Top

Published in:

Open Access 30-05-2023 | Food Allergy | REVIEW

The role of the atopy patch test in the diagnostic work-up of non-IgE gastrointestinal food allergy in children: a systematic review

Authors: Barbara Cuomo, Caterina Anania, Enza D’Auria, Fabio Decimo, Giovanni Cosimo Indirli, Enrica Manca, Gian Luigi Marseglia, Violetta Mastrorilli, Valentina Panetta, Angelica Santoro, Marco Ugo Andrea Sartorio, Elisabetta Veronelli, Mauro Calvani

Published in: European Journal of Pediatrics | Issue 8/2023

Abstract

The “Atopy Patch Test” (APT) has been proposed as a diagnostic tool for food allergies (FA), especially in children with FA-related gastrointestinal symptoms. However, its diagnostic accuracy is debated, and its usefulness is controversial. The aim of this systematic review was to evaluate the APT diagnostic accuracy compared with the diagnostic gold standard, i.e., the oral food challenge (OFC), in children affected by non-IgE mediated gastrointestinal food allergies, including the evaluation in milk allergic subgroup. Both classical non-IgE mediated clinical pictures and food induced motility disorders (FPIMD) were considered. The search was conducted in PubMed and Scopus from January 2000 to June 2022 by two independent researchers. The patient, intervention, comparators, outcome, and study design approach (PICOS) format was used for developing key questions, to address the APT diagnostic accuracy compared with the oral food challenge (OFC). The quality of the studies was assessed by the QUADAS-2 system. The meta‐analysis was performed to calculate the pooled sensitivity, specificity, DOR (diagnostic odds ratio), PLR (positive likelihood ratio), and NLR (negative likelihood ratio) with their 95% confidence intervals (CI). Out of the 457 citations initially identified via the search (196 on PubMed and 261 on Scopus), 37 advanced to full-text screening, and 16 studies were identified to be included in the systematic review. Reference lists from relevant retrievals were searched, and one additional article was added. Finally, 17 studies were included in the systematic review. The analysis showed that APT has a high specificity of 94% (95%CI: 0.88–0.97) in the group of patients affected by FPIMD. Data showed a high pooled specificity of 96% (95% CI: 0.89–0.98) and the highest accuracy of APT in patients affected by cow’s milk allergy (AUC = 0.93).

Conclusion: APT is effective in identifying causative food in children with food-induced motility disorders.

What is Known:

• Atopy patch test could be a useful diagnostic test for diagnosing food allergy, especially in children with food allergy-related gastrointestinal symptoms.

What is New:

• Atopy patch test may be a useful tool in diagnosing non IgE food allergy, especially in children with food-induced gastrointestinal motility disorders and cow's milk allergy.

Calvani M, Anania C, Cuomo B, D'Auria E, Decimo F, Indirli GC, Marseglia G, Mastrorilli V, Sartorio MUA, Santoro A et al (2021) Non-IgE- or Mixed IgE/Non-IgEMediated gastrointestinal food allergies in the first years of life: old and new tools for diagnosis. Nutrients 13(1):226. https://doi.org/10.3390/nu13010226

Sicherer SH, Sampson HA (2018) Food allergy, a review and update on epidemiology, pathogenesis, diagnosis, prevention, and management. J Allergy Clin Immunol 141:41–58. https://doi.org/10.1016/j.jaci.2017.11.003CrossRefPubMed

Calvani M, Anania C, Bianchi A, D'Auria E, Cardinale F, Votto M, Duse M, Manti S, Tosca MA, Cardinale F, et al (2021) Update on food protein-induced-entero-colitis syndrome (FPIES). Acta Biomed 92: 1–16. https://doi.org/10.23750/abm.v91i11-S.10316

Canani BR, Caffarelli C, Calvani M, Martelli A, Carucci L, Cozzolino T, Alvisi P, Agostoni C, Lionetti P, Marseglia GL (2022) Diagnostic therapeutic care pathway for pediatric food allergies and intolerances in Italy: a joint position paper by the Italian Society for Pediatric Gastroenterology Hepatology and Nutrition (SIGENP) and the Italian Society for Pediatric Allergy and Immunology (SIAIP). Ital J Pediatrics 48:87. https://doi.org/10.1186/s13052-022-01277-8CrossRef

Meyer R, Lozinsky AC, Fleischer DM, Vieira MC, Du Toit G, Vandenplas I, Dupont C, Knibb R, Uysal P, Cavkaytar O et al (2020) Diagnosis and management of Non-IgE gastrointestinal allergies in breastfed infants - an EAACI position paper. Allergy 75(1):14–32. https://doi.org/10.1111/all.13947CrossRefPubMed

Pensabene L, Salvatore S, D’Auria E, Parisi F, Concolino D, Borrelli O,Thapar N, Staiano A, Vandenplas Y, Saps M (2018) Cow’s milk protein allergy in infancy: a risk factor for functional gastrointestinal disorders in children? Nutrients10–1716. https://doi.org/10.3390/nu10111716

Schäppi MG, Borrelli O, Knafelz D, Williams S, Smith VV, Milla PJ, Lindley KJ (2008) Mast cell–nerve interactions in children with functional dyspepsia. J Pediatr Gastroenterol Nutr 47:472–480. https://doi.org/10.1097/MPG.0b013e318186008eCrossRefPubMed

Labrosse R, Graham F, Caubet JC (2020) Non-IgE mediated gastrointestinal food allergies in children: an update. Nutrients 12:2086. https://doi.org/10.3390/nu12072086CrossRefPubMedPubMedCentral

Walter A, Seegräber M (2019) Wollenberg A (2018) Food-related contact dermatitis, contact urticaria, and atopy patch test with food. Nature Clin Rev Allergy Immunol 56(1):19–31. https://doi.org/10.1007/s12016-018-8687-yCrossRef

10.

Wollenberg A, Vogel S (2013) Patch testing for noncontact dermatitis: the atopy patch test for food and inhalants. Curr Allergy Asthma Rep 13(5):539–544. https://doi.org/10.1007/s11882-013-0368-6CrossRef

11.

Muraro A, Werfel T, Hoffmann-Sommergruber K, Roberts G, Beyer K, Bindslev-Jensen C, Cardona V, Dubois A, du Toit G, Eigenmann P et al (2014) EAACI food allergy and ana-phylaxis guidelines: diagnosis and management of food allergy. Allergy 69:1008–1025. https://doi.org/10.1111/all.12429CrossRefPubMed

12.

Nowak-Wegrzyn A, Chehade M, Groetch ME, Spergel JM, Wood RA, Allen K, Atkins D, Bahna S, Barad A, Berin C et al (2017) 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 139:1111–1126. https://doi.org/10.1016/j.jaci.2016.12.966CrossRefPubMed

13.

Devillers AC, de Waard-van der Spek FB, Mulder PG, Oranje AP, (2009) Delayed- and immediate-type reactions in the atopy patch test with food allergens in young children with atopic dermatitis. Pediatr Allergy Immunol 20(1):53–58. https://doi.org/10.1111/j.1399-3038.2008.00760.xCrossRefPubMed

14.

Pustisek N, Jaklin-Kekez A, Frkanec R, Sikanić-Dugić N, Misak Z, Jadresin O, Kolacek S (2010) Our experiences with the use of atopy patch test in the diagnosis of cow’s milk hypersensitivity. Acta DermatoVenerol Croat 18(1):14–20PubMed

15.

Mehl A, Rolinck-Werninghaus C, Staden U, Verstege A, Wahn U, Beyer K, Niggemann B (2006) The atopy patch test in the diagnostic workup of suspected food-related symptoms in children. J Allergy Clin Immunol 118(4):923–929. https://doi.org/10.1016/j.jaci.2006.07.003CrossRefPubMed

16.

