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Nut sensitization profile in Southern Taiwan
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Journal of Microbiology, Immunology and Infection xxx (xxxx) xxx
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Original Article
Nut sensitization profile in Southern Taiwan Chih-Wei Cheng a, Yung-Chih Lin e, Bao-Ren Nong a,d, Po-Yen Liu a, Yung-Feng Huang a,d,f,*, Ling-Ying Lu c, Herng-Sheng Lee b a Department of Pediatrics, Kaohsiung Veterans General Hospital, Number 386, Dazhong 1st Road, Zuoying District, Kaohsiung City 813, Taiwan b Department of Pathology and Laboratory, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan c Division of Allergy, Immunology and Rheumatology, Department of Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan d Department of Pediatrics, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan e Department of Pediatrics, Taipei Veterans General Hospital, Taitung Branch, Taitung, Taiwan f Wellem Medical Group, Hangzhou, China
Received 27 May 2018; received in revised form 21 November 2018; accepted 12 December 2018
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KEYWORDS Peanut sensitization; Brazil nut sensitization; Specific IgE; Asthma; Atopic diseases
Abstract Background/purpose: To evaluate the relationship between serum-specific immunoglobulin E (IgE) to peanuts/tree nuts and their clinical manifestations in atopic diseases. Method: Serum from people with the classical symptoms of asthma, allergic rhinitis (AR), or atopic dermatitis (AD) was collected for the measurement of serum-specific IgE to peanuts, cashew nuts, Brazil nuts, almonds, and coconuts. Cases with possible sensitization to these nuts (serum specific IgE S 0.35 kU/L) were selected and their clinical relationships with physician-diagnosed asthma, allergic rhinitis, or atopic dermatitis were analyzed. Result: Compared with non-sensitization group, people with peanut/tree nut sensitization have higher prevalence of atopic dermatitis, but no such difference noted in the prevalence of allergic rhinitis. In the situation of asthma, people with sensitization to peanuts and Brazil nuts, but not other nuts, have higher prevalence of asthma than people without sensitization to any nut (p < 0.001 and p < 0.05, respectively). Binary logistic regression analysis also showed positive associations between peanut (OR: 1.164, p value Z 0.017) and Brazil nut (OR: 1.304, p value Z 0.055) sensitization and asthma. The associations between peanut and Brazil nut sensitization and asthma were independent of the prevalence of other atopic diseases. Conclusion: People in Asia may have less severe allergic effects as in Western countries, but sensitization to specific food allergens such as peanuts or Brazil nuts may predispose individuals to asthma, which could be helpful in diagnosis and deserves more attention than previously considered.
* Corresponding author. No.8 Lane 121 Bansin Road Banciao District, New Taipei City 22052, Taiwan. Fax: þ886 7 3468207. E-mail addresses: [email protected] (C.-W. Cheng), [email protected] (Y.-F. Huang). https://doi.org/10.1016/j.jmii.2018.12.005 1684-1182/Copyright ª 2019, Taiwan Society of Microbiology. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005
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C.-W. Cheng et al. Copyright ª 2019, Taiwan Society of Microbiology. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/bync-nd/4.0/).
Introduction Food allergy affects 3.44e6.40% of children and 7.65% of adults in Taiwan, with growing evidence of a worldwide increasing in its prevalence.1e6 The “major allergens” responsible for most significant reactions include milk, eggs, peanuts, tree nuts, shellfish, fish, wheat, and soy.6e8 Even though a population-based study indicated peanut and tree nut allergy and related adverse effects are relatively low in Asian populations,9e11 peanuts are still one of the most common food triggers in Taiwan.3,5 Over the past decades, both food allergy and atopic disorders have shown an increasing prevalence in children worldwide, and asthma is now one of the most common chronic disorders in Asian adults and children.12e16 In addition to the wellestablished linkage between eczema and food allergy,17 studies have also shown the association between food sensitization and the development and exacerbation of asthma. Increased asthma severity, hospitalization, and the use of corticosteroids are also correlated with food sensitization.18e21 Quantification of food-specific IgE by ImmunoCAP is now an available and reliable tool to predict possible food allergy without taking the risks of anaphylaxis after food challenges into account.22,23 In this study, we collected the data of specific IgE to different nuts and attempted to determine the relationship between food sensitization to peanuts or tree nuts and atopic diseases.
Methods Patients and samples People showed the classical symptoms of asthma, allergic rhinitis, or atopic dermatitis (detail clinical symptoms and signs were described in following section “clinical manifestations”), were enrolled from the outpatient department of Kaohsiung Veterans General Hospital, Taiwan, from January 2014 to April 2017. The serum was collected and specific IgE to peanuts, cashew nuts, Brazil nuts, almonds, and coconuts was measured by the Phadia ImmunoCAP system (ImmunoCAP specific IgE; Phadia, Inc, Uppsala, Sweden). The cut-off value of sensitization to a specific allergen was defined as food specific IgES0.35 kU/L.23
Clinical manifestations Data were collected through retrospective medical chart reviews, and diagnoses were made by board-certified doctors based on patient histories, clinical features and related criteria. Asthma was defined as per physician diagnosis and being symptomatic in the prior year of the survey. Atopic dermatitis was diagnosed by typical skin manifestations, pruritus, chronic or relapsing course, and personal/family
history of atopic diseases. The diagnosis of allergic rhinitis was based upon the presence of characteristic symptoms, suggestive clinical histories, and supportive findings on physical examination.
