Update on Food protein-induced enterocolitis syndrome (FPIES)

Mauro  Calvani; Caterina  Anania; Annamaria  Bianchi; Enza  D'Auria; Fabio  Cardinale; Martina  Votto; Alberto Martelli; Mariangela  Tosca; Elena  Chiappini; Ilaria  Brambilla; Michele  Miraglia Del Giudice; Carlo Caffarelli

doi:10.23750/abm.v92iS7.12394

Update on Food protein-induced enterocolitis syndrome (FPIES)

Authors

Mauro Calvani UOC di Pediatria. Azienda Ospedaliera S. Camillo Forlanini, Rome, Italy
Caterina Anania Dipartimento Materno Infantile e Scienze Urologiche, Policlinico Umberto I, “La Sapienza” University, Rome, Italy
Annamaria Bianchi UOC di Pediatria. Azienda Ospedaliera S. Camillo Forlanini, Rome, Italy
Enza D'Auria Clinica Pediatrica, Ospedale dei Bambini Vittore Buzzi, University of Milan, Milan, Italy
Fabio Cardinale Department of Pediatrics, Giovanni XXIII Pediatric Hospital, University of Bari, Bari, Italy
Martina Votto Pediatric Clinic, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy; Pediatric Unit, Department of Clinical, Surgical, Diagnostic, and Pediatric Sciences, University of Pavia, Pavia, Italy
Alberto Martelli University of Pavia, Pavia, Italy
Mariangela Tosca Allergy Centre, IRCCS G. Gaslini Pediatric Hospital, Genova, Italy
Elena Chiappini Department of Pediatric Infectious Disease, Anna Meyer Children’s Hospital, Firenze, Italy
Ilaria Brambilla Pediatric Clinic, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy; Pediatric Unit, Department of Clinical, Surgical, Diagnostic, and Pediatric Sciences, University of Pavia, Pavia, Italy
Michele Miraglia Del Giudice Department of Woman, Child and of General and Specialized Surgery, University of Campania ‘Luigi Vanvitelli’, Naples, Italy
Carlo Caffarelli Pediatric Clinic, Department of Medicine and Surgery, Unversity of Parma, Parma, Italy

DOI: https://doi.org/10.23750/abm.v92iS7.12394

Keywords:

food protein-induced enterocolitis syndrome, FPIES, non-IgE mediated food allergy, diagnosis

Abstract

Food protein-induced enterocolitis syndrome (FPIES) is a non-IgE mediated food allergy (FA) characterized by delayed and severe gastrointestinal symptoms that typically occurs within the first year of life. Many aspects of this pathology are currently unclear. FPIES is classified as a non-IgE immune-mediated FA in which the immune response is thought to act mainly through cell-mediated mechanisms. In patients with FPIES, the symptom pattern is determined by the frequency and dose of food allergen in the diet. Diagnosis of FPIES may be difficult, mainly due to the lack of specific biomarkers to confirm or exclude the diagnosis. FPIES is a clinical diagnosis, mainly based on clinical features which, although not specific, are reproducible every time the patient takes the food. Different diagnostic criteria of FPIES were published over time in the literature. The present narrative review aims to analyze the current clinical evidence in epidemiology, pathophysiology, diagnosis, and management of this condition.

References

Nowak-Wegrzyn 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;139:1111-26.

Katz Y, Goldbert MR, Rajuan N, Cohen A, Leshno M. The prevalence and natural course of protein-induced enterocolitis syndrome to cow’s milk: a large scale, prospective population-based study. J Allergy Clin Immunol 2011;127:647-53.

Alonso SB, Ezquiaga JG, Berzal PT, et al. Food protein induced enterocolitis syndrome: increased prevalence of this great unknown-results of PREVALE study. J Allergy Clin Immunol 2019,143:430-433.

Mehr S, Frith K, Barnes EH, Campbell DE. Food protein induced enterocolitis syndrome in Australia: a population based study. J Allergy Clin Immunol 2017;140:1323-30.

Sopo SM, Giorgio V, Dello Iacono I, et al. A multicentre retrospective study of 66 Italian children with food protein-induced enterocolitis syndrome: different management for different phenotypes. Clin Exp Allergy 2012,42:1257-65.

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;113:290-94.

Xepapadaki P, Kitsioulis NA, Manousakis E, et al. Remissione patterns of food protein- induced enterocolitis syndrome in a Greek pediatric population. Int Arch Allergy Immunol 2019;180:113-19.

Nowak-Wegrzyn A, Warren CM, Brown-Whitehon T, et al. Food protein-induced enterocolitis syndrome in the US population-based study. J Allergy Clin Immunol 2019;144:1128-30.

Ruffner MA, Wang KY, Dudley JW, et al. Elevated atopic comorbidity in patients with food protein- induced enterocolitis. J Allergy Clin Immunol Pract 2020;8:1039-46.

Nowak-Wegrzyn A, Katz Y, Mehr SS, Koletzko S. Non-IgE-mediated gastrointestinal food allergy. J Allergy Clin Immunol 2015,135:1114-24.

Agyemang A, Nowak-Wegrzyn A. Food protein-induced enterocolitis syndrome: a comprehensive review. Clinic Rev Allerg Immunol 2019;57:261-71.

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;134:382-89.

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;1:343-49.

Barni S, Sarti L, Liccioli G, et al. Oral food challenge protocol for food protein-induced enterocolitis syndrome: time for a change? J Allergy Clin Immunol Pract 2020,8.2842-43.

Diaz JJ, Espin B, Segarra O, Dominguez-Ortega G, Blasco-Alonso J, Cano B, et al. Food Protein-Induced Enterocolitis Syndrome: data from multicenter retrospective study in Spain. JPGN 2019;68:232-36.

Cianferoni A. Food Protein Induced Enterocolitis (FPIES) epidemilogy. Ann Allergy Asthma Immunol 2021;126:469-77.

Hwang JB, Sohn SM, Kim AS. Prospective follow-up oral food challenge in food protein- induced enterocolitis syndrome. Arch Dis Child 2009;94:425-28.

Leonard SA, Pecora V, Fiocchi AG, Nowak-Wegrzyn A. Food protein-induced enterocolitis syndrome: a review of the new guidelines. World Allergy Organ J 2018;11:4

Blackman AC, Anvari S, Davis CM, Anagnostou A. Emerging triggers of food protein-induced enterocolitis syndrome: lesson from a pediatric cohort of 74 children in the United States. Ann Allergy Asthma Immunol 2019;122:407-11.

Hoffman KM, Ho DG, Sampson HA. Evaluation of the usefulness of lymphocyte proliferation assays in the diagnosis of cow's milk allergy. J Allergy Clin Immunol 1997;99:360-66.

Van Sickle GJ, Powell GK, McDonald PJ, Goldblum RM. Milk- and soy protein-induced enterocolitis: evidence for lymphocyte sensitization to specific food proteins. Gastroenterology 1985;88:1915-21.

Mori F, Barni S, Cianferoni A, Pucci N, de Martino M, Novembre E. Cytokine expression in CD3+ cells in an infant with food protein-induced enterocolitis syndrome (FPIES): case report. Clin Dev Immunol 2009;2009:679381.

Petrosino MI, Scaparrotta A, Di Filippo P, et al. Food protein-induced enterocolitis syndrome in children: what’s known? What’s new? Eur Ann Allergy Clin Immunol 2018;50:99-107.

Caubet JC, Bencharitiwong R, Ross A, Sampson HA, Berin MC, Nowak-Wegrzyn A. Humoral and cellular responses to casein in patients with food protein-induced enterocolitis to cow’s milk. J Allergy Clin Immunol 2016;139:572–83

Goswami R, Blazquez AB, Roman K, Rahman A, Nowak-Wegrzyn A, Berin C. Systemic innate immune activation in food protein–induced enterocolitis syndrome. J Allergy Clin Immunol 2017;139:188596.

Chung HL, Hwang JB, Park JJ, Kim SG. Expression of transforming growth factor beta1, transforming growth factor type I and II receptors, and TNF-alpha in the mucosa of the small intestine in infants with food protein-induced enterocolitis syndrome. J Allergy Clin Immunol 2002;109:150–54.

Konstantinou GN, Bencharitingwong R, Grishing A, et al. The role of casein-specific IgA and TGF-β in children with Food Protein-Induced Enterocolitis Syndrome to milk. Pediatr Allergy Immunol 2014;25:651-56.

Adel-Patient K, Lezmi G, Castelli FA, et al. Deep analysis of immune response and metabolic signature in children with food protein induced enterocolitis to cow’s milk. Clin Transl Allergy 2018;8:38.

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;13:226.

Miceli Sopo S, Monaco S, Cerchiara G, Bersani G. A very unusual case of food allergy, between FPIES and IgE-mediated food allergy. Eur Ann Allergy Clin Immunol 2017;49:42–44.

Onesimo R, Dello Iacono I, Giorgio V, Limongelli MG, Miceli Sopo S. Can food protein induced enterocolitis syndrome shift to immediate gastrointestinal hypersensitivity? A report of two cases. Eur Ann Allergy Clin Immunol 2011;43:61-63.

Nowak-Wegrzyn A, Sampson HA, Wood RA, Sicherer SH. Food protein-induced enterocolitis syndrome caused by solid food proteins. Pediatrics 2003;111:829-35.

Kemp AS, Hill DJ, Allen KJ, et al. Guidelines for the use of infant formulas to treat cows-milk protein allergy: an Australian consensus panel opinion. Med J Aust 2008;188:109–12.

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;127:685-88.

Nowak-Wegrzyn A, Jarocka-Cyrta E, Moschione Castro APB. Food protein-induced enterocolitis syndrome. J Investig Allergol Clin Immunol 2017;27:1-18.

Manti S, Leonardi S, Salpietro A, Del Campo G, Salpietro C, Cuppari C. A systematic review of food protein-induced enterocolitis syndrome from the last 40 years. Ann Allergy Asthma Immunol 2017;118:411-18.

Gonzales-Delgado P, Caparros E, Moreno MV, et al. Clinical and immunological characteristics of a pediatric population with food protein-induced enterocolitis syndrome (FPIES) to fish. Pediatr Allergy Immunol 2016;27:269-75.

Vila L, Garcia V, Rial MJ, Novoa E, Cacharron T. Fish is a major trigger of solid food protein-induced enterocolitis syndrome in Spanish children. J Allergy Clin Immunol Pract 2015;3:621-23.

Miceli Sopo S, Monaco S, Badina L, et al. Food protein-induced enterocolitis syndrome caused by fish and/or shellfish in Italy. Pediatr Allergy Immunol 2015;26:731-36.

Mehr SS, Kakakios AM, Kemp AS. Rice: a common and severe cause of food protein- induced enterocolitis syndrome. Arch Dis Child 2009;94:220-23.

Hsu P, Mehr S. Egg: a frequent trigger of food protein-induced enterocolitis syndrome. J Allergy Clin Immunol 2013;131:241-42.

Diaz JJ, Espin B, Segarra O, et al. Food protein-induced enterocolitis syndrome: data from a multicenter retrospective study in Spain. J Pediatr Gastroenterol Nutr 2019;68:232-36.

Zapatero Remon L, Alonso Lebrero E, Martin Fernandez E, Martinez Molero MI. Food protein-induced enterocolitis syndrome caused by fish. Allergol Immunopathol (Madr) 2005;33:312-16.

Ruiz-Garcia M, Diez CE, Garcia SS, del Rio PR, Ibanez MD. Diagnosis and natural history of food protein-induced enterocolitis syndrome in children from a tertiary hospital in central Spain. J Investig Allergol Clin Immunol 2014;24:354-56.

Gonzales-Delgado P, Caparros E, Moreno MV, et al. Clinical and immunological characteristics of a pediatric population with food protein-induced enterocolitis syndrome (FPIES) to fish. Pediatr Allergy Immunol 2016;27:269-75.

Karefylaki S, Gustafsson D. Recovery from food protein-induced enterocolitis syndrome caused by fish. Pediatr Allergy Immunol 2016;27:105-06.

Sicherer SH, Eigenmann PA, Sampson HA. Clinical features of food protein-induced enterocolitis syndrome. J Pediatr 1998;133:214-19.

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 TH-2. J Allergy Clin Immunol 2013;131:590-92.

Powell GK. Food protein-induced enterocolitis of infancy: differential diagnosis and management. Compr Ther 1986;12:28-37.

Leonard SA, Nowak-Węgrzyn A. Clinical diagnosis and management of food protein-induced enterocolitis syndrome. Curr Opin Pediatr 2012;24:739-45.

Miceli Sopo S, Greco M, Monaco S, Tripodi S, Calvani M. Food protein-induced enterocolitis syndrome, from practice to theory. Expert Rev Clin Immunol 2013;9:707-15.

Leonard SA, Nowak-Węgrzyn A. Food Protein-Induced Enterocolitis Syndrome. Pediatr Clin North Am 2015;62:1463-77.

Lee E, Campbell DE, Barnes EH, Mehr SS. Resolution of acute food protein-induced enterocolitis syndrome in children. J Allergy Clin Immunol Pract 2017;5:486-88.

Vazquez-Ortiz M, Argiz L, Machinena A, et al. Diagnostic criteria for acute FPIES: what are we missing? J Allergy Clin Immunol Pract 2020;8:1717-20.

Miceli Sopo S, Gelsomino M, Rivetti S, Del Vescovo E. Food Protein-Induced Enterocolitis Syndrome: proposals for new definitions. Medicina (Kaunas) 2019;55:216.

Banzato C, Piacentini G, Comberiati P, et al. Unusual shift from IgE-mediated milk allergy to food protein-induced enterocolitis syndrome. Eur Ann Allergy Clin Immunol 2013;45:209-11.

Nowak-Wegrzyn A, Assa’ad AH, Bahna SL, Bock SA, Sicherer SH, Teuber SS. Work group report: oral food challenge testing. J Allergy Clin Immunol 2009;123:S365-83.

Fogg MI, Brown-Whitehorn TA, Pawlowski NA, Spergel JM. Atopy patch test for the diagnosis of food protein-induced enterocolitis syndrome. Pediatr Allergy Immunol 2006:17:351–55.

Jarvinen KM, Caubet JC, Sickles L, Ford LS, Sampson HA, Nowak‐Wegrzyn A. Poor utility of atopy patch test in predicting tolerance development in food protein‐induced enterocolitis syndrome. Ann Allergy Asthma Immunol. 2012;109:221‐22.

Mehr S, Kakakios A, Frith K, Kemp AS. Food protein-induced enterocolitis syndrome: 16- year experience. Pediatrics 2009;123:459-64.

Kimura M, Shimomura M, Morishita H, Meguro T, Seto S. Eosinophilia in infants with food protein‐induced enterocolitis syndrome in Japan. Allergol Int 2017;66:310‐16.

Powell G. Milk- and soy-induced enterocolitis of infancy. Clinical features and standardization of challenge. J Pediatr 1978;93:553–60.

Pecora V, Prencipe G, Valluzzi R, et al. Inflammatory events during food protein-induced enterocolitis syndrome reactions. Pediatr Allergy Immunol 2017;28:464–70.

Murray KF, Christie DL. Dietary protein intolerance in infants with transient methemoglobinemia and diarrhea. J Pediatr 1993;122:90‐92.

Malin SW, Lutfi R, Friedman ML, Teagarden AM. Food protein‐induced enterocolitis syndrome causing hypovolemic shock and methemoglobinemia. Case Rep Crit Care 2018;2018:1903787.

Hwang J-B, Park MH, Kang YN, Kim SP, Suh S-I, Kam S. Advanced criteria for clinicopathological diagnosis of food protein-induced proctocolitis. J Korean Med Sci 2007;22:213–17.

Hwang JB. Is this symptom even a food allergy?: clinical types of food protein-induced enterocolitis syndrome. Pediatr Gastroenterol Hepatol Nutr 2014;17:74-79.

