimen. A sample order of food reintroduction is given in table 2.
Facilitation of Linear Growth
Impairment of linear growth commonly complicates Crohn disease. The major contributing factors are the direct growth-inhibiting effects of proinflammatory cytokines produced by the inflamed intestine and chronic undernutrition [14]. Inappropriate use of chronic corticosteroid therapy will also impede linear growth. Other treatment strategies, which induce mucosal healing, will be associated with reduced cytokine production and will facilitate growth as long as the control of inflammation can be sustained. Resumption of normal linear growth is a marker of therapeutic success. Conversely, if a child merely gains weight but does not grow normally in height, it can be assumed that the inflamed intestine is not healing, and that other anti-inflammatory interventions must be adopted.
Maintenance of Clinical Remission
Symptoms tend to recur following the cessation of enteral nutrition. In most studies, 60–70% of patients experience a symptomatic relapse within 12 months of enteral nutrition [3]. Two nutritional strategies can be considered to maintain remission: firstly, ‘cyclical EEN’, meaning administration of a liquid diet and avoidance of regular food 1 month out of 4, or, secondly, ‘supplementary enteral nutrition’. The latter, which has been employed primarily if nocturnal NG feeding is used, involves continuation of such feeding 4–5 times weekly as supplement to an unrestricted ad libitum daytime diet [15]. In Europe, the most common strategy to maintain clinical remission following EEN is institution of immunomodulatory drugs.
Conclusions
• Exacerbations of Crohn disease, particularly involving the small intestine, may be treated with 4–6 weeks of EEN • Use of palatable polymeric formulae may avoid the need for nocturnal NG infusion • Because relapse is common following cessation of enteral nutrition, strategies to maintain remission must be planned • Sustained, normal linear growth is a marker of success of therapy
References
242
3 Zachos M, Tondeur M, Griffiths AM: Enteral nutritional therapy for induction of remission in Crohn’s disease. Cochrane Database Syst Rev 2007;1:CD000542. 4 Leach ST, Mitchell HM, Eng WR, Zhang L, Day AS: Sustained modulation of intestinal bacteria by exclusive enteral nutrition used to treat children with Crohn’s disease. Aliment Pharmacol Ther 2008;28:724–733.
5 Critch J, Day AS, Otley A, et al: Use of enteral nutrition for the control of intestinal inflammation in pediatric Crohn disease. J Pediatr Gastroenterol Nutr 2012;54:298–305. 6 Buchanan E, Gaunt WW, Cardigan T, et al: The use of exclusive enteral nutrition for induction of remission in children with Crohn’s disease demonstrates that disease phenotype does not influence clinical remission. Aliment Pharmacol Ther 2009;30:501–507.
Mouzaki Griffiths Koletzko B, et al. (eds): Pediatric Nutrition in Practice. World Rev Nutr Diet. Basel, Karger, 2015, vol 113, pp 239–243 DOI: 10.1159/000360345
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
1 Voitk AJ, Echave V, Feller JH, et al: Experience with elemental diet in the treatment of inflammatory bowel disease: is this primary therapy? Arch Surg 1973; 107:329–333. 2 Levine A, Milo T, Buller H, Markowitz J: Consensus and controversy in the management of pediatric Crohn disease: an international survey. J Pediatr Gastroenterol Nutr 2003;36:464–469.
7 Borrelli O, Cordischi L, Cirulli M, et al: Polymeric diet alone versus corticosteroids in the treatment of active pediatric Crohn’s disease: a randomized controlled open-label trial. Clin Gastroenterol Hepatol 2006;4:744–753. 8 Heuschkel RB, Menache CC, Megerian JT, Baird AE: Enteral nutrition and corticosteroids in the treatment of acute Crohn’s disease in children. J Pediatr Gastroenterol Nutr 2000;31:8–15. 9 Afzal NA, Davies S, Paintin M, ArnaudBattandier F, Walker-Smith JA, Murch S, Heuschkel R, Fell J: Colonic Crohn’s disease in children does not respond well to treatment with enteral nutrition if the ileum is not involved. Dig Dis Sci 2005;50:1471–1475.
10 Sandhu BK, Fell JM, Beattie RM, Mitton SG, Wilson DC, Jenkins H; IBD Working Group of the British Society of Paediatric Gastroenterology, Hepatology, and Nutrition: Guidelines for the management of inflammatory bowel disease in children in the United Kingdom. J Pediatr Gastroenterol Nutr 2010;50(suppl 1): S1–S13. 11 Johnson T, Macdonald S, Hill SM, Thomas A, Murphy MS: Treatment of active Crohn’s disease in children using partial enteral nutrition with liquid formula: a randomized controlled trial. Gut 2006;55:356–361. 12 Gerasimidis K, Talwar D, Duncan A, Moyes P, Buchanan E, Hassan K, O’Reilly D, McGrogan P, Edwards CA: Impact of exclusive enteral nutrition on body composition and circulating micronutrients in plasma and erythrocytes of children with active Crohn’s disease. Inflamm Bowel Dis 2012;18:1672–1681.
13 Gassull MA, Fernández-Bañares F, Cabré E, Papo M, Giaffer MH, SánchezLombraña JL, Richart C, Malchow H, González-Huix F, Esteve M: Fat composition may be a clue to explain the primary therapeutic effect of enteral nutrition in Crohn’s disease: results of a double blind randomized multicentre European trial. Gut 2002;51:164–168. 14 Walters T, Griffiths A: Mechanisms of growth impairment in pediatric Crohn’s disease. Nat Rev Gastroenterol Hepatol 2009;6:513–523. 15 Wilschanski M, Sherman P, Pencharz P, Davis L, Corey M, Griffiths A: Supplementary enteral nutrition maintains remission in paediatric Crohn’s disease. Gut 1996;38:543–548.
Enteral Nutrition for Paediatric Inflammatory Bowel Disease
Koletzko B, et al. (eds): Pediatric Nutrition in Practice. World Rev Nutr Diet. Basel, Karger, 2015, vol 113, pp 239–243 DOI: 10.1159/000360345
243
Downloaded by: UCONN Storrs 137.99.31.134 - 5/21/2015 3:20:09 PM
3
