718
Views
3
CrossRef citations to date
0
Altmetric
REVIEW

Perspectives on Non-IgE-Mediated Gastrointestinal Food Allergy in Pediatrics: A Review of Current Evidence and Guidelines

ORCID Icon, ORCID Icon, ORCID Icon &
Pages 279-291 | Received 23 Dec 2022, Accepted 17 Feb 2023, Published online: 14 Mar 2023

References

  • Nomura I, Morita H, Hosokawa S, et al. Four distinct subtypes of non-IgE-mediated gastrointestinal food allergies in neonates and infants, distinguished by their initial symptoms. J Allergy Clin Immunol. 2011;127(3):685–688.e1–8. doi:10.1016/j.jaci.2011.01.019
  • Connors L, O’Keefe A, Rosenfield L, Kim H. Non-IgE-mediated food hypersensitivity. Allergy Asthma Clin Immunol. 2018;14(Suppl 2):56. doi:10.1186/s13223-018-0285-2
  • Sampson HA, Aceves S, Bock SA, et al. Food allergy: a practice parameter update-2014. J Allergy Clin Immunol. 2014;134(5):1016–1025.e43. doi:10.1016/j.jaci.2014.05.013
  • Guidelines for the diagnosis and management of food allergy in the United States: report of the NIAID-sponsored expert panel - PubMed. Available from: https://pubmed.ncbi.nlm.nih.gov/21134576/. Accessed August 30, 2022.
  • Sabra A, Bellanti JA, Rais JM, Castro HJ, Mendez de Inocencio J, Sabra S. IgE and non-IgE food allergy. Ann Allergy Asthma Immunol. 2003;90(6, Supplement):71–76. doi:10.1016/S1081-1206(10)61664-X
  • Morita H, Nomura I, Orihara K, et al. Antigen-specific T-cell responses in patients with non-IgE-mediated gastrointestinal food allergy are predominantly skewed to T(H)2. J Allergy Clin Immunol. 2013;131(2):590–592.e1–6. doi:10.1016/j.jaci.2012.09.005
  • Muraro A, Werfel T, Hoffmann-Sommergruber K, et al. EAACI food allergy and anaphylaxis guidelines: diagnosis and management of food allergy. Allergy. 2014;69(8):1008–1025. doi:10.1111/all.12429
  • Ruffner MA, Spergel JM. Non-IgE-mediated food allergy syndromes. Ann Allergy Asthma Immunol. 2016;117(5):452–454. doi:10.1016/j.anai.2016.04.014
  • Chehade M, Meyer R, Beauregard A. Feeding difficulties in children with non–IgE-mediated food allergic gastrointestinal disorders. Ann Allergy Asthma Immunol. 2019;122(6):603–609. doi:10.1016/j.anai.2019.03.020
  • Squire JD, Stallings AP. Food Protein-Induced Enterocolitis Syndrome (FPIES) is associated with increased risk of feeding disorders. J Allergy Clin Immunol Pract. 2018;141(2):AB132. doi:10.1016/j.jaci.2017.12.422
  • Feuille E, Nowak-Węgrzyn A. Food protein-induced enterocolitis syndrome, allergic proctocolitis, and enteropathy. Curr Allergy Asthma Rep. 2015;15(8):50. doi:10.1007/s11882-015-0546-9
  • Martin VM, Virkud YV, Seay H, et al. Prospective assessment of pediatrician-diagnosed food protein-induced allergic proctocolitis by gross or occult blood. J Allergy Clin Immunol Pract. 2020;8(5):1692–1699.e1. doi:10.1016/j.jaip.2019.12.029
  • Nowak-Wegrzyn A, Berin MC, Mehr S. Food protein-induced enterocolitis syndrome. J Allergy Clin Immunol Pract. 2020;8(1):24–35. doi:10.1016/j.jaip.2019.08.020
  • Mehr S, Frith K, Barnes EH, Campbell DE; FPIES Study Group. Food protein-induced enterocolitis syndrome in Australia: a population-based study, 2012–2014. J Allergy Clin Immunol. 2017;140(5):1323–1330. doi:10.1016/j.jaci.2017.03.027
  • Katz Y, Goldberg MR, Rajuan N, Cohen A, Leshno M. The prevalence and natural course of food protein–induced enterocolitis syndrome to cow’s milk: a large-scale, prospective population-based study. J Allergy Clin Immunol Pract. 2011;127(3):647–653.e3. doi:10.1016/j.jaci.2010.12.1105