Statistical analysis Sigmaplot (Systat Software Inc., version 12.5, San Jose, CA, USA) and the SPSS statistics analysis package (SPSS for Windows, version 20.0, Chicago, IL, USA) were used to perform the statistical analysis. One-way ANOVA was used to analyze the differences between nut sensitization groups. Test of proportion, Z test, was utilized to calculate the difference in disease prevalence between groups. The binary logistic regression was used to analyze the association between specific IgE level and atopic diseases, the odds ratio (OR), the p value, and the 95% confidence interval (CI) of OR. A p value < 0.05 was considered statistically significant. The HosmereLemeshow test was used to verify if the binary logistic regression models were valid. The p value > 0.05 was considered the model is valid.
Results Three hundred and thirty-three patients were enrolled in this study. The age range was from 2 to 93 years old with the mean age 38.0 years old, and men comprised 37.8% of the study participants. More than half of patients had cutaneous and respiratory symptoms. There were 555 data of serum specific IgE, among them, 339 were considered as food sensitization based on their antigen specific IgE level (S0.35 kU/L). These included peanuts (n Z 124, 36.6%), cashew nuts (n Z 64, 18.9%), Brazil nuts (n Z 28, 8.3%), almonds (n Z 73, 21.5%), and coconuts (n Z 50, 14.7%), respectively. Another 216 samples were considered as non-sensitization to nuts according to the same criteria. The most common nut of sensitization was the peanut, and the least was Brazil nut. The specific IgE levels ranged from 0.35 to 47.5 kU/L (Fig. 1). Most specific IgE levels were around 0.35e10 kU/L, and the mean level was 3.00 kU/L (peanuts), 2.72 kU/L (cashew nuts), 2.09 kU/L (Brazil nuts), 2.07 kU/L (almonds), and 2.06 kU/L (coconuts), respectively. The distribution patterns were similar in different groups of nut sensitization. A few patients had extremely high specific IgE levels up to around 30e40 kU/L. There was no difference in specific IgE level noted between groups. For each group of nut sensitization, the prevalence of asthma was 39.52% for the peanuts, 12.50% for the cashew nuts, 21.43% for the Brazil nuts, 13.70% for the almonds, and 12.00% for the coconuts. The prevalence of asthma in non-sensitization group was 7.4%. Test of proportion, Z test, was introduced for statistical analysis. There are
Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005
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Nut sensitization profile in Southern Taiwan
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Figure 1. The serum specific IgE level was plotted with logarithmic scale. Each dot represents one sample. The horizontal line is the mean of each group.
significant differences in asthma prevalence of peanut or Brazil nut sensitization group and non-sensitization group, and the p values were <0.001 and < 0.05, respectively (Fig. 2). The relationship between diseases and specific IgE levels were estimated by using binary logistic regression analysis. There was a trend of positive correlations between asthma and specific IgE to different nuts (Table 1). The OR in binary logistic regression means the probability of asthma. With the serum-specific IgE increasing every one unit (kU/L), the possibility of asthma increases by ORfold. For Brazil nuts, as the serum-specific IgE level increases from 1 to 2 kU/L, the possibility of asthma increases 1.304 times. In these analyses, peanuts bore a strong correlation to asthma development when the specific IgE level increased (OR: 1.164, 95% CI: 1.027e1.319, p value Z 0.017). Brazil nuts group also showed a possible correlation between serum IgE level and asthma, although this lacked statistical significance. The HosmereLemeshow test was used to verify if the binary logistic regression models were valid. The p Z 0.122 for peanut and 0.425 for Brazil nut, both non-significant, means the regression results were valid. The prevalence of allergic rhinitis was 41.94% in the peanut sensitization group, 42.19% in the cashew nut group, 42.86% for Brazil nuts, 36.97% for almonds, 38.00% for coconuts, and 41.2% for non-sensitization group. There was no significant difference in the prevalence of allergic rhinitis, whether sensitization to nuts or not. For the situation of atopic dermatitis, the prevalence was 45.97%, 38.36%, 46.43%, 42.47%, 44% and 26.4, respectively. Higher
prevalence of atopic dermatitis was noted in nuts sensitization groups. Considering the association with nut sensitization, unlike the situation in asthma, there was no significant difference noted between different nuts sensitization groups, but significant difference was noted between sensitization and non-sensitization group (all p < 0.05 according to different nuts). Under the binary logistic regression model, there was no obvious positive correlation between specific IgE level and allergic rhinitis or atopic dermatitis, as shown in Table 1.
Discussions With the increasing prevalence of food sensitization1,5,24 and atopic diseases, the use of specific IgE to identify allergic conditions has increased. The goal of this study was to identify the relationship between specific IgE to nuts and atopic diseases. The Kaohsiung Veterans General Hospital is located in southern Taiwan, in a sub-tropical region. According to our knowledge, this is the first study to evaluate the relationship between nut sensitization and atopic diseases in a tropical area. In our data, there was no difference in specific IgE level distribution between population sensitization to different nuts. People with nut sensitization have higher asthma prevalence compared with non-sensitization group, especially those sensitized to peanuts (39.52%, 49/124 persons) and Brazil nuts (21.43%, 6/28 persons) (Fig. 2). Patients enrolled in this study also showed a much higher prevalence of atopic dermatitis than non-sensitization
Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005
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Figure 2.
The prevalence of asthma in each nut sensitization group.
