Anaphylactic Reactions to Novel Foods: Case Report of a Child With Severe Crocodile Meat Allergy - American Academy of Pediatrics

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Anaphylactic Reactions to Novel Foods: Case Report of a Child With Severe Crocodile Meat Allergy - American Academy of Pediatrics
Anaphylactic Reactions to Novel
                           Foods: Case Report of a Child With
                           Severe Crocodile Meat Allergy
                           Natalia Ballardini, MD, PhD,a,b,c Anna Nopp, PhD,d Carl Hamsten, MSc, PhD,d Mirja Vetander, MD, PhD,a,b,e
                           Erik Melén, MD, PhD,a,b Caroline Nilsson, MD, PhD,b,f Markus Ollert, MD, PhD,g,h Carsten Flohr, MD, PhD,i
                           Annette Kuehn, MD, PhD,g Marianne van Hage, MD, PhDd

Availability of “exotic” foods is steadily increasing. In this report, we                               abstract
describe the first case of anaphylaxis to crocodile meat. The patient was
a 13-year-old boy with severe immunoglobulin E–mediated allergy to
chicken meat. When tasting crocodile meat for the first time, he developed
an anaphylactic reaction. Cross-reactivity between chicken and crocodile
meat was suspected to have triggered this reaction. Basophil activation and
immunoglobulin E testing confirmed the boy’s allergic reaction to crocodile
                                                                                                        aInstitute of Environmental Medicine, eCentre for
meat proteins. Molecular analysis identified a crocodile α-parvalbumin,                                 Allergy Research, and fDepartment of Clinical Science
with extensive sequence homology to chicken α-parvalbumin, as the                                       and Education, Södersjukhuset, Karolinska Institutet,
                                                                                                        Stockholm, Sweden; dClinical Immunology and Allergy Unit,
main cross-reactive allergen. We conclude that crocodile meat can be a
                                                                                                        Department of Medicine Solna, Karolinska Institutet, and
potent food allergen and patients with allergy to chicken meat should be                                Karolinska University Hospital, Stockholm, Sweden bSachs’
advised to avoid intake of meat from crocodile species. Both foods and                                  Children and Youth Hospital, Södersjukhuset, Stockholm,
                                                                                                        Sweden; cSt John’s Institute of Dermatology, King’s College
people travel around the world and accessibility to exotic foods is steadily                            London, London, United Kingdom; gDepartment of Infection
growing. As a result, novel allergic cross-reactivities are likely to become a                          and Immunity, Luxembourg Institute of Health, Esch-sur-
                                                                                                        Alzette, Luxembourg; hDepartment of Dermatology and
challenge in the management of food allergy and, as our report illustrates,                             Allergy Center, Odense Research Center for Anaphylaxis,
cross-reactivity has to be considered even between foods that might not                                 University of Southern Denmark, Odense, Denmark; and
                                                                                                        iSt John’s Institute of Dermatology, Guy’s and St Thomas’
intuitively be perceived as related.                                                                    Hospital NHS Foundation Trust and King’s College London,
                                                                                                        London, United Kingdom

                                                                                                        Dr Ballardini conceptualized and designed the
                                                                                                        study, was responsible for care of the patient, and
                                                                                                        drafted the first manuscript; Dr van Hage designed
Food allergy is an increasing                       PRESENTATION                                        the study and was responsible for the initial
problem in the pediatric population                                                                     immunoglobulin E (IgE) analyses, immunoblots,
                                                                                                        and cross-inhibition experiments, and critically
and is estimated to affect 8% of                    A 13-year-old boy presented to the
                                                                                                        reviewed and revised the manuscript; Drs Kuehn
children with a high negative                       pediatric emergency department                      and Ollert planned and carried out the molecular
impact on quality of life.1–3 Allergy               at Sachs’ Children and Youth                        experiments, subsequent IgE analysis, immunoblots,
to chicken meat has been reported                   Hospital in Stockholm, Sweden,                      and cross-inhibition tests, and critically reviewed
both in children and adults and is                  due to an anaphylactic reaction                     and revised the manuscript; Dr Nopp conceptualized
                                                                                                        and designed the study, performed basophil
estimated to be rare, but reliable                  to crocodile meat. He had been a
                                                                                                        allergen threshold sensitivity analysis, and reviewed
prevalence data are missing.4–8                     regular outpatient at the hospital’s                and revised the manuscript; Dr Hamsten carried
Cross reactivity between chicken                    pediatric allergy department since 5                out the initial IgE analyses, immunoblots, and cross-
and duck, turkey, and goose has                     years of age when he was diagnosed                  inhibition experiments and critically reviewed and
been described.4 Little is known                    with chicken meat allergy (specific                 revised the manuscript; Dr Vetander performed
                                                                                                        the literature review and reviewed and revised the
about the causative allergens for                   immunoglobulin E [IgE], 19 kUA/L).
                                                                                                        manuscript; Dr Nilsson participated in patient care
chicken meat allergy. There are                     He was otherwise healthy and ate
no reports of allergic reactions to                 all foods except poultry. At 7 years
crocodile meat. Although crocodiles                 of age, an adrenaline autoinjector                    To cite: Ballardini N, Nopp A, Hamsten C, et al.
belong to the reptile group, they                   was prescribed after an anaphylactic                  Anaphylactic Reactions to Novel Foods: Case
                                                                                                          Report of a Child With Severe Crocodile Meat
are also the closest living relatives               reaction due to accidental
                                                                                                          Allergy. Pediatrics. 2017;139(4):e20161404
of birds.9                                          consumption of turkey. Although strict

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PEDIATRICS Volume 139, number 4, April 2017:e20161404                                                                                        CASE REPORT
avoidance of chicken and turkey meat        for content of DNA and protein from              crocodile extract at a concentration
was recommended, he continued to            chicken and turkey. In addition, the             of 1 mg inhibitor/mL for immunoblot
experience anaphylactic reactions           crocodile filet was used to prepare a            and 200 μg inhibitor/mL for ELISA.
due to accidental consumption of            protein extract.11 Briefly, the muscle           Parvalbumins were detected by using
foods contaminated by chicken or            tissue was grinded in liquid nitrogen            an antiparvalbumin IgG antibody mix
turkey. As a consequence, he was            followed by extraction in lysis buffer           (Swant, Marly, Switzerland; Abcam,
reluctant to eat foods outside of           (50 mM Tris-HCl, pH 8, 150 mM                    Cambridge, MA).
his home, which had a significant           NaCl, and 1% Triton X-100). Extract
impact on his social life. More             supernatants were dialyzed against               Biomolecular Allergen
recently, his father, a professional        phosphate-buffered saline (pH 7.2)               Characterization
chef, bought and prepared crocodile         before basophil activation assay and             Chicken and crocodile parvalbumins
meat to create a novel meal for his         specific IgE–binding analysis. For               were isolated by ion exchange and
son. The boy reacted at first bite          the basophil activation assay and                gel filtration chromatography as
with itch in the mouth and throat,          measurements of allergen-specific                previously reported.7,14 Protein
facial urticaria, conjunctivitis,           IgE, muscle tissue was homogenized               purity of chicken and crocodile
angioedema, chest tightness, and            followed by extraction in phosphate-             parvalbumins was confirmed by
breathing difficulties. Intramuscular       buffered saline (pH 7.4).                        silver-stained, two-dimensional
adrenaline and β-2 agonist inhalation                                                        SDS-PAGE.11 Crocodile parvalbumin
was administered at home by the             Measurement of Allergen-Specific                  isoforms were additionally separated
parents. At the pediatric emergency         IgE                                              by isoelectric focusing (Offgel,
department, he presented with               IgE antibodies against chicken                   Agilent, Diegem, Belgium) before
facial urticaria, angioedema around         (f83), turkey (f284), and crocodile              an intact mass measurement by
the eyes, bilateral redness of the          meat proteins (5 μg of biotinylated              mass spectrometry (MS) analysis.
sclera, and heavy breathing but no          crocodile extract coupled to                     Parvalbumins were trypsinized for
bronchoconstriction. After 4 hours of       Streptavidin ImmunoCAP) and total                MS peptide mass fingerprint analysis,11
observation, he was free of symptoms        IgE were measured by ImmunoCAP                   which revealed the complete
and discharged.                             (Phadia AB/Thermo Fisher Scientific,             sequence of 1 crocodile parvalbumin
                                            Uppsala, Sweden).                                isoform. Unidentified peptides of
Reviewing the literature, we found
                                                                                             the other isoform were sequenced
no reports of allergic reactions            Basophil Activation Assay                        de novo on a second MALDI TOF/
to crocodile. We had previously
                                            Basophil allergen threshold                      TOF instrument (AB Sciex 5800,
identified α-parvalbumin as a
                                            sensitivity (CD-sens) was performed              Framingham, MA), identifying 92%
relevant chicken meat allergen7 and
                                            as previously described.12,13 Briefly,           of the protein sequence. Protein
because another report showed that
                                            cells were stimulated with increasing            structures were calculated using
parvalbumin is expressed in the tail
                                            concentrations of crocodile or                   Modeller 9v2 software,15,16 and
muscle of Alligator mississippiensis,10
                                            chicken extracts (0.5–500 ng                     chicken parvalbumin (P43305; 2KYF)
we hypothesized that the reaction
                                            protein/mL) or negative controls                 was used to establish the surface
to crocodile was due to IgE cross-
                                            (peanut, birch, casein) and then                 model.
reactivity between α-parvalbumins in
chicken and crocodile meat.                 analyzed by flow cytometry.

                                            Allergen Analysis by IgE Immunoblot              RESULTS
                                            and Enzyme-Linked Immunosorbent                  No contamination of the crocodile
METHODS                                     Assay                                            meat by chicken or turkey residues
Written informed consent was                Chicken and crocodile meat                       was demonstrated. The boy’s
obtained from the patient and his           extracts were separated by                       serum immunoglobulin E (sIgE)
parents.                                    SDS-PAGE (sodium dodecyl                         levels were 40 kUA/L to chicken,
                                            sulfate polyacrylamide gel                       14 kUA/L to turkey, and 6 kUA/L
Allergen Preparation
                                            electrophoresis).11 Patient serum                to crocodile meat extract, whereas
Crocodile filet was purchased               was diluted 5× in 3% bovine                      total serum-IgE was 190 kU/L.
from the same store that sold the           serum albumin (Sigma-Alderich,                   CD-sens was clearly positive to both
crocodile meat that caused the              Bornem, Belgium) for immunoblot                  crocodile and chicken meat extracts
allergic reaction. It was analyzed          and 5–10× for IgE enzyme-linked                  (Fig 1A). In immunoblot analysis,
by the certified laboratory of the          immunosorbent assay (ELISA).11 For               the patient’s IgE bound to chicken
Swedish National Food Agency                IgE cross-inhibition, patient serum              (14 kDa, 19/22 kDa, 30 kDa) and
(Livsmedelsverket; Uppsala, Sweden)         was preincubated with chicken or                 crocodile meat proteins (18–50 kDa)

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e2                                                                                                                     BALLARDINI et al
(Fig 1B). IgE-binding to chicken                                                                        phylogenetic relationship. In another
allergens was not inhibited by                                                                          recent publication, we reported on
preincubation with crocodile extract,                                                                   36 patients (including 17 children
whereas IgE-binding was inhibited
ABBREVIATIONS
                                                          CD-sens: basophil allergen
                                                                    threshold sensitivity
                                                          ELISA: enzyme-linked immuno-
                                                                  sorbent assay
                                                          IgE: immunoglobulin E
                                                          MS: mass spectrometry
                                                          sIgE: serum immunoglobulin E

FIGURE 2
Comparison of chicken and crocodile α-parvalbumin. A, Three-dimensional model of chicken parvalbumin, protein surface coloring by identity to crocodile
parvalbumin. Red, identical residues; gray, variable residues. B, Amino acid sequence alignment of chicken and crocodile parvalbumins as allergens
involved in the clinical cross-reaction to both meats.

Agency (Uppsala, Sweden) for                           and turkey DNA by real time PCR.                        We also thank Dr K. Arumugam
analysis of crocodile meat for (1)                     We thank D. Revets (Luxembourg                          (Luxembourg Institute of Health) for
detection of poultry protein by use                    Institute of Health) for excellent                      establishing the structural model of
of ELISA and (2) detection of chicken                  technical support with MS analysis.                     chicken and crocodile parvalbumin.

and reviewed and revised the manuscript; Drs Melén and Flohr provided intellectual input and reviewed and revised the manuscript; and all authors approved
the final manuscript as submitted.
DOI: 10.1542/peds.2016-1404
Accepted for publication Sep 22, 2016
Address correspondence to Natalia Ballardini, MD, PhD, Institute of Environmental Medicine, Karolinska Institutet, Nobels väg 13, SE-171 77 Stockholm, Sweden.
E-mail: natalia.ballardini@ki.se
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2017 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: This work was supported by research grants from the Swedish Research Council, the Stockholm County Council, the Swedish Asthma and Allergy
Association’s Research Foundation, the Swedish Cancer and Allergy Foundation, the Hesselman Foundation, Karolinska Institutet, the Karin and Sten Mörtstedt
Initiative on Anaphylaxis, and the Ministry of Higher Education and Research in Luxembourg.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

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PEDIATRICS Volume 139, number 4, April 2017                                                                                                    e5
Anaphylactic Reactions to Novel Foods: Case Report of a Child With Severe
                             Crocodile Meat Allergy
Natalia Ballardini, Anna Nopp, Carl Hamsten, Mirja Vetander, Erik Melén, Caroline
  Nilsson, Markus Ollert, Carsten Flohr, Annette Kuehn and Marianne van Hage
               Pediatrics originally published online March 8, 2017;

Updated Information &          including high resolution figures, can be found at:
Services                       http://pediatrics.aappublications.org/content/early/2017/03/06/peds.2
                               016-1404
References                     This article cites 18 articles, 2 of which you can access for free at:
                               http://pediatrics.aappublications.org/content/early/2017/03/06/peds.2
                               016-1404#BIBL
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Anaphylactic Reactions to Novel Foods: Case Report of a Child With Severe
                             Crocodile Meat Allergy
Natalia Ballardini, Anna Nopp, Carl Hamsten, Mirja Vetander, Erik Melén, Caroline
  Nilsson, Markus Ollert, Carsten Flohr, Annette Kuehn and Marianne van Hage
               Pediatrics originally published online March 8, 2017;

 The online version of this article, along with updated information and services, is
                        located on the World Wide Web at:
  http://pediatrics.aappublications.org/content/early/2017/03/06/peds.2016-1404

Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it
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