  • Alonso SB, Ezquiaga JG, Berzal PT, et al. Food protein–induced enterocolitis syndrome: increased prevalence of this great unknown—results of the PREVALE study. J Allergy Clin Immunol Pract. 2019;143(1):430–433. doi:10.1016/j.jaci.2018.08.045
  • Mehr S, Frith K, Campbell DE. Epidemiology of food protein-induced enterocolitis syndrome. Curr Opin Allergy Clin Immunol. 2014;14(3):208–216. doi:10.1097/ACI.0000000000000056
  • Anvari S, Ruffner MA. adult food protein-induced enterocolitis syndrome. Front Allergy. 2022;3:889879. doi:10.3389/falgy.2022.889879
  • Nowak-Wegrzyn A, Warren CM, Brown-Whitehorn T, Cianferoni A, Schultz-Matney F, Gupta RS. Food protein-induced enterocolitis syndrome in the US population-based study. J Allergy Clin Immunol. 2019;144(4):1128–1130. doi:10.1016/j.jaci.2019.06.032
  • González-Delgado P, Muriel J, Jiménez T, Cameo JI, Palazón-Bru A, Fernández J. Food protein-induced enterocolitis syndrome in adulthood: clinical characteristics, prognosis, and risk factors. J Allergy Clin Immunol Pract. 2022;10(9):2397–2403. doi:10.1016/j.jaip.2022.05.006
  • Savilahti E. Food-Induced Malabsorption Syndromes. J Pediatr Gastroenterol Nutr. 2000;30(1):S61. doi:10.1097/00005176-200001001-00010
  • Schieve LA, Boulet SL, Boyle C, Rasmussen SA, Schendel D. Health of children 3 to 17 years of age with down syndrome in the 1997–2005 national health interview survey. Pediatrics. 2009;123(2):e253–e260. doi:10.1542/peds.2008-1440
  • Wakiguchi H, Hasegawa S, Kaneyasu H, et al. Long-lasting non-IgE-mediated gastrointestinal cow’s milk allergy in infants with Down syndrome. Pediatr Allergy Immunol. 2015;26(8):821–823. doi:10.1111/pai.12351
  • Pecora V, Mennini M, Valentini D, et al. Food protein induced enterocolitis syndrome and down syndrome: an unexpected association? Dig Liver Dis. 2017;49(4):e268. doi:10.1016/j.dld.2017.09.069
  • Verkasalo M, Kuitunen P, Savilahti E, Tiilikainen A. Changing pattern of cow’s milk intolerance. An analysis of the occurrence and clinical course in the 60s and mid-70s. Acta Paediatr. 1981;70(3):289–295. doi:10.1111/j.1651-2227.1981.tb16554.x
  • Odze RD, Bines J, Leichtner AM, Goldman H, Antonioli DA. Allergic proctocolitis in infants: a prospective clinicopathologic biopsy study. Hum Pathol. 1993;24(6):668–674. doi:10.1016/0046-8177(93)90248-f
  • Caubet JC, Szajewska H, Shamir R, Nowak-Węgrzyn A. Non-IgE-mediated gastrointestinal food allergies in children. Pediatr Allergy Immunol. 2017;28(1):6–17. doi:10.1111/pai.12659
  • Nowak-Węgrzyn A, Katz Y, Mehr SS, Koletzko S. Non-IgE-mediated gastrointestinal food allergy. J Allergy Clin Immunol. 2015;135(5):1114–1124. doi:10.1016/j.jaci.2015.03.025
  • Goldman H, Proujansky R. Allergic proctitis and gastroenteritis in children. Clinical and mucosal biopsy features in 53 cases. Am J Surg Pathol. 1986;10(2):75–86. doi:10.1097/00000478-198602000-00001
  • Sicherer SH. Clinical aspects of gastrointestinal food allergy in childhood. Pediatrics. 2003;111(6 Pt 3):1609–1616. doi:10.1542/peds.111.S3.1609
  • Lake AM. Food-induced eosinophilic proctocolitis. J Pediatr Gastroenterol Nutr. 2000;30(Suppl):S58–60. doi:10.1097/00005176-200001001-00009
  • Lake AM, Whitington PF, Hamilton SR. Dietary protein-induced colitis in breast-fed infants. J Pediatr. 1982;101(6):906–910. doi:10.1016/s0022-3476(82)80008-5