Table 1 The binary logistic regression results between the level of specific IgE and atopic diseases development. Disease/Nuts
OR
95% CI
p value
Asthma
1.164 1.123 1.304 1.048 1.093 1.064 0.974 0.959 1.006 1.026 0.973 1.029 0.903 0.885 0.846
1.027e1.319 0.989e1.274 0.994e1.710 0.946e1.161 0.957e1.249 0.973e1.163 0.890e1.065 0.758e1.213 0.914e1.109 0.905e1.163 0.909e1.042 0.949e1.116 0.699e1.166 0.704e1.112 0.615e1.163
0.017 0.073 0.055 0.369 0.191 0.172 0.561 0.727 0.895 0.689 0.438 0.485 0.435 0.293 0.303
AR
AD
Peanuts Cashew Nuts Brazil Nuts Almonds Coconuts Peanuts Cashew Nuts Brazil Nuts Almonds Coconuts Peanuts Cashew Nuts Brazil Nuts Almonds Coconuts
OR Z odds ratio; CI Z confidence interval.
group. The binary logistic regression model also showed positive association between odds ratios of asthma development and level of specific IgE to peanuts or Brazil nuts (Table 1). The gold standard for the diagnosis of food allergy is the double-blind, placebo-controlled food challenge, but food
challenge can be time-consuming, and catastrophic to patients with potential danger.25,26 By using data from retrospective and prospective studies, it is possible to generate probability curves that depict the likelihood of patients with particular food-specific IgE reaction during a food challenge.22,23,26 The detection of specific IgE to certain food antigens has been shown to be predictive of symptomatic IgE-medicated food allergy. Illustrated by the example of peanuts, specific IgES0.35 kU/L could be considered as peanut sensitization and specific IgE as high as 13 kU/L could be diagnosed as food allergy with 96% of specificity.23 Quantification of specific IgE to certain food antigens would aid in the diagnosis of food sensitization or food allergy and decrease the necessity of food challenge. As a part of “atopic march”, the link between food allergy and infantile eczema has been well-established.17 The relationship between food allergy and respiratory manifestations of atopic disease has been less emphasized before, but evidences have emerged recently. Tariq et al. indicated egg allergy in infancy, especially when co-existing with eczema, increases respiratory allergic symptoms and aero-allergen sensitization in childhood.27 The study of Roberts et al. showed poor controlled asthma and food allergy are significant risk factors for life-threatening asthma.28 In France, Penard-Morand et al. found reported food allergy, food sensitization and skin prick-tested food allergy were all positively associated with asthma and allergic rhinitis. They concluded the relationship between food allergy and asthma or allergic rhinitis could be totally
Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005
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Nut sensitization profile in Southern Taiwan explained neither by existence of respiratory manifestations of food allergy nor by sensitization to aero-allergens. Instead, food allergy might intervene via other mechanisms than sensitization to aero-allergens in asthma and allergic rhinitis development.21 The following studies revealed not only strong linkage between asthma development and food allergy, but also that the severity and morbidity of asthma, and even healthcare utilization and medication use were associated with the severity and the numbers of food allergies.18,19,29 In addition to egg and milk allergy, which have been specifically implicated as risk factors for the development of asthma, both peanut allergy and tree nut allergy were also notorious culprits as determined in the literature.30,31 Food allergy alone could lead to the increased odds ratios of hospitalization (OR: 2.35, 95% CI: 1.30e4.24, p Z 0.005), and the need for the use of controller medication (OR: 1.99, 95% CI: 1.06e3.74, p Z 0.03).19,29 Increasing evidences imply food allergy is an important and independent risk factor for asthma, and is even irrespective of whether food allergy resolves.20 According to the study using the National Health Insurance database in Taiwan based on ICD-9 coding, the prevalence of asthma, allergic rhinitis, and atopic dermatitis were 2.9%, 11.3%, and 1.2%, respectively.16 Large international studies via questionnaires, ISAAC phase three study, between 2002 and 2003 disclosed the prevalence of asthma symptoms, allergic rhinoconjunctivitis symptoms, and eczema symptoms in Taiwan were 9.8%, 24.2%, and 6.7%, respectively.12 Compared with the findings of previous studies, our study showed much higher prevalence of asthma, allergic rhinitis, and atopic dermatitis in all nut sensitization groups and even nonsensitization group than in the general population. This further implied possible correlation between food allergy and atopic diseases as mentioned in previous studies. Although the population enrolled in this study was people with suspecting atopic diseases which would influence the interpretation, it is worth noting that people with peanut and Brazil nut sensitization had much higher asthma prevalence even within nut sensitization groups. No such difference was noted in the prevalence of allergic rhinitis and atopic dermatitis. These results suggested the relationship between asthma and peanut or Brazil nut sensitization is independent of the prevalence of other atopic diseases. Binary logistic regression analysis also revealed a positive association between nut sensitization and asthma, especially in the peanut group. These results suggested that sensitization to some specific foods, but not all, can be independent risk factors of asthma development. Peanut allergy deserves particular attentions in Western countries for its severe allergic reactions, which do not usually resolve spontaneously, and trace quantities of peanuts are enough to induce an allergic reaction.32,33 Based on data from food anaphylaxis registries, the peanut is the most common food trigger of fatal anaphylaxis in these communities.34,35 Unlike the growing prevalence and severe allergic reactions of peanuts in Western populations, some studies have revealed seafood and fish were mainly responsible for severe food allergy in Taiwanese and Asian populations.9,10 Peanuts and tree nuts are important food allergens to cause anaphylaxis in Westerners, but they also
5 cause severe reactions in patients in Asian regions.10 According to the Japanese food allergy guideline 201736, the frequency of anaphylactic shock due to peanut allergy was 13.2%. Similarly, peanut and tree nut allergies are not rare in Taiwan. According to a questionnaire-based study in Taiwan, shrimp (51.6%) and crab (34.0%) are the most common causes of severe food allergy, but peanuts still account for an important part (9.9%).37 Apart from anaphylaxis, peanut and tree nut allergies might play an important role in atopic diseases in Taiwan population as shown in our study. This study has some limitations. First, this was a single center study in southern Taiwan comprising a small sample size. For the geographic difference of food allergy, the results may be not applicable to other ethnicities. Instead, the emphasis of this study is on the fact that not only aerosensitization but also some food sensitization could be a risk factor in asthma development. Second, the samples were collected from people suspected of having atopic diseases. They might come to outpatient departments for their pre-existing atopic diseases and thereby cause the high prevalence of atopic diseases in our study. No data were acquired from the health population, and therefore these results may not apply to the general population, and should be interpreted with caution. The prevalence of food sensitization and likely food allergy, is increasing in patients with asthma and this is associated with increased healthcare-related expenditure. Sensitization to peanuts or Brazil nuts might predispose individuals to asthma. Caregivers should consider the analysis of food allergy for patients under standard medications for intractable asthma. Sensitization to specific food allergens may account for more attention in asthma prediction and diagnosis than previously considered.