Genere L, Pecciarini N, Peretti N, Villard F, Lachaux A. Food protein-induced enterocolitis syndrome: a case report of diarrhea with hypovolemic shock and. Arch Pediatr 2017;24:28-32.

Mizuno M, Masaki H, Yoshinare R, et al. Hematochezia before the First Feeding in a Newborn with Food Protein-Induced Enterocolitis Syndrome. AJP Rep 2011;1:53–57.

Khan S. Testing for fecal calprotectin in food protein‐induced enterocolitis syndrome. J Investig Allergol Clin Immunol 2018;28:287‐88.

Barni S, Vazquez-Ortiz M, Giovannini M, et al. Diagnosing food protein-induced enterocolitis syndrome. Clin Exp Allergy 2021;51:14-28.

Bird JA, Barni S, Brown-Whitehorn TF, du Toit G, Infante S, Nowak-Wegrzyn A. Food protein-induced enterocolitis syndrome oral food challenge: time for a change? Ann Allergy Asthma Immunol 2021:126:506-15.

Sicherer SH. Food protein-induced enterocolitis syndrome: case presentations and management lessons. J Allergy Clin Immunol 2005;115:149-56.

Hwang JB, Song JY, Kang YN, et al. The significance of gastric juice analysis for a positive challenge by a standard oral challenge test in typical cow’s milk protein-induced enterocolitis. J Korean Med Sci 2008;23:251-55.

Vazquez-Ortiz M, Machinena A, Dominguez O, et al. Food protein-induced enterocolitis syndrome to fish and egg usually resolves by age 5 years in Spanish children. J Allergy Clin Immunol Pract 2017;5:512-15.

Barni S, Sarti L, Mori F, Liotti L, Pucci N, Novembre E. A modified oral food challenge in children with food protein induced enterocolitis syndrome. Clin Exp Allergy 2019;49:1633-36.

Infante S, Marco-Martín G, Zubeldia JM, et al. Oral food challenge in food protein-induced enterocolitis syndrome by fish: is there any room for improvement? Int Arch Allergy Immunol 2019;179:215–20.

Wang KY, Lee J, Cianferoni A, et al. Food protein–induced enterocolitis syndrome food challenges: experience from a large referral center. J Allergy Clin Immunol Pract 2019;7:444–50.

Guenther MW, Crain M, Parrish CP, Bird JA. An observed serving dose may not be necessary following a standard divided-dose FPIES oral food challenge. J Allergy Clin Immunol Pract 2020;8:1462-64.

Monti G, Castagno E, Liguori SA, et al. Food protein-induced enterocolitis syndrome by cow’s milk protein passed through breast milk. J Allergy Clin Immunol 2011;127:679-80.

Tan j, Campbell D, Mehr S. Food protein-induced enterocolitis syndrome in an exclusive breast-fed infant- an uncommon entity. J Allergy Clin Immunol 2012;129:873.

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;75:14-32.

Koletzko S, Niggemann B, Arato A, et al. Diagnostic approach and management of cow’s-milk protein allergy in infants and children: ESPGHAN GI Committee practical guidelines. J Pediatr Gastroenterol Nutr 2012;55:221–29.

Miceli Sopo S, Buonsenso D, Monaco S, Crocco S, Longo G, Calvani M. Food protein-induced enterocolitis syndrome (FPIES) and well-cooked foods: a working hypothesis. Allergol Immunopathol 2013;41:346-48.

Nowak-Wegrzyn A, Bloom KA, Sicherer SH, et al. Tolerance to extensively heated milk in children with cow’s milk allergy. J Allergy Clin Immunol 2008;122:342-47.

Caffarelli C, Di Mauro D, Mastrorilli C, Bottau P, Cipriani F, Ricci G. Solid food introduction and the development of food allergies. Nutrients 2018;10:1790.

Jarvinen K, Nowak-Wegrzyn A. Food protein-induced enterocolitis syndrome: current management strategies. J Allergy Clin Immunol Pract 2013;1:317.

Grimshaw KE, Allen K, Edwards CA, et al. Infant feeding and allergy prevention: a review of current knowledge and recommendations. A EuroPrevall state of the art paper. Allergy 2009;64:1407-16.