  • Arvola T, Ruuska T, Keränen J, Hyöty H, Salminen S, Isolauri E. Rectal bleeding in infancy: clinical, allergological, and microbiological examination. Pediatrics. 2006;117(4):e760–768. doi:10.1542/peds.2005-1069
  • Ravelli A, Villanacci V, Chiappa S, Bolognini S, Manenti S, Fuoti M. Dietary protein-induced proctocolitis in childhood. Am J Gastroenterol. 2008;103(10):2605–2612. doi:10.1111/j.1572-0241.2008.02035.x
  • Agyemang A, Nowak-Wegrzyn A. Food protein-induced enterocolitis syndrome: a comprehensive review. Clin Rev Allergy Immunol. 2019;57(2):261–271. doi:10.1007/s12016-018-8722-z
  • Ruffner MA, Wang KY, Dudley JW, et al. Elevated atopic comorbidity in patients with food protein-induced enterocolitis. J Allergy Clin Immunol Pract. 2020;8(3):1039–1046. doi:10.1016/j.jaip.2019.10.047
  • Schultz F, Westcott-Chavez A. Food protein-induced enterocolitis syndrome from the parent perspective. Curr Opin Allergy Clin Immunol. 2014;14(3):263–267. doi:10.1097/ACI.0000000000000059
  • Boyer J, Sgambelluri L, Yuan Q. Association of antibiotic usage with food protein-induced enterocolitis syndrome development from a Caregiver’s survey. JPGN Rep. 2021;2(4):e132. doi:10.1097/pg9.0000000000000132
  • Nowak-Wegrzyn A, Sampson HA, Wood RA, Sicherer SH. Food protein-induced enterocolitis syndrome caused by solid food proteins. Pediatrics. 2003;111(4 Pt 1):829–835. doi:10.1542/peds.111.4.829
  • Ocak M, Akarsu A, Sahiner UM, Soyer O, Sekerel BE. Phenotypes and natural history of food protein-induced enterocolitis syndrome in the east Mediterranean region. Allergy Asthma Proc. 2020;41(6):420–427. doi:10.2500/aap.2020.41.200078
  • Nowak-Węgrzyn A, Chehade M, Groetch ME, et al. International consensus guidelines for the diagnosis and management of food protein-induced enterocolitis syndrome: executive summary-workgroup report of the adverse reactions to foods committee, American Academy of Allergy, Asthma & Immunology. J Allergy Clin Immunol. 2017;139(4):1111–1126.e4. doi:10.1016/j.jaci.2016.12.966
  • Tan JA, Smith WB. Non-IgE-mediated gastrointestinal food hypersensitivity syndrome in adults. J Allergy Clin Immunol Pract. 2014;2(3):355–357.e1. doi:10.1016/j.jaip.2014.02.002
  • Labrosse R, Graham F, Caubet JC. Non-IgE-mediated gastrointestinal food allergies in children: an update. Nutrients. 2020;12(7):2086. doi:10.3390/nu12072086
  • Iyngkaran N, Robinson MJ, Sumithran E, Lam SK, Puthucheary SD, Yadav M. Cows’ milk protein-sensitive enteropathy. An important factor in prolonging diarrhoea of acute infective enteritis in early infancy. Arch Dis Child. 1978;53(2):150–153. doi:10.1136/adc.53.2.150
  • Foong R-X, Meyer R, Dziubak R, et al. Establishing the prevalence of low vitamin D in non-immunoglobulin-E mediated gastrointestinal food allergic children in a tertiary centre. World Allergy Organ J. 2017;10(1):4. doi:10.1186/s40413-016-0135-y
  • Meyer R, Godwin H, Dziubak R, et al. The impact on quality of life on families of children on an elimination diet for Non-immunoglobulin E mediated gastrointestinal food allergies. World Allergy Organ J. 2017;10(1):8. doi:10.1186/s40413-016-0139-7
  • Murray KF, Christie DL. Dietary protein intolerance in infants with transient methemoglobinemia and diarrhea. J Pediatr. 1993;122(1):90–92. doi:10.1016/s0022-3476(05)83495-x