Conflicts of interest The authors declare that they have no conflicts of interest relevant to the material discussed in this article.
Acknowledgments This study was funded by Kaohsiung Veterans General Hospital (VGHKS 106-040).
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6 5. Prescott SL, Pawankar R, Allen KJ, Campbell DE, Sinn J, Fiocchi A, et al. A global survey of changing patterns of food allergy burden in children. World Allergy Organ J 2013;6:21. 6. Sicherer SH, Sampson HA. Food allergy. J Allergy Clin Immunol 2010;125:S116e25. 7. Hefle SL, Nordlee JA, Taylor SL. Allergenic foods. Crit Rev Food Sci Nutr 1996;36(Suppl):S69e89. 8. Sicherer SH, Munoz-Furlong A, Godbold JH, Sampson HA. US prevalence of self-reported peanut, tree nut, and sesame allergy: 11-year follow-up. J Allergy Clin Immunol 2010;125: 1322e6. 9. Shek LP, Cabrera-Morales EA, Soh SE, Gerez I, Ng PZ, Yi FC, et al. A population-based questionnaire survey on the prevalence of peanut, tree nut, and shellfish allergy in 2 Asian populations. J Allergy Clin Immunol 2010;126:324e31. 331 e1-7. 10. Chan CF, Chen PH, Huang CF, Wu TC. Emergency department visits for food allergy in Taiwan: a retrospective study. Pediatr Neonatol 2014;55:275e81. 11. Al-Muhsen S, Clarke AE, Kagan RS. Peanut allergy: an overview. CMAJ 2003;168:1279e85. 12. Asher MI, Montefort S, Bjorksten B, Lai CK, Strachan DP, Weiland SK, et al. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet 2006;368:733e43. 13. Song WJ, Wong GWK. Changing trends and challenges in the management of asthma in Asia. J Allergy Clin Immunol 2017; 140:1272e4. 14. Song WJ, Kang MG, Chang YS. Epidemiology of adult asthma in Asia: toward a better understanding. Asia Pac Allergy 2014;4: 75e85. 15. Wong GW, Leung TF, Ko FW. Changing prevalence of allergic diseases in the Asia-Pacific region. Allergy Asthma Immunol Res 2013;5:251e7. 16. Hwang CY, Chen YJ, Lin MW, Chen TJ, Chu SY, Chen CC, et al. Prevalence of atopic dermatitis, allergic rhinitis and asthma in Taiwan: a national study 2000 to 2007. Acta Derm Venereol 2010;90:589e94. 17. Arshad SH, Matthews S, Gant C, Hide DW. Effect 0of allergen avoidance on development of allergic disorders in infancy. Lancet 1992;339:1493e7. 18. Wang J, Visness CM, Sampson HA. Food allergen sensitization in inner-city children with asthma. J Allergy Clin Immunol 2005; 115:1076e80. 19. Schroeder A, Kumar R, Pongracic JA, Sullivan CL, Caruso DM, Costello J, et al. Food allergy is associated with an increased risk of asthma. Clin Exp Allergy 2009;39:261e70. 20. Vermeulen EM, Koplin JJ, Dharmage SC, Gurrin LC, Peters RL, McWilliam V, et al. Food allergy is an important risk factor for childhood asthma, irrespective of whether it resolves. J Allergy Clin Immunol Pract 2017. https: //doi.org/10.1016/j.jaip.2017.10.019. 21. Penard-Morand C, Raherison C, Kopferschmitt C, Caillaud D, Lavaud F, Charpin D, et al. Prevalence of food allergy and its relationship to asthma and allergic rhinitis in schoolchildren. Allergy 2005;60:1165e71.
C.-W. Cheng et al. 22. Maloney JM, Rudengren M, Ahlstedt S, Bock SA, Sampson HA. The use of serum-specific IgE measurements for the diagnosis of peanut, tree nut, and seed allergy. J Allergy Clin Immunol 2008;122:145e51. 23. Sampson HA. Utility of food-specific IgE concentrations in predicting symptomatic food allergy. J Allergy Clin Immunol 2001;107:891e6. 24. Sasaki M, Koplin JJ, Dharmage SC, Field MJ, Sawyer SM, McWilliam V, et al. Prevalence of clinic-defined food allergy in early adolescence: the SchoolNuts study. J Allergy Clin Immunol 2018;141. 391-398 e4. 25. Griffiths RLM, El-Shanawany T, Jolles SRA, Selwood C, Heaps AG, Carne EM, et al. Comparison of the performance of skin prick, ImmunoCAP, and ISAC tests in the diagnosis of patients with allergy. Int Arch Allergy Immunol 2017;172: 215e23. 26. Onell A, Whiteman A, Nordlund B, Baldracchini F, Mazzoleni G, Hedlin G, et al. Allergy testing in children with persistent asthma: comparison of four diagnostic methods. Allergy 2017; 72:590e7. 27. Tariq SM, Matthews SM, Hakim EA, Arshad SH. Egg allergy in infancy predicts respiratory allergic disease by 4 years of age. Pediatr Allergy Immunol 2000;11:162e7. 28. Roberts G, Patel N, Levi-Schaffer F, Habibi P, Lack G. Food allergy as a risk factor for life-threatening asthma in childhood: a case-controlled study. J Allergy Clin Immunol 2003; 112:168e74. 29. Friedlander JL, Sheehan WJ, Baxi SN, Kopel LS, Gaffin JM, Ozonoff A, et al. Food allergy and increased asthma morbidity in a school-based inner-city asthma study. J Allergy Clin Immunol Pract 2013;1:479e84. 30. Gaffin JM, Sheehan WJ, Morrill J, Cinar M, Borras Coughlin IM, Sawicki GS, et al. Tree nut allergy, egg allergy, and asthma in children. Clin Pediatr 2011;50:133e9. 31. Rentzos G, Johanson L, Sjolander S, Telemo E, Ekerljung L. Self-reported adverse reactions and IgE sensitization to common foods in adults with asthma. Clin Transl Allergy 2015;5: 25. 32. Sicherer SH, Furlong TJ, Munoz-Furlong A, Burks AW, Sampson HA. A voluntary registry for peanut and tree nut allergy: characteristics of the first 5149 registrants. J Allergy Clin Immunol 2001;108:128e32. 33. Sicherer SH, Burks AW, Sampson HA. Clinical features of acute allergic reactions to peanut and tree nuts in children. Pediatrics 1998;102. e6. 34. Bock SA, Munoz-Furlong A, Sampson HA. Further fatalities caused by anaphylactic reactions to food, 2001-2006. J Allergy Clin Immunol 2007;119:1016e8. 35. Pumphrey RS, Gowland MH. Further fatal allergic reactions to food in the United Kingdom, 1999-2006. J Allergy Clin Immunol 2007;119:1018e9. 36. Ebisawa M, Ito K, Fujisawa T. Japanese guidelines for food allergy 2017. Allergol Int 2017;66:248e64. 37. Wu TC, Tsai TC, Huang CF, Chang FY, Lin CC, Huang IF, et al. Prevalence of food allergy in Taiwan: a questionnaire-based survey. Intern Med J 2012;42:1310e5.
Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005
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Journal of Microbiology, Immunology and Infection xxx (xxxx) xxx
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.e-jmii.com
Original Article
Nut sensitization profile in Southern Taiwan Chih-Wei Cheng a, Yung-Chih Lin e, Bao-Ren Nong a,d, Po-Yen Liu a, Yung-Feng Huang a,d,f,*, Ling-Ying Lu c, Herng-Sheng Lee b a Department of Pediatrics, Kaohsiung Veterans General Hospital, Number 386, Dazhong 1st Road, Zuoying District, Kaohsiung City 813, Taiwan b Department of Pathology and Laboratory, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan c Division of Allergy, Immunology and Rheumatology, Department of Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan d Department of Pediatrics, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan e Department of Pediatrics, Taipei Veterans General Hospital, Taitung Branch, Taitung, Taiwan f Wellem Medical Group, Hangzhou, China
Received 27 May 2018; received in revised form 21 November 2018; accepted 12 December 2018
Available online - - -
KEYWORDS Peanut sensitization; Brazil nut sensitization; Specific IgE; Asthma; Atopic diseases
Abstract Background/purpose: To evaluate the relationship between serum-specific immunoglobulin E (IgE) to peanuts/tree nuts and their clinical manifestations in atopic diseases. Method: Serum from people with the classical symptoms of asthma, allergic rhinitis (AR), or atopic dermatitis (AD) was collected for the measurement of serum-specific IgE to peanuts, cashew nuts, Brazil nuts, almonds, and coconuts. Cases with possible sensitization to these nuts (serum specific IgE S 0.35 kU/L) were selected and their clinical relationships with physician-diagnosed asthma, allergic rhinitis, or atopic dermatitis were analyzed. Result: Compared with non-sensitization group, people with peanut/tree nut sensitization have higher prevalence of atopic dermatitis, but no such difference noted in the prevalence of allergic rhinitis. In the situation of asthma, people with sensitization to peanuts and Brazil nuts, but not other nuts, have higher prevalence of asthma than people without sensitization to any nut (p < 0.001 and p < 0.05, respectively). Binary logistic regression analysis also showed positive associations between peanut (OR: 1.164, p value Z 0.017) and Brazil nut (OR: 1.304, p value Z 0.055) sensitization and asthma. The associations between peanut and Brazil nut sensitization and asthma were independent of the prevalence of other atopic diseases. Conclusion: People in Asia may have less severe allergic effects as in Western countries, but sensitization to specific food allergens such as peanuts or Brazil nuts may predispose individuals to asthma, which could be helpful in diagnosis and deserves more attention than previously considered.
* Corresponding author. No.8 Lane 121 Bansin Road Banciao District, New Taipei City 22052, Taiwan. Fax: þ886 7 3468207. E-mail addresses: [email protected] (C.-W. Cheng), [email protected] (Y.-F. Huang). https://doi.org/10.1016/j.jmii.2018.12.005 1684-1182/Copyright ª 2019, Taiwan Society of Microbiology. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005
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C.-W. Cheng et al. Copyright ª 2019, Taiwan Society of Microbiology. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/bync-nd/4.0/).
Introduction Food allergy affects 3.44e6.40% of children and 7.65% of adults in Taiwan, with growing evidence of a worldwide increasing in its prevalence.1e6 The “major allergens” responsible for most significant reactions include milk, eggs, peanuts, tree nuts, shellfish, fish, wheat, and soy.6e8 Even though a population-based study indicated peanut and tree nut allergy and related adverse effects are relatively low in Asian populations,9e11 peanuts are still one of the most common food triggers in Taiwan.3,5 Over the past decades, both food allergy and atopic disorders have shown an increasing prevalence in children worldwide, and asthma is now one of the most common chronic disorders in Asian adults and children.12e16 In addition to the wellestablished linkage between eczema and food allergy,17 studies have also shown the association between food sensitization and the development and exacerbation of asthma. Increased asthma severity, hospitalization, and the use of corticosteroids are also correlated with food sensitization.18e21 Quantification of food-specific IgE by ImmunoCAP is now an available and reliable tool to predict possible food allergy without taking the risks of anaphylaxis after food challenges into account.22,23 In this study, we collected the data of specific IgE to different nuts and attempted to determine the relationship between food sensitization to peanuts or tree nuts and atopic diseases.
Methods Patients and samples People showed the classical symptoms of asthma, allergic rhinitis, or atopic dermatitis (detail clinical symptoms and signs were described in following section “clinical manifestations”), were enrolled from the outpatient department of Kaohsiung Veterans General Hospital, Taiwan, from January 2014 to April 2017. The serum was collected and specific IgE to peanuts, cashew nuts, Brazil nuts, almonds, and coconuts was measured by the Phadia ImmunoCAP system (ImmunoCAP specific IgE; Phadia, Inc, Uppsala, Sweden). The cut-off value of sensitization to a specific allergen was defined as food specific IgES0.35 kU/L.23
Clinical manifestations Data were collected through retrospective medical chart reviews, and diagnoses were made by board-certified doctors based on patient histories, clinical features and related criteria. Asthma was defined as per physician diagnosis and being symptomatic in the prior year of the survey. Atopic dermatitis was diagnosed by typical skin manifestations, pruritus, chronic or relapsing course, and personal/family
history of atopic diseases. The diagnosis of allergic rhinitis was based upon the presence of characteristic symptoms, suggestive clinical histories, and supportive findings on physical examination.
Statistical analysis Sigmaplot (Systat Software Inc., version 12.5, San Jose, CA, USA) and the SPSS statistics analysis package (SPSS for Windows, version 20.0, Chicago, IL, USA) were used to perform the statistical analysis. One-way ANOVA was used to analyze the differences between nut sensitization groups. Test of proportion, Z test, was utilized to calculate the difference in disease prevalence between groups. The binary logistic regression was used to analyze the association between specific IgE level and atopic diseases, the odds ratio (OR), the p value, and the 95% confidence interval (CI) of OR. A p value < 0.05 was considered statistically significant. The HosmereLemeshow test was used to verify if the binary logistic regression models were valid. The p value > 0.05 was considered the model is valid.
Results Three hundred and thirty-three patients were enrolled in this study. The age range was from 2 to 93 years old with the mean age 38.0 years old, and men comprised 37.8% of the study participants. More than half of patients had cutaneous and respiratory symptoms. There were 555 data of serum specific IgE, among them, 339 were considered as food sensitization based on their antigen specific IgE level (S0.35 kU/L). These included peanuts (n Z 124, 36.6%), cashew nuts (n Z 64, 18.9%), Brazil nuts (n Z 28, 8.3%), almonds (n Z 73, 21.5%), and coconuts (n Z 50, 14.7%), respectively. Another 216 samples were considered as non-sensitization to nuts according to the same criteria. The most common nut of sensitization was the peanut, and the least was Brazil nut. The specific IgE levels ranged from 0.35 to 47.5 kU/L (Fig. 1). Most specific IgE levels were around 0.35e10 kU/L, and the mean level was 3.00 kU/L (peanuts), 2.72 kU/L (cashew nuts), 2.09 kU/L (Brazil nuts), 2.07 kU/L (almonds), and 2.06 kU/L (coconuts), respectively. The distribution patterns were similar in different groups of nut sensitization. A few patients had extremely high specific IgE levels up to around 30e40 kU/L. There was no difference in specific IgE level noted between groups. For each group of nut sensitization, the prevalence of asthma was 39.52% for the peanuts, 12.50% for the cashew nuts, 21.43% for the Brazil nuts, 13.70% for the almonds, and 12.00% for the coconuts. The prevalence of asthma in non-sensitization group was 7.4%. Test of proportion, Z test, was introduced for statistical analysis. There are
Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005
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Nut sensitization profile in Southern Taiwan
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Figure 1. The serum specific IgE level was plotted with logarithmic scale. Each dot represents one sample. The horizontal line is the mean of each group.
