Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Anaphylaxis triggers in a large tertiary care hospital in Qatar: a retrospective study

Anaphylaxis triggers in a large tertiary care hospital in Qatar: a retrospective study Background: Anaphylaxis is a serious allergic disease that may lead to death if not immediately recognized and treated. Triggers of anaphylaxis including food, drugs, and insect stings can vary widely. The incidence of anaphylaxis seems to be affected by age, sex, atopy, and geographic location. This study aims to examine the common triggers of anaphylaxis in Qatar. Methods: A total of 1068 electronic medical records were audited using power chart system: 446 from the medical coding system of anaphylaxis and 622 from the epinephrine auto-injectors (EAIs) dispensed during January 2012– December 2017. Results: Of 1068 patients, 574 (53.5%) had anaphylaxis; male to female ratio was 1.2, and 300 patients (77.9%) were less than 10 years old. The common triggers were food (n = 316, 55.0%), insect stings (n = 161, 28.0%), and drugs (n = 103, 17.9%). Common anaphylaxis food triggers were nuts (n = 173, 30.1%), eggs (n = 89, 15.5%), and seafood (n = 72, 12.5%), and common anaphylaxis medication triggers were antibiotics (n = 49, 8.5%) and nonsteroidal anti-inflammatory drugs (n = 30, 5.2%). Interestingly, 135 anaphylactic patients (23.5%) were due to black ant stings. The anaphylaxis triggers varied significantly between children and adults. Among children (less than 10 years), three quarters of the events were triggered by food (223, 74.3%) while among adults (20–55 years), insect stings (n = 59, 43.0%) and drugs (n = 44, 32.0%) were dominant. Discussion: This is the first national study stratifying anaphylaxis triggers among different age groups in Qatar. This study will serve as a guide for clinical practice in allergy clinics in Qatar and will help to assess future trends of anaphylaxis in Qatar. Keywords: Anaphylaxis, Allergy, Triggers, Qatar Background Although it is difficult to characterize anaphylaxis Anaphylaxisisa serioussystemic allergic reaction that is incidence due to its transient acute nature and rapid in onset and may be fatal if not immediately recog- under-recognition especially in case of cutaneous symp- nized and treated [1–3]. Triggers of anaphylaxis vary widely toms absence (20% of the cases) [3, 5, 6]. Several studies and include food, drugs, and insect stings. Once triggered, from USA, UK, and Australia suggested that the inci- the disease manifests itself by compromising the function dence of anaphylaxis is on a gradual rise over the last of multiple organs, including skin (90%), respiratory (70%), two decades [7–14]. To estimate the incidence, preva- gastrointestinal (30–45%), cardiovascular (35%) and central lence, and triggers, scientists have used different meth- nervous system (10–15%) [2, 4]. Personal predisposition odologies including patients’ case reports [15–17], and family history of atopy usually worsen the course of international medical coding systems [7–9, 18–24], hos- anaphylaxis in affected subjects [2–4]. pital admission rates [11, 13, 25, 26], public surveys and epinephrine dispense records [10, 12, 21, 25, 27, 28]. These studies have demonstrated that distribution of * Correspondence: mariamali@hamad.qa anaphylaxis tends to fluctuate based on age, gender, race, Allergy and Immunology Unit, Hamad Medical Corporation, P.O. Box 3050, Doha, Qatar Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 2 of 8 geographical residence, and socioeconomic status of hypotension (minutes to several hours) after exposure to a involved subjects. likely allergen; or (3) reduced blood pressure after exposure Anaphylaxis was described in a few case-reports in to a known allergen (minutes to several hours). Generalized Qatar [15, 29–31], however, its triggers have not been Allergic Reaction (GAR) was identified as patients who thoroughly studied. The aim of this study is to retrospect- were exposed to triggers that resulted in symptoms of aller- ively estimate and describe the distribution of anaphylaxis gic reaction without fulfilling the clinical criteria of anaphyl- triggers in different age and gender groups in Qatar from axis. Patients with GAR may have underlying allergic January 2012 to December 2016. diseases such as asthma, atopic dermatitis, urticaria, angio- edema or allergic rhinitis. Anaphylaxis and GAR definitions Method were applied to the records that were reviewed. Demo- Data collection graphic information and clinical diagnosis of patients were Between January 2012–December 2016, electronic