  • Okura Y, Shimomura M, Takahashi Y, Kobayashi I. Usefulness of thymus and activation-regulated chemokine in solid food protein-induced enterocolitis syndrome. Pediatr Allergy Immunol. 2022;33(1):e13677. doi:10.1111/pai.13677
  • Mathew M, Leeds S, Nowak-Węgrzyn A. Recent update in food protein-induced enterocolitis syndrome: pathophysiology, diagnosis, and management. Allergy Asthma Immunol Res. 2022;14(6):587–603. doi:10.4168/aair.2022.14.6.587
  • Makita E, Sugawara D, Kuroda S, Itabashi K, Ichihashi K. Usefulness of thymus and activation-regulated chemokine (TARC) for FPIES diagnosis. Pediatr Allergy Immunol. 2022;33(1):e13649. doi:10.1111/pai.13649
  • Baudon JJ, Fontaine JL, Mougenot JF, Navarro J, Polonovski C, Laplane R. L'intolerance digestive aux proteines du lait de vache chez le nourrisson. Etude clinique de 42 cas [Digestive intolerance to cow’s milk proteins in infants. Biological and histological study]. Arch Fr Pediatr. 1975;32(9):787–801. French.
  • Cetinkaya PG, Kahveci M, Karaatmaca B, et al. Predictors for late tolerance development in food protein-induced allergic proctocolitis. Allergy Asthma Proc. 2020;41(1):e11–e18. doi:10.2500/aap.2020.41.190017
  • Kimura M, Shimomura M, Morishita H, Meguro T, Seto S. Eosinophilia in infants with food protein-induced enterocolitis syndrome in Japan. Allergol Int. 2017;66(2):310–316. doi:10.1016/j.alit.2016.08.003
  • Beşer OF, Sancak S, Erkan T, Kutlu T, Cokuğraş H, Cokuğraş FÇ. Can fecal calprotectin level be used as a markers of inflammation in the diagnosis and follow-up of cow’s milk protein allergy? Allergy Asthma Immunol Res. 2014;6(1):33–38. doi:10.4168/aair.2014.6.1.33
  • Trillo Belizón C, Ortega Páez E, Medina Claros AF, et al. Calprotectina fecal como apoyo al diagnóstico en la alergia a las proteínas de leche de vaca no IgE mediada [Faecal calprotectin as an aid to the diagnosis of non-IgE mediated cow’s milk protein allergy]. An Pediatr. 2016;84(6):318–323. French. doi:10.1016/j.anpedi.2015.07.007
  • Calvani M, Anania C, Bianchi A, et al. Update on Food protein-induced enterocolitis syndrome (FPIES). Acta Biomed. 2021;92(S7):e2021518. doi:10.23750/abm.v92iS7.12394
  • Variend S, Placzek M, Raafat F, Walker-Smith JA. Small intestinal mucosal fat in childhood enteropathies. J Clin Pathol. 1984;37(4):373–377. doi:10.1136/jcp.37.4.373
  • Iyngkaran N, Abdin Z, Davis K, et al. Acquired carbohydrate intolerance and cow milk protein-sensitive enteropathy in young infants. J Pediatr. 1979;95(3):373–378. doi:10.1016/s0022-3476(79)80509-0
  • Calvani M, Anania C, Cuomo B, et al. Non-IgE- or mixed IgE/Non-IgE-mediated gastrointestinal food allergies in the first years of life: old and new tools for diagnosis. Nutrients. 2021;13(1):226. doi:10.3390/nu13010226
  • Su KW, Patil SU, Stockbridge JL, et al. Food aversion and poor weight gain in food protein-induced enterocolitis syndrome: a retrospective study. J Allergy Clin Immunol. 2020;145(5):1430–1437.e11. doi:10.1016/j.jaci.2020.01.001
  • Ruffner MA, Ruymann K, Barni S, Cianferoni A, Brown-Whitehorn T, Spergel JM. Food protein-induced enterocolitis syndrome: insights from review of a large referral population. J Allergy Clin Immunol Pract. 2013;1(4):343–349. doi:10.1016/j.jaip.2013.05.011
  • Ludman S, Harmon M, Whiting D, du Toit G. Clinical presentation and referral characteristics of food protein-induced enterocolitis syndrome in the United Kingdom. Ann Allergy Asthma Immunol. 2014;113(3):290–294. doi:10.1016/j.anai.2014.06.020
  • Abrams EM, Hildebrand KJ, Chan ES. Non-IgE-mediated food allergy: evaluation and management. Paediatr Child Health. 2021;26(3):173–181. doi:10.1093/pch/pxaa131
  • Miceli Sopo S, Romano A, Bersani G, et al. Cooking influence in tolerance acquisition in egg-induced acute food protein enterocolitis syndrome. Allergol Immunopathol. 2019;47(3):221–226. doi:10.1016/j.aller.2018.07.006
  • Corica D, Aversa T, Caminiti L, Lombardo F, Wasniewska M, Pajno GB. Nutrition and avoidance diets in children with food allergy. Front Pediatr. 2020;8:518. doi:10.3389/fped.2020.00518
  • Caubet JC, Ford LS, Sickles L, et al. Clinical features and resolution of food protein-induced enterocolitis syndrome: 10-year experience. J Allergy Clin Immunol. 2014;134(2):382–389. doi:10.1016/j.jaci.2014.04.008
  • Fiocchi A, Barrio-Torres J, Dupont C, et al. Hydrolyzed rice formula for dietary management of infants with cow’s milk allergy. World Allergy Organ J. 2022;15(12):100717. doi:10.1016/j.waojou.2022.100717
  • Meyer R, Chebar Lozinsky A, Fleischer DM, et al. Diagnosis and management of Non-IgE gastrointestinal allergies in breastfed infants-An EAACI position paper. Allergy. 2020;75(1):14–32. doi:10.1111/all.13947
  • Mennini M, Fiocchi AG, Cafarotti A, et al. Food protein-induced allergic proctocolitis in infants: literature review and proposal of a management protocol. World Allergy Organ J. 2020;13(10):100471. doi:10.1016/j.waojou.2020.100471
  • Nowak-Węgrzyn A. Food protein-induced enterocolitis syndrome and allergic proctocolitis. Allergy Asthma Proc. 2015;36(3):172–184. doi:10.2500/aap.2015.36.3811
  • Miceli Sopo S, Monaco S, Bersani G, Romano A, Fantacci C. Proposal for management of the infant with suspected food protein-induced allergic proctocolitis. Pediatr Allergy Immunol. 2018;29(2):215–218. doi:10.1111/pai.12844
  • Lozinsky AC, Meyer R, De Koker C, et al. Time to symptom improvement using elimination diets in non-IgE-mediated gastrointestinal food allergies. Pediatr Allergy Immunol. 2015;26(5):403–408. doi:10.1111/pai.12404
  • Zubeldia-Varela E, Barker-Tejeda TC, Blanco-Pérez F, Infante S, Zubeldia JM, Pérez-Gordo M. Non-IgE-mediated gastrointestinal food protein-induced allergic disorders. clinical perspectives and analytical approaches. Foods. 2021;10(11):2662. doi:10.3390/foods10112662
  • Meyer R, Groetch M, Venter C. When should infants with cow’s milk protein allergy use an amino acid formula? A practical guide. J Allergy Clin Immunol Pract. 2018;6(2):383–399. doi:10.1016/j.jaip.2017.09.003
  • Leung A, Otley A; Canadian Paediatric Society. Concerns for the use of soy-based formulas in infant nutrition. Paediatr Child Health. 2009;14(2):109–118. doi:10.1093/pch/14.2.109
  • Venter C, Brown T, Shah N, Walsh J, Fox AT. Diagnosis and management of non-IgE-mediated cow’s milk allergy in infancy - a UK primary care practical guide. Clin Transl Allergy. 2013;3(1):23. doi:10.1186/2045-7022-3-23
  • Espín Jaime B, Díaz Martín JJ, Blesa Baviera LC, et al. Alergia a las proteínas de leche de vaca no mediada por IgE: documento de consenso de la Sociedad Española de Gastroenterología, Hepatología y Nutrición Pediátrica (SEGHNP), la Asociación Española de Pediatría de Atención Primaria (AEPAP), la Sociedad Española de Pediatría Extrahospitalaria y Atención Primaria (SEPEAP) y la Sociedad Española de Inmunología Clínica, Alergología y Asma Pediátrica (SEICAP) [Non-IgE-mediated cow’s milk allergy: consensus document of the Spanish Society of Paediatric Gastroenterology, Hepatology, and Nutrition (SEGHNP), the Spanish Association of Paediatric Primary Care (AEPAP), the Spanish Society of Extra-hospital Paediatrics and Primary Health Care (SEPEAP), and the Spanish Society of Paediatric ClinicaL Immunology, Allergy, and Asthma (SEICAP)]. An Pediatr. 2019;90(3):193.e1–193.e11. Spanish. doi:10.1016/j.anpedi.2018.11.007
  • Stróżyk A, Ruszczyński M, Horvath A, et al. World Allergy Organization (WAO) Diagnosis and Rationale for Action against Cow’s Milk Allergy (DRACMA) Guidelines update – IV – a quality appraisal with the AGREE II instrument. World Allergy Organ J. 2022;15:2. doi:10.1016/j.waojou.2021.100613
  • Mehr S, Brown-Whitehorn T. What do allergists in practice need to know about non-IgE-mediated food allergies. Ann Allergy Asthma Immunol. 2019;122(6):589–597. doi:10.1016/j.anai.2019.03.025
  • Michelet M, Schluckebier D, Petit LM, Caubet JC. Food protein-induced enterocolitis syndrome - a review of the literature with focus on clinical management. J Asthma Allergy. 2017;10:197–207. doi:10.2147/JAA.S100379
  • Nowak-Wegrzyn A, Cianferoni A, Bird JA, Fiocchi A, Caubet JC; Medical Advisory Board of the International FPIES Association. Managing food protein-induced enterocolitis syndrome during the coronavirus disease 2019 pandemic: expert recommendations. Ann Allergy Asthma Immunol. 2020;125(1):14–16. doi:10.1016/j.anai.2020.04.032
  • Kaya A, Toyran M, Civelek E, Mısırlıoglu ED, Kırsaçlıoglu CT, Kocabaş CN. Food protein-induced enterocolitis syndrome in two exclusively breastfed infants. Pediatr Allergy Immunol. 2016;27(7):749–750. doi:10.1111/pai.12605
  • Baker RD, Greer FR; Committee on Nutrition American Academy of Pediatrics. Diagnosis and prevention of iron deficiency and iron-deficiency anemia in infants and young children (0–3 years of age). Pediatrics. 2010;126(5):1040–1050. doi:10.1542/peds.2010-2576
  • Staceyrivers. Controversies on special products for managing cow’s milk protein allergy in infants: safety and suitability. EMJ. 2017;2(1):46–51. doi:10.33590/emjallergyimmunol/10313836
  • Sackesen C, Altintas DU, Bingol A, et al. Current trends in tolerance induction in cow’s milk allergy: from passive to proactive strategies. Front Pediatr. 2019;7:372. doi:10.3389/fped.2019.00372
  • Kansu A, Yüce A, Dalgıç B, Şekerel BE, Çullu-çokuğraş F, Çokuğraş H. Consensus statement on diagnosis, treatment and follow-up of cow’s milk protein allergy among infants and children in Turkey. Turk J Pediatr. 2016;58(1):1–11. doi:10.24953/turkjped.2016.01.001
  • Foong RX, Santos AF. Oral tolerance induction-opportunities and mechanisms. Foods. 2022;11(21):3386. doi:10.3390/foods11213386
  • Abrams EM, Hildebrand K, Blair B, Chan ES. Timing of introduction of allergenic solids for infants at high risk. Paediatr Child Health. 2019;24(1):56–57. doi:10.1093/pch/pxy195
  • Nowak-Węgrzyn A, Chatchatee P. Mechanisms of tolerance induction. Ann Nutr Metab. 2017;70(Suppl 2):7–24. doi:10.1159/000457915
  • Sicherer SH, Eigenmann PA, Sampson HA. Clinical features of food protein-induced enterocolitis syndrome. J Pediatr. 1998;133(2):214–219. doi:10.1016/s0022-3476(98)70222-7