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Red meat allergy in Sweden: Association with tick sensitization and B-negative blood groups

2013; Elsevier BV; Volume: 132; Issue: 6 Linguagem: Inglês

10.1016/j.jaci.2013.07.050

ISSN

1097-6825

Autores

Carl Hamsten, Thi Anh Thu Tran, Maria Starkhammar, Annelie Brauner, Scott P. Commins, Thomas A.E. Platts‐Mills, Marianne van Hage,

Tópico(s)

Contact Dermatitis and Allergies

Resumo

Over the past few years, allergy to mammalian meat has been identified as a new syndrome of food allergy presenting as symptoms of delayed severe allergic reactions after consumption of red meat (beef, lamb, or pork).1Chung C.H. Mirakhur B. Chan E. Le Q.T. Berlin J. Morse M. et al.Cetuximab-induced anaphylaxis and IgE specific for galactose-alpha-1,3-galactose.N Engl J Med. 2008; 358: 1109-1117Crossref PubMed Scopus (1092) Google Scholar, 2Commins S.P. Satinover S.M. Hosen J. Mozena J. Borish L. Lewis B.D. et al.Delayed anaphylaxis, angioedema, or urticaria after consumption of red meat in patients with IgE antibodies specific for galactose-alpha-1,3-galactose.J Allergy Clin Immunol. 2009; 123: 426-433Abstract Full Text Full Text PDF PubMed Scopus (466) Google Scholar, 3Jacquenet S. Moneret-Vautrin D.A. Bihain B.E. Mammalian meat-induced anaphylaxis: clinical relevance of anti-galactose-alpha-1,3-galactose IgE confirmed by means of skin tests to cetuximab.J Allergy Clin Immunol. 2009; 124: 603-605Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar, 4Morisset M. Richard C. Astier C. Jacquenet S. Croizier A. Beaudouin E. et al.Anaphylaxis to pork kidney is related to IgE antibodies specific for galactose-alpha-1,3-galactose.Allergy. 2012; 67: 699-704Crossref PubMed Scopus (132) Google Scholar These allergic reactions are directed against the carbohydrate galactose-α-1,3-galactose (α-Gal). In the initial studies on red meat allergy, Commins et al5Commins S.P. James H.R. Kelly L.A. Pochan S.L. Workman L.J. Perzanowski M.S. et al.The relevance of tick bites to the production of IgE antibodies to the mammalian oligosaccharide galactose-alpha-1,3-galactose.J Allergy Clin Immunol. 2011; 127: 1286-1293.e6Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar observed that the geographic distribution of IgE antibodies to α-Gal in the United States overlapped the region where the tick Amblyomma americanum is common, suggesting that tick bites might be relevant to these reactions. Since then, several reports have confirmed a relationship between tick bites and red meat allergy.6Nunez R. Carballada F. Gonzalez-Quintela A. Gomez-Rial J. Boquete M. Vidal C. Delayed mammalian meat-induced anaphylaxis due to galactose-alpha-1,3-galactose in 5 European patients.J Allergy Clin Immunol. 2011; 128: 1122-1124.e1Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar, 7Hamsten C. Starkhammar M. Tran T.A. Johansson M. Bengtsson U. Ahlen G. et al.Identification of galactose-alpha-1,3-galactose in the gastrointestinal tract of the tick Ixodes ricinus; possible relationship with red meat allergy.Allergy. 2013; 68: 549-552Crossref PubMed Scopus (155) Google Scholar We have recently identified α-Gal in the gastrointestinal tract of the European tick Ixodes ricinus, which provides further evidence of the tick as an initiator of red meat allergy.7Hamsten C. Starkhammar M. Tran T.A. Johansson M. Bengtsson U. Ahlen G. et al.Identification of galactose-alpha-1,3-galactose in the gastrointestinal tract of the tick Ixodes ricinus; possible relationship with red meat allergy.Allergy. 2013; 68: 549-552Crossref PubMed Scopus (155) Google Scholar In this study we have identified 39 patients with a history of allergic reactions after consumption of mammalian meat and IgE against α-Gal (ImmunoCAP; Thermo Fisher Scientific, Uppsala, Sweden; median, 20 kUA/L; range, 1.3-130 kUA/L; Table I). With the exception of 2 patients, they all described delayed symptoms in which urticaria was dominant, but as many as 45% had experienced anaphylaxis (Table I). All patients had IgE against α-Gal–containing allergen sources, such as beef and pork, and the majority also had IgE to cow's milk, dog, cat, and moose (see Table E1 in this article's Online Repository at www.jacionline.org). Significant correlations between IgE to α-Gal and the different mammalian allergens were noted (see Fig E1 in this article's Online Repository at www.jacionline.org). Because the medical investigation revealed that all patients had been bitten by ticks, the majority more than 10 times (Table I), we investigated whether our patients were sensitized to the European tick I ricinus and whether they also recognized IgE epitopes in A americanum (described in the Methods section in this article's Online Repository at www.jacionline.org). We found that all but 2 patients had IgE antibodies to I ricinus (Table I). Although the IgE levels to I ricinus were less than those to α-Gal, we observed a strong correlation, supporting the association between tick bites and sensitization to α-Gal (Fig 1, A). This is in line with the results by Commins et al,5Commins S.P. James H.R. Kelly L.A. Pochan S.L. Workman L.J. Perzanowski M.S. et al.The relevance of tick bites to the production of IgE antibodies to the mammalian oligosaccharide galactose-alpha-1,3-galactose.J Allergy Clin Immunol. 2011; 127: 1286-1293.e6Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar who reported an equally strong correlation between IgE to α-Gal and the tick A americanum among patients presenting with allergic reactions from the southeastern United States. More than 35% of the patients with red meat allergy reported here were also sensitized to A americanum, but the IgE levels were much lower than those to I ricinus, suggesting that I ricinus is the species to which they were primarily sensitized. However, the IgE antibody levels against both tick species correlated significantly (Fig 1, B).Table ICharacteristics of patients with meat allergyPatient no.Age (y)/sexReactionTime to reaction†Reported time to reaction expressed in hours.IgE∗ImmunoCAP IgE results: total IgE levels are expressed in kilounits per liter, and allergen-specific IgE levels are expressed in kilounits of allergen per liter.Tick bites‡Estimated total number of tick bites: +, 1 to 10; ++, 10 to 50; and +++, 50 to 100.Blood groupTotalα-GalBeefI ricinusA americanum167/MAE, GI, U6260545.0305.2+++A240/FANA, GI, U3-4120163.50.46<0.10++A363/FGI, U220135.50.60<0.10++A469/MAE, GI, U42802311406.0+++A539/MAE, GI, U4-5336.44.40.72<0.10++A674/MU3-421030101.9<0.10+A751/MANA, U4-5252.21.40.17<0.10+++A848/FAE, ANA, GI, U0.25-1150167.94.7<0.10+++O943/MAE, ANA, GI, U832088113.10.15+++O1069/MGI, U687184.91.5<0.10+A1146/MGI2904.42.20.35<0.10+O1270/MAE, U642013016371.5+++O1348/FGI, U2-68706.2112.80.87++A1444/MAE, ANA, GI, U4-71800244.5102.6++O1533/FAE, ANA, GI, U6-7270467.20.34<0.10+O1665/FAE, ANA, U655031221311+O1769/MAE, U10-1213025208.10.13+A1863/FAE, ANA, GI, U3-4140203.00.17<0.10+A1938/FGI, U6140193.22.30.23++A2054/MANA, GI, U2203.61.10.27<0.10+O2174/FAE, GI, U8301.60.530.3<0.10++A2236/MGI, U6-780223.32.10.11+++O2360/MAE, ANA, U6-72200766.2545.9+++O2454/FANA, U5-6130193.82.9<0.10+++A2537/FAE, ANA, GI, U6-7110122.81.2<0.10+O2657/FGI, U2-850296.30.61<0.10+A2769/MAE, ANA, GI, U6486.60.49<0.10<0.10+++O2849/MANA, U748101.80.36<0.10++A2957/MU3332.40.250.11<0.10++O3052/FAE, ANA, U1-287125.42.7<0.10++O3173/MGIND340376.01.41.3+O3245/FAE, U5445.00.3<0.10<0.10++AB3336/FAE, GI, U4-5120379.96.90.32+++O3444/FU2-72401109.70.26<0.10++O3540/MGI, U627084283.3<0.10++O3641/FGI, U336061121.5<0.10+A3718/FAE, ANA, GI, U4-81801.30.930.560.64+O3855/MGI, U4-12150221.94.4<0.10+++B3970/MAE, ANA, GI, U0.25-3150231.93.6<0.10++OAE, Angioedema; ANA, anaphylaxis; F, female; GI, gastrointestinal symptoms; M, male; ND, not determined; U, urticaria.∗ ImmunoCAP IgE results: total IgE levels are expressed in kilounits per liter, and allergen-specific IgE levels are expressed in kilounits of allergen per liter.† Reported time to reaction expressed in hours.‡ Estimated total number of tick bites: +, 1 to 10; ++, 10 to 50; and +++, 50 to 100. Open table in a new tab AE, Angioedema; ANA, anaphylaxis; F, female; GI, gastrointestinal symptoms; M, male; ND, not determined; U, urticaria. We were also interested in examining the allergenic cross-reactivity between I ricinus and A americanum. A serum pool of 4 Swedish patients with meat allergy (25 kUA/L to I ricinus and 8.5 kUA/L to A americanum) was preincubated with I ricinus or A americanum tick extract before measurement of I ricinus–specific IgE by mean of ImmunoCAP. The results revealed that the A americanum extract was only able to inhibit 37% of IgE binding to I ricinus at the highest concentration (81 μg/mL). In contrast, the I ricinus extract almost completely inhibited the IgE binding to I ricinus (91%) at the same concentration. The results indicate that the 2 tick species share similar allergen epitopes but that they also have species-specific epitopes. To investigate how common IgE antibodies against α-Gal are in the general population, we screened 143 healthy blood donors from the greater Stockholm area. We found that as many as 10% had IgE antibodies to α-Gal (see Table E2 in this article's Online Repository at www.jacionline.org) compared with 0.7% (1/150) of teenagers from a prospective study on asthma in northern Sweden, where tick bites are rare.5Commins S.P. James H.R. Kelly L.A. Pochan S.L. Workman L.J. Perzanowski M.S. et al.The relevance of tick bites to the production of IgE antibodies to the mammalian oligosaccharide galactose-alpha-1,3-galactose.J Allergy Clin Immunol. 2011; 127: 1286-1293.e6Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar, 8Rönmark E. Bjerg A. Perzanowski M. Platts-Mills T. Lundbäck B. Major increase in allergic sensitization in schoolchildren from 1996 to 2006 in northern Sweden.J Allergy Clin Immunol. 2009; 124 (e1-15): 357-363Abstract Full Text Full Text PDF PubMed Scopus (137) Google Scholar We also screened 207 patients with Lyme disease as a confirmed recently tick-bitten population and found 22% to have positive IgE levels to α-Gal (see Table E3 in this article's Online Repository at www.jacionline.org). We noted that the IgE titers to α-Gal between healthy blood donors and patients with Lyme disease did not differ and were significantly lower (median titer of α-Gal–positive subjects: 0.16 kUA/L and 0.25 kUA/L, respectively) than the levels of the patients with red meat allergy (20 kUA/L, P < .001; Fig 1, C). These low levels probably reflect sensitization only and are not predictive of an allergic reaction. However, the frequency of α-Gal–sensitized subjects was significantly higher in the group with Lyme disease compared with the healthy blood donors (46/207 vs 5/143; Fig 1, D; χ2 = 8.09; P = .005), which strengthens the role of tick bites for the induction of IgE to α-Gal. When comparing the patients with red meat allergy with the α-Gal–positive patients with Lyme disease, we found that their median IgE titer to α-Gal was significantly higher and that the correlations between α-Gal and total IgE, as well as I ricinus, were significantly stronger. Similarly, IgE responses to I ricinus were significantly higher in both frequency (37/39 vs 21/46, χ2 = 23.59, P < .001) and median levels (1.49 vs <0.10 kUA/L, P < .001) in patients with red meat allergy compared with those seen in α-Gal–positive patients with Lyme disease. For both groups, the responses to I ricinus correlated with total IgE levels (r = 0.65 and r = 0.52, respectively; P < .001, see Fig E2 in this article's Online Repository at www.jacionline.org). Because the α-Gal epitope is a major blood group substance of nonprimate mammals and structurally related to blood group B, we investigated the blood type of our population with meat allergy. We found that all but 2 patients belonged to the B-negative blood groups (A or O, 5%) which is significantly less compared with the expected number in the Swedish population (18%; www.geblod.nu). A recent study on the relationship between IgG and IgE responses to α-Gal and blood group B found that none of the B-positive subjects expressed IgE to α-Gal.9Rispens T. Derksen N.I. Commins S.P. Platts-Mills T.A. Aalberse R.C. IgE production to alpha-Gal is accompanied by elevated levels of specific IgG1 antibodies and low amounts of IgE to blood group B.PLoS One. 2013; 8: e55566Crossref PubMed Scopus (88) Google Scholar Also, 86% of the healthy blood donors and 78% of the patients with Lyme disease who had positive IgE levels to α-Gal were B-negative, and in the majority the IgE levels to α-Gal were very low. Taken together, we here report that there is a strong relationship with tick bites for the production of IgE to α-Gal and, for the first time, that red meat allergy is strongly associated with the B-negative blood groups. A total of 39 patients reporting delayed allergic reactions after consumptions of red meat; attending the Allergy Unit at Södersjukhuset, Stockholm, Sweden; and having IgE to α-Gal were enrolled in the study. All patients were examined by a physician experienced in allergic diseases and responded to a detailed questionnaire regarding symptoms of meat intake and exposure to ticks. Blood samples were drawn for analysis of IgE antibodies to a panel of different food and inhalant allergens. The patients were also blood typed according to routine methods (Blood Center, Karolinska University Hospital, Stockholm, Sweden). Sera from 143 healthy blood donors (Blood Center, Karolinska University Hospital) were tested for IgE antibodies to α-Gal. Sera from 207 patients with confirmed Borrelia species infection (IgG to Borrelia burgdorferi; median ratio, 2.22 arbitrary units (AU); range, 0.9-5.04 AU; cutoff, 0.5 AU [OXOID IDEIA Borrelia burgdorferi IgG, OXOID, Cambridgeshire, United Kingdom]; Department of Clinical Microbiology, Karolinska University Hospital) were also tested for IgE antibodies to α-Gal. Subjects in these 2 groups with α-Gal titers of 0.1 kUA/L or greater were analyzed for total IgE and a panel of allergens. Borrelia species–positive sera having an α-Gal level of 0.1 kUA/L or greater were blood typed. The study was approved by the local ethics committee. Adult pathogen-free I ricinus ticks (IS Insect Service GmbH, Berlin, Germany) were stored at −80°C until preparation of whole-body extracts. Tick extract was prepared by crushing frozen ticks with a tissue homogenizer (Bertin Technologies, Montigny-le-Bretonneux, France) in PBS (pH 7.4). After centrifugation, the supernatant was collected. In addition, extract of adult pathogen-free A americanum ticks (Oklahoma State Tick Rearing Facility, Stillwater, Okla) was prepared, as previously described.E1Commins S.P. James H.R. Kelly L.A. Pochan S.L. Workman L.J. Perzanowski M.S. et al.The relevance of tick bites to the production of IgE antibodies to the mammalian oligosaccharide galactose-alpha-1,3-galactose.J Allergy Clin Immunol. 2011; 127: 1286-1293.e6Abstract Full Text Full Text PDF PubMed Scopus (392) Google Scholar Total IgE levels and allergen-specific IgE antibody reactivity to α-Gal, beef, moose, pork, chicken, milk, dog, cat, the major cat allergen rFel d 1 and serum albumin from cat (Fel d 2), and beef (Bos d 6) were determined (ImmunoCAP, Phadia AB/Thermo Fisher Scientific). IgE antibodies against tick proteins (I ricinus and A americanum) were measured by coupling 5 μg of biotinylated tick antigen to Streptavidin ImmunoCAP, as described by the manufacturer (Phadia AB/Thermo Fisher Scientific). This assay is not commercially available. All IgE determinations were analyzed by using the ImmunoCAP System (Phadia AB/Thermo Fisher Scientific), according to the manufacturer's instructions. The results are presented as kilounits of allergen per liter. The cutoff for total IgE was 2 kU/L or greater, and that for allergen-specific IgE was 0.1 kUA/L or greater. The capacity of I ricinus (2 mg/mL) or A americanum (2.6 mg/mL) extracts to inhibit IgE binding to solid phase–bound I ricinus (Streptavidin ImmunoCAP) was performed, essentially as described for the ImmunoCAP System (Phadia AB/Thermo Fisher Scientific). However, a prior step of 1-hour preincubation of a serum pool of 4 Swedish patients with meat allergy with 3-fold dilutions (0.01-81 μg/mL) of either extracts from I ricinus or A americanum was included. The expected ABO blood group distribution was obtained from official national data in Sweden (available at http://www.geblod.nu). Statistical analysis was performed with GraphPad Prism software (version 6; GraphPad Software, La Jolla, Calif). Quantitative measurements of IgE antibodies were compared by using Spearman rank correlation and Mann-Whitney U tests. Categorical measures were compared with the χ2 test for trend. The frequency of B-positive subjects compared with a theoretical outcome was performed by using the binominal test. A P value of less than .05 was considered significant.Fig E2Correlation between IgE responses to I ricinus and total IgE levels in patients with meat allergy (A) and patients with Lyme disease with positive IgE levels to α-Gal (B).View Large Image Figure ViewerDownload Hi-res image Download (PPT)Table E1Further characteristics of patients with meat allergyPatient no.IgE∗ImmunoCAP IgE results are presented in kilounits of allergen per liter.PorkMooseChickenMilkDogCatrFel d 11120.84<0.100.842.21.5<0.1022.10.5<0.100.380.830.40.3732.30.3<0.101.20.280.45<0.1046.22.0<0.103.83.40.96<0.1053.11.4<0.100.51.00.24<0.1061.71.01.42.80.611.1<0.1070.90.7<0.100.170.30.640.4185.22.2<0.103.15.33.1<0.1095.51.60.223.02.61.5<0.10104.41.5<0.101.10.980.64<0.10112.50.12<0.100.290.26<0.10<0.1012193.6<0.1054.41.9<0.10135.20.48<0.100.392.40.93<0.10144.86.10.391.4142012155.10.8<0.100.921.40.41<0.1016266.20.134.29.13.30.1517132.1<0.103.63.12.00.44181.60.28<0.100.320.160.3<0.10192.51.1<0.100.81.10.4<0.10200.860.19<0.100.160.270.11<0.10210.480.21<0.100.180.17<0.10<0.102220.820.130.560.650.280.1623210.920.43.26.33.50.47247.60.61<0.100.422.70.78<0.10251.80.85<0.100.762.90.53<0.10262.31.0<0.101.10.690.2<0.10270.27<0.10<0.10<0.100.12<0.10<0.10280.990.31<0.100.180.472.41.6290.14<0.10<0.10<0.100.21<0.10<0.10304.53.9<0.102.61.81.3<0.10315.90.890.120.980.610.31<0.10320.14<0.10<0.10<0.10<0.10<0.10<0.1033101.8<0.102.31.10.72<0.10348.10.69<0.100.840.730.35<0.1035245.4<0.105.05.92.00.23367.91.9<0.101.61.41.91.9370.860.33<0.100.210.210.12<0.10380.750.47<0.100.340.563.02.3390.670.44<0.100.360.532.92.3∗ ImmunoCAP IgE results are presented in kilounits of allergen per liter. Open table in a new tab Table E2Characteristics of healthy blood donors with IgE responses of 0.1 kUA/L or greater to α-GalSample IDAge (y)/sexIgE∗ImmunoCAP IgE results (total IgE, kilounits per liter; allergen-specific IgE, kilounits of allergen per liter).Blood typeTotalα-GalBeefTickMilkDogCatrFel d 1ChickenH2367/M1500.16<0.10<0.10<0.10<0.10<0.10<0.10<0.10AH2638/F610.14<0.10<0.10<0.100.10<0.10<0.10<0.10AH2829/M180.12<0.10<0.10<0.10<0.10<0.10<0.10<0.10AH3436/M180.70.30.160.110.10<0.10<0.10<0.10AH4058/M1200.14<0.10<0.10<0.10<0.10<0.10<0.10<0.10AH4522/M100.13<0.10<0.10<0.10<0.10<0.10<0.10<0.10AH4823/M8600.59<0.10<0.100.32<0.10<0.10<0.10<0.10BH5147/M151.20.27<0.10<0.100.110.260.28<0.10AH6546/F200.2<0.10<0.10<0.10<0.10<0.10<0.10<0.10AH9665/F180.13<0.10<0.10<0.10<0.10<0.10<0.10<0.10OH11419/F90.12<0.10<0.10<0.10<0.10<0.10<0.10<0.10ABH11835/F1100.190.80.131.86.29.80.22<0.10OH11942/M1800.1<0.10<0.10<0.10<0.10<0.10<0.10<0.10OH12855/M600.620.140.15<0.10<0.10<0.10<0.10<0.10AH13662/F110.37<0.10<0.10<0.10<0.10<0.10<0.10<0.10A∗ ImmunoCAP IgE results (total IgE, kilounits per liter; allergen-specific IgE, kilounits of allergen per liter). Open table in a new tab Table E3Characteristics of patients with Lyme disease with IgE responses of 0.1 kUA/L or greater to α-GalSample IDIgE∗ImmunoCAP IgE results (total IgE, kilounits per liter; allergen-specific IgE, kilounits of allergen per liter).Blood typeTotalα-GalBeefTickMilkDogCatrFel d 1ChickenL12408.53.20.820.660.340.2<0.10<0.10AL4350.530.14<0.100.1<0.10<0.10<0.10<0.10AL62500.85<0.10220.19<0.10<0.10<0.10<0.10AL14440111.20.510.370.280.11<0.10<0.10ABL17120.23<0.10<0.10<0.10<0.10<0.10<0.10<0.10AL28290.13<0.100.220.22<0.10<0.10<0.10<0.10OL39171.70.30<0.10<0.10<0.10<0.10<0.10<0.10OL44300.12<0.10<0.10<0.10<0.10<0.10<0.10<0.10AL453200.170.17<0.10<0.100.14<0.10<0.10<0.10AL68270.24<0.100.13<0.10<0.10<0.10<0.10<0.10OL71590.12<0.10<0.10<0.10<0.10<0.10<0.10<0.10AL727.80.12<0.10<0.10<0.10<0.10<0.10<0.10<0.10AL74130.190.17<0.100.14<0.10<0.10<0.10<0.10OL75150.12<0.100.28<0.10<0.10<0.10<0.10<0.10OL811800.26<0.10<0.100.774.73.12.8<0.10OL951800.110.13<0.100.680.310.680.60<0.10OL96780.270.115.4<0.100.10<0.10<0.10<0.10OL99172.70.790.430.260.18<0.10<0.10<0.10OL100920.36<0.100.140.21NANA<0.10<0.10OL1024500.11<0.109.3<0.105.78.88.5<0.10OL1039.10.18<0.10<0.100.16<0.10<0.10<0.10<0.10BL106100.46<0.10<0.10<0.10<0.10<0.10<0.10<0.10OL111630.410.232.80.130.20<0.10<0.10<0.10OL1121500.16<0.107.50.180.251.21.4<0.10OL1166403.00.100.622.4NANA<0.100.13BL122420.170.16<0.100.77<0.10<0.10<0.10<0.10OL1252200.60.490.390.231.03.11.4<0.10OL1289.90.11<0.10<0.100.15<0.10<0.10<0.10<0.10OL139120.13<0.10<0.10<0.10<0.10<0.10<0.10<0.10BL140370.24<0.10<0.10NANANANANAABL14420.21<0.10<0.10<0.10<0.10<0.10<0.10<0.10OL147910.40.18<0.10<0.10<0.10<0.10<0.10<0.10AL149190.25<0.10<0.10<0.10<0.10<0.10<0.10<0.10OL15440002006761716157.80.14AL155260.340.171.2<0.10<0.10<0.10<0.10<0.10AL164870.630.25<0.10<0.10<0.10<0.10<0.10<0.10AL1662000.72<0.102.6<0.10<0.10<0.10<0.10<0.10ABL171510.470.13<0.10<0.10<0.10<0.10<0.10<0.10BL1751700.14<0.10<0.10<0.10<0.10<0.10<0.10<0.10OL178260.52<0.10<0.10<0.10<0.10<0.10<0.10<0.10BL1884400.49<0.100.10<0.10<0.10<0.10<0.10<0.10BL1918.80.23<0.10<0.10<0.10<0.10<0.10<0.10<0.10AL192NA0.21NA1.7NANANANANABL1953000.590.320.160.12<0.10<0.10<0.10 100>100<0.10OL205860.12<0.10<0.10<0.10<0.10<0.10<0.10<0.10ONA, Not available.∗ ImmunoCAP IgE results (total IgE, kilounits per liter; allergen-specific IgE, kilounits of allergen per liter). Open table in a new tab NA, Not available.

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