significant differences in asthma prevalence of peanut or Brazil nut sensitization group and non-sensitization group, and the p values were <0.001 and < 0.05, respectively (Fig. 2). The relationship between diseases and specific IgE levels were estimated by using binary logistic regression analysis. There was a trend of positive correlations between asthma and specific IgE to different nuts (Table 1). The OR in binary logistic regression means the probability of asthma. With the serum-specific IgE increasing every one unit (kU/L), the possibility of asthma increases by ORfold. For Brazil nuts, as the serum-specific IgE level increases from 1 to 2 kU/L, the possibility of asthma increases 1.304 times. In these analyses, peanuts bore a strong correlation to asthma development when the specific IgE level increased (OR: 1.164, 95% CI: 1.027e1.319, p value Z 0.017). Brazil nuts group also showed a possible correlation between serum IgE level and asthma, although this lacked statistical significance. The HosmereLemeshow test was used to verify if the binary logistic regression models were valid. The p Z 0.122 for peanut and 0.425 for Brazil nut, both non-significant, means the regression results were valid. The prevalence of allergic rhinitis was 41.94% in the peanut sensitization group, 42.19% in the cashew nut group, 42.86% for Brazil nuts, 36.97% for almonds, 38.00% for coconuts, and 41.2% for non-sensitization group. There was no significant difference in the prevalence of allergic rhinitis, whether sensitization to nuts or not. For the situation of atopic dermatitis, the prevalence was 45.97%, 38.36%, 46.43%, 42.47%, 44% and 26.4, respectively. Higher
prevalence of atopic dermatitis was noted in nuts sensitization groups. Considering the association with nut sensitization, unlike the situation in asthma, there was no significant difference noted between different nuts sensitization groups, but significant difference was noted between sensitization and non-sensitization group (all p < 0.05 according to different nuts). Under the binary logistic regression model, there was no obvious positive correlation between specific IgE level and allergic rhinitis or atopic dermatitis, as shown in Table 1.
Discussions With the increasing prevalence of food sensitization1,5,24 and atopic diseases, the use of specific IgE to identify allergic conditions has increased. The goal of this study was to identify the relationship between specific IgE to nuts and atopic diseases. The Kaohsiung Veterans General Hospital is located in southern Taiwan, in a sub-tropical region. According to our knowledge, this is the first study to evaluate the relationship between nut sensitization and atopic diseases in a tropical area. In our data, there was no difference in specific IgE level distribution between population sensitization to different nuts. People with nut sensitization have higher asthma prevalence compared with non-sensitization group, especially those sensitized to peanuts (39.52%, 49/124 persons) and Brazil nuts (21.43%, 6/28 persons) (Fig. 2). Patients enrolled in this study also showed a much higher prevalence of atopic dermatitis than non-sensitization
Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005
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Figure 2.
The prevalence of asthma in each nut sensitization group.
Table 1 The binary logistic regression results between the level of specific IgE and atopic diseases development. Disease/Nuts
OR
95% CI
p value
Asthma
1.164 1.123 1.304 1.048 1.093 1.064 0.974 0.959 1.006 1.026 0.973 1.029 0.903 0.885 0.846
1.027e1.319 0.989e1.274 0.994e1.710 0.946e1.161 0.957e1.249 0.973e1.163 0.890e1.065 0.758e1.213 0.914e1.109 0.905e1.163 0.909e1.042 0.949e1.116 0.699e1.166 0.704e1.112 0.615e1.163
0.017 0.073 0.055 0.369 0.191 0.172 0.561 0.727 0.895 0.689 0.438 0.485 0.435 0.293 0.303
AR
AD
Peanuts Cashew Nuts Brazil Nuts Almonds Coconuts Peanuts Cashew Nuts Brazil Nuts Almonds Coconuts Peanuts Cashew Nuts Brazil Nuts Almonds Coconuts
OR Z odds ratio; CI Z confidence interval.
group. The binary logistic regression model also showed positive association between odds ratios of asthma development and level of specific IgE to peanuts or Brazil nuts (Table 1). The gold standard for the diagnosis of food allergy is the double-blind, placebo-controlled food challenge, but food
challenge can be time-consuming, and catastrophic to patients with potential danger.25,26 By using data from retrospective and prospective studies, it is possible to generate probability curves that depict the likelihood of patients with particular food-specific IgE reaction during a food challenge.22,23,26 The detection of specific IgE to certain food antigens has been shown to be predictive of symptomatic IgE-medicated food allergy. Illustrated by the example of peanuts, specific IgES0.35 kU/L could be considered as peanut sensitization and specific IgE as high as 13 kU/L could be diagnosed as food allergy with 96% of specificity.23 Quantification of specific IgE to certain food antigens would aid in the diagnosis of food sensitization or food allergy and decrease the necessity of food challenge. As a part of “atopic march”, the link between food allergy and infantile eczema has been well-established.17 The relationship between food allergy and respiratory manifestations of atopic disease has been less emphasized before, but evidences have emerged recently. Tariq et al. indicated egg allergy in infancy, especially when co-existing with eczema, increases respiratory allergic symptoms and aero-allergen sensitization in childhood.27 The study of Roberts et al. showed poor controlled asthma and food allergy are significant risk factors for life-threatening asthma.28 In France, Penard-Morand et al. found reported food allergy, food sensitization and skin prick-tested food allergy were all positively associated with asthma and allergic rhinitis. They concluded the relationship between food allergy and asthma or allergic rhinitis could be totally
Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005
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Nut sensitization profile in Southern Taiwan explained neither by existence of respiratory manifestations of food allergy nor by sensitization to aero-allergens. Instead, food allergy might intervene via other mechanisms than sensitization to aero-allergens in asthma and allergic rhinitis development.21 The following studies revealed not only strong linkage between asthma development and food allergy, but also that the severity and morbidity of asthma, and even healthcare utilization and medication use were associated with the severity and the numbers of food allergies.18,19,29 In addition to egg and milk allergy, which have been specifically implicated as risk factors for the development of asthma, both peanut allergy and tree nut allergy were also notorious culprits as determined in the literature.30,31 Food allergy alone could lead to the increased odds ratios of hospitalization (OR: 2.35, 95% CI: 1.30e4.24, p Z 0.005), and the need for the use of controller medication (OR: 1.99, 95% CI: 1.06e3.74, p Z 0.03).19,29 Increasing evidences imply food allergy is an important and independent risk factor for asthma, and is even irrespective of whether food allergy resolves.20 According to the study using the National Health Insurance database in Taiwan based on ICD-9 coding, the prevalence of asthma, allergic rhinitis, and atopic dermatitis were 2.9%, 11.3%, and 1.2%, respectively.16 Large international studies via questionnaires, ISAAC phase three study, between 2002 and 2003 disclosed the prevalence of asthma symptoms, allergic rhinoconjunctivitis symptoms, and eczema symptoms in Taiwan were 9.8%, 24.2%, and 6.7%, respectively.12 Compared with the findings of previous studies, our study showed much higher prevalence of asthma, allergic rhinitis, and atopic dermatitis in all nut sensitization groups and even nonsensitization group than in the general population. This further implied possible correlation between food allergy and atopic diseases as mentioned in previous studies. Although the population enrolled in this study was people with suspecting atopic diseases which would influence the interpretation, it is worth noting that people with peanut and Brazil nut sensitization had much higher asthma prevalence even within nut sensitization groups. No such difference was noted in the prevalence of allergic rhinitis and atopic dermatitis. These results suggested the relationship between asthma and peanut or Brazil nut sensitization is independent of the prevalence of other atopic diseases. Binary logistic regression analysis also revealed a positive association between nut sensitization and asthma, especially in the peanut group. These results suggested that sensitization to some specific foods, but not all, can be independent risk factors of asthma development. Peanut allergy deserves particular attentions in Western countries for its severe allergic reactions, which do not usually resolve spontaneously, and trace quantities of peanuts are enough to induce an allergic reaction.32,33 Based on data from food anaphylaxis registries, the peanut is the most common food trigger of fatal anaphylaxis in these communities.34,35 Unlike the growing prevalence and severe allergic reactions of peanuts in Western populations, some studies have revealed seafood and fish were mainly responsible for severe food allergy in Taiwanese and Asian populations.9,10 Peanuts and tree nuts are important food allergens to cause anaphylaxis in Westerners, but they also
5 cause severe reactions in patients in Asian regions.10 According to the Japanese food allergy guideline 201736, the frequency of anaphylactic shock due to peanut allergy was 13.2%. Similarly, peanut and tree nut allergies are not rare in Taiwan. According to a questionnaire-based study in Taiwan, shrimp (51.6%) and crab (34.0%) are the most common causes of severe food allergy, but peanuts still account for an important part (9.9%).37 Apart from anaphylaxis, peanut and tree nut allergies might play an important role in atopic diseases in Taiwan population as shown in our study. This study has some limitations. First, this was a single center study in southern Taiwan comprising a small sample size. For the geographic difference of food allergy, the results may be not applicable to other ethnicities. Instead, the emphasis of this study is on the fact that not only aerosensitization but also some food sensitization could be a risk factor in asthma development. Second, the samples were collected from people suspected of having atopic diseases. They might come to outpatient departments for their pre-existing atopic diseases and thereby cause the high prevalence of atopic diseases in our study. No data were acquired from the health population, and therefore these results may not apply to the general population, and should be interpreted with caution. The prevalence of food sensitization and likely food allergy, is increasing in patients with asthma and this is associated with increased healthcare-related expenditure. Sensitization to peanuts or Brazil nuts might predispose individuals to asthma. Caregivers should consider the analysis of food allergy for patients under standard medications for intractable asthma. Sensitization to specific food allergens may account for more attention in asthma prediction and diagnosis than previously considered.
Conflicts of interest The authors declare that they have no conflicts of interest relevant to the material discussed in this article.
Acknowledgments This study was funded by Kaohsiung Veterans General Hospital (VGHKS 106-040).
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Please cite this article as: Cheng C-W et al., Nut sensitization profile in Southern Taiwan, Journal of Microbiology, Immunology and Infection, https://doi.org/10.1016/j.jmii.2018.12.005