Canani RB, Ruotolo S, Auricchio L, Caldore M, Porcaro F, Manguso F, Terrin G, Troncone R (2007) Diagnostic accuracy of the atopy patch test in children with food allergy-related gastrointestinal symptoms. Allergy 62(7):738–743. https://doi.org/10.1111/j.1398-9995.2007.01351.xCrossRefPubMed

17.

Luo Y, Zhang G-Q, Li Z-Y (2019) The diagnostic value of APT for food allergy in children: a systematic review and meta-analysis. Pediatr Allergy Immunol 30:451–461. https://doi.org/10.1111/pai.13031CrossRefPubMed

18.

Gayam S, Zinn Z, Chelliah M, Teng J (2018) Patch testing in gastrointestinal diseases-a systematic review of the patch test and atopypatch test. J Eur Acad Dermatol Venereol 32:e349–e351. https://doi.org/10.1111/jdv.14923CrossRefPubMed

19.

Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. Oct 18;155(8):529–36. https://doi.org/10.7326/0003-4819-155-8-201110180-00009.

20.

Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560. https://doi.org/10.1136/bmj.327.7414.557CrossRefPubMedPubMedCentral

21.

Zapatero RL, Alonso LE, Martín FE, Martínez MMI (2005) Food-protein-induced enterocolitis syndrome caused by fish. Allergol Immunopathol (Madr) 33(6):312–316. https://doi.org/10.1016/s0301-0546(05)73249-3CrossRef

22.

Fogg MI, Brown-Whitehorn TA, Pawlowski NA, Spergel JM (2006) Atopy patch test for the diagnosis of food protein-induced enterocolitis syndrome. Pediatr Allergy Immunol 17:351–355. https://doi.org/10.1111/j.1399-3038.2006.00418.xCrossRefPubMed

23.

Järvinen KM, Caubet JC, Sickles L, Ford LS, Sampson HA, Nowak-WęgrzynA, (2012) Poor utility of atopy patch test in predicting tolerance development in food protein-induced enterocolitis syndrome. Ann Allergy Asthma Immunol 109(3):221–222. https://doi.org/10.1016/j.anai.2012.06.020CrossRefPubMedPubMedCentral

24.

Lucarelli S, Di Nardo G, Lastrucci G, D’Alfonso Y, Marcheggiano A, Federici T, Frediani S, Frediani T, Cucchiara S (2011) Allergic proctocolitis refractory to maternal hypoallergenic diet in exclusively breast-fed infants: a clinical observation. BMC Gastroenterol 16(11):82. https://doi.org/10.1186/1471-230x-11-82CrossRef

25.

Alves FA, Cheik MFA, De Nápolis ACR, Rezende ÉRMDA, Barros CP, Segundo GRS (2015) Poor utility of the atopy patch test in infants with fresh rectal bleeding. Ann Allergy Asthma Immunol 115:161–162. https://doi.org/10.1016/j.anai.2015.06.005CrossRefPubMed

26.

Arshi S, Khoshmirsafa M, Khalife M, Nabavi M, Bemanian MH, Shokri S, Seif F, Yousefi A, Fallahpour M (2021) Atopy patch test in the diagnosis of food allergens in infants with allergic proctocolitis compared with elimination/introduction C. Iran J Allergy Asthma Immunol Sep 28;20(5):520–524. https://doi.org/10.18502/ijaai.v20i5.7402

27.

Sirin Kose S, Asilsoy S, Tezcan D, Atakul G, Al S, Atay O, Kangalli Boyacioglu O, Kangalli Boyacioglu O, Uzuner N, Anal O et al (2020) Atopy patch test in children with cow’s milk and hen’s egg allergy: do clinical symptoms matter? Allergol Immunopathol (Madr) 48:323–331. https://doi.org/10.1016/j.aller.2020.03.002CrossRefPubMed

28.

De Boissieu D, Waguet JC, Dupont C (2003) The atopy patch tests for detection of cow’s milk allergy with digestive symptoms. J Pediatr 142(2):203–205. https://doi.org/10.1067/mpd.2003.92CrossRefPubMed

29.

Nocerino R, Granata V, Di Costanzo M, Pezzella V, Leone L, Passariello A, Troncone TR, Berni Canani R (2013) Atopy patch tests are useful to predict oral tolerance in children with gastrointestinal symptoms related to non-IgE mediated cow’s milk allergy. Allergy 68:246–248. https://doi.org/10.1186/2045-7022-3-S3-P41CrossRefPubMed

30.

Yukselen A, Celtik C (2016) Food allergy in children with refractory gastroesophageal reflux disease. Pediatr Int 58:254–258. https://doi.org/10.1111/ped.12779CrossRefPubMed

31.

Kokkonen J, Ruuska T, Karttunen TJ, Niinimäki A (2001) Mucosal pathology of the foregut associated with food allergy and recurrent abdominal pains in children. Acta Paediatr 90(1):16–21. https://doi.org/10.1080/080352501750064824CrossRefPubMed

32.

Kalach N, Soulaines P, de Boissieu D, Dupont C (2005) A pilot study of the usefulness and safety of a ready-to-use atopy patch test (Diallertest) versus a comparator (Finn Chamber) during cow’s milk allergy in children. J Allergy Clin Immunol 116(6):1321–1326. https://doi.org/10.1016/j.jaci.2005.08.033CrossRefPubMed

33.

Cudowska B, Kaczmarski M (2010) Atopy patch test in the diagnosis of food allergy in children with gastrointestinal symptoms. Adv Med Sci 55(2):153–160. https://doi.org/10.2478/v10039-010-0038-zCrossRefPubMed

34.

Syrigou EI, Pitsios C, Panagiotou I, Chouliaras G, Kitsiou S, Kanariou M, Roma-Giannikou E (2011) Food allergy-related paediatric constipation: the usefulness of atopy patch test. Eur J Pediatr 170(9):1173–1178. https://doi.org/10.1007/s00431-011-1417-6CrossRefPubMed

35.

Mowszet K, Matusiewicz K, Iwańczak B (2014) Value of the atopy patch test in the diagnosis of food allergy in children with gastrointestinal symptoms. Adv Clin Exp Med 23(3):403–9. https://doi.org/10.17219/acem/37136

36.

Boonyaviwat O, Pacharn P, Jirapongsananuruk O, Vichyanond P, Visitsunthorn N (2015) Role of atopy patch test for diagnosis of food allergy- related gastrointestinal symptoms in children. Pediatr Allergy Immunol 26(8):737–741. https://doi.org/10.1111/pai.12382CrossRefPubMed

37.

Ruffner MA, Spergel JM (2016) Non-IgE mediated food allergy syndrome. Ann Allergy Asthma Immunol 117(5):452–454. https://doi.org/10.1016/j.anai.2016.04.014CrossRefPubMedPubMedCentral

38.

Cianferoni A (2020) Non-IgE mediated food allergy. Curr Pediatr Rev 16:95–105. https://doi.org/10.2174/1573396315666191031103714CrossRefPubMed

39.

Nowak-Wegrzyn A, Mehr KY, SS, Koletzko S, (2015) Non-IgE mediated gastrointestinal food allergy. J Allergy Clin Immunol 135:1114–1124. https://doi.org/10.1016/j.jaci.2015.03.025CrossRefPubMed

40.

Isolauri E, Turjanmaa K (1996) Combined skin prick and patch testing enhances identification of food allergy in infants with atopic dermatitis. J Allergy Clin Immunol 97:9–15. https://doi.org/10.1016/S0091-6749(96)70277-4CrossRefPubMed

41.

Roehr C, Reibel S, Ziegert M, Sommerfeld C, Wahn U, Niggemann B (2001) Atopy patch test together with level of specific IgE reduces the need for oral food challenges in children with atopic dermatitis. J Allergy Clin Immunol 107:548–553. https://doi.org/10.1067/MAI.2001.112849CrossRefPubMed

42.

Niggemann B, Reibel S, Wahn U (2000) The atopy patch test (APT) a useful tool for the diagnosis of food allergy in children with atopic dermatitis. Allergy 55:281–285. https://doi.org/10.1034/j.1398-9995.2000.00464.xCrossRefPubMed

43.

Erwin EA, James HR, Gutekunst HM, Russo JM, Kelleher KJ, Platts-Mills TA (2010) Serum IgE measurement and detection of food allergy in pediatric patients with eosinophilic esophagitis. Ann Allergy Asthma Immunol 104(6):496–502. https://doi.org/10.1016/j.anai.2010.03.018

44.

Dalby K, Nielsen RG, Kruse-Andersen S, Fenger C, Bindslev-Jensen C, Ljungberg S, Larsen K, Walsted AM, Husby S (2010) Eosinophilic oesophagitis in infants and children in the region of southern Denmark: a prospective study of prevalence and clinical presentation. Pediatr Gastroenterol Nutr 51(3):280–282. https://doi.org/10.1097/MPG.0b013e3181d1b107CrossRef

45.

Syrigou E, Angelakopoulou A, Zande M, Panagiotou I, Roma E, Pitsios C (2015) Allergy-test-driven elimination diet is useful in children with eosinophilic esophagitis, regardless of the severity of symptoms. Pediatr Allergy Immunol 26(4):323–329. https://doi.org/10.1111/pai.12389CrossRefPubMed

46.

Spergel JM, Brown-Whitehorn TF, Cianferoni A, Shuker M, Wang ML, Verma R, Liacouras CA (2012) Identification of causative foods in children with eosinophilic esophagitis treated with an elimination diet. J Allergy Clin Immunol 130(2):461–7.e5. https://doi.org/10.1016/j.jaci.2012.05.021CrossRefPubMed

47.

Spergel JM, Andrews T, Brown-Whitehorn TF, Beausoleil JL, Liacouras CA (2005) Treatment of eosinophilic esophagitis with specific food elimination diet directed by a combination of skin prick and patch tests. Ann Allergy Asthma Immunol 95(4):336–343. https://doi.org/10.1016/S1081-1206(10)61151-9CrossRefPubMed

48.

Spergel JM, Brown-Whitehorn T, Beausoleil JL, Shuker M, Liacouras CA (2007) Predictive values for skin prick test and atopy patch test for eosinophilic esophagitis. J Allergy Clin Immunol 119(2):509–511. https://doi.org/10.1016/j.jaci.2006.11.016CrossRefPubMed

Title: The role of the atopy patch test in the diagnostic work-up of non-IgE gastrointestinal food allergy in children: a systematic review
Authors: Barbara Cuomo
Caterina Anania
Enza D’Auria
Fabio Decimo
Giovanni Cosimo Indirli
Enrica Manca
Gian Luigi Marseglia
Violetta Mastrorilli
Valentina Panetta
Angelica Santoro
Marco Ugo Andrea Sartorio
Elisabetta Veronelli
Mauro Calvani
Publication date: 30-05-2023
Publisher: Springer Berlin Heidelberg
Keywords: Food Allergy
Motility Disorder
Motility Disorder
Published in: European Journal of Pediatrics / Issue 8/2023
Print ISSN: 0340-6199
Electronic ISSN: 1432-1076
DOI: https://doi.org/10.1007/s00431-023-04994-2

Keynote webinar | Spotlight on medication adherence

Springer Medicine

The role of the atopy patch test in the diagnostic work-up of non-IgE gastrointestinal food allergy in children: a systematic review

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 8/2023

Symptoms for early diagnosis of chronic kidney disease in children — a machine learning–based score

The increase in diaphragm thickness in preterm infants is related to birth weight: a pilot study

High consumption of ultra-processed foods is associated with increased risk of micronutrient inadequacy in children: The SENDO project

Acute kidney injury in infants hospitalized for viral bronchiolitis

The neonatal DAV-expert algorithm: a GAVeCeLT/GAVePed consensus for the choice of the most appropriate venous access in newborns

Validation of an accelerometer system for measuring physical activity and sedentary behavior in healthy children and adolescents