medical retrieved, reviewed, and documented anonymously, and records were reviewed retrospectively using Cerner power then sub-categorized to be analyzed based on gender, age, chart system. This includes patients admitted and regis- history of atopy, symptoms, and triggers. tered in Cerner power chart system with the International Classification of Diseases 10th revision-Australian Modifi- Triggers cation (ICD10-AM) and discharged with diagnostic codes Triggers were defined as etiological agents that may lead of anaphylaxis: T 78.0 (anaphylactic shock due to adverse to either GAR or anaphylaxis [1, 3] . Triggers were clas- food reactions), T 78.1 (other adverse food reactions, not sified into food, drugs, insect stings, or idiopathic fac- elsewhere classified), T78.2 (anaphylactic shock, unspeci- tors. All the triggers of allergic reactions and anaphylaxis fied), T80.5 (anaphylactic shock due to serum), or T88.6 were identified based on patient’s history of exposure to (anaphylactic shock due to adverse effect of correct drug the triggers and the circumstances accompanying the or medication properly administered) and patients who reactions that have been recognized and confirmed by had Epinephrine Auto-Injector (EAIs) dispensed from the treating physician. These details were documented Hamad General Hospital pharmacy (Fig. 1). by the treating physicians in the electronic medical records. When possible triggers of the reactions were Sample selection not clearly recognized by the patients or physicians, they The study was approved by Hamad Medical Corporation were classified to be idiopathic. (HMC) local ethics committee (IRB 17122/17). Anaphyl- axis was defined based on physician diagnosis and the clinical protocols of HMC that are in accordance with Statistical analysis the clinical criteria of anaphylaxis guidelines [32]. Our Data analysis was performed using Statistical Package for inclusion criteria patients with anaphylaxis were either Social Sciences (SPSS Chicago IL, USA). Groups were one of the following: (1) acute onset of illness (minutes compared using chi-square test and the Fisher’s exact test to several hours) with involvement of the skin, mucosal (two-tailed) replaced the chi-square in case of small tissue or both, and at least respiratory compromise or sample size, where the expected frequency is less than 5 in reduced blood pressure; (2) involvement of two or more: any of the cells. The level where P < 0.05 (two-tailed) was skin-mucosal, respiratory, gastrointestinal and/ or considered as the cut-off for significance. Fig. 1 Flowchart of the study design Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 3 of 8 Results are detailed in Table 2. Other triggers that contributed to Characteristics of the study population anaphylaxis were cold (3, 0.5%), latex (2, 0.3%), contrast Out of 1068 electronic medical records audited using media (2, 0.3%), exercises (1, 0.1%) and food-dependent Cerner power chart system; 446 inpatients registered exercise-induced anaphylaxis (1, 0.1%) (Table 2). with ICD-10 codes of anaphylaxis and 622 outpatients had EAIs dispensed. Five hundred seventy-four patients Age and gender variation in anaphylaxis (53.5%) had anaphylaxis; 315 (54.8%) were males and Insects’ stings, food, and drug were significantly different 300 (52.2%) were children less than 10 years old, 251 between the different age groups (P < 0.001), while only patients (43.7%) were Qatari, 162 patients (28.2%) were the food and insects’ stings showed significance among gen- non-Qatari Arabs, and 118 patients (20.5%) were Asian. der groups (P < 0.001). The nationality of patients with Personal history of asthma, atopic dermatitis, urticaria anaphylaxis showed no such significant difference in rela- and allergic rhinitis were determined in 208 (36.2%), 195 tion to anaphylaxis triggers (Additional file 1:Table S1). (33.9%), 179 (31.1%), and 81 (14.1%) respectively. The distribution of anaphylaxis and GAR among different One-fifth of the study population had a positive family age and gender groups is shown in Fig. 2. history of atopy (Table 1). Discussion Triggers This study stratifies anaphylaxis triggers among different Overall, triggers were not identified in 44 cases (7.6%) of age and gender groups and provides a profile of the anaphylaxis and five cases (3.7%) of GAR. Food accounted common allergens that trigger anaphylaxis, to alert clini- for 403 (37.7%), followed by insects’ stings 184 (17.2%) and cians and serve as a baseline to assess future trends of drugs 123 (11.5%). The common triggers of anaphylaxis anaphylaxis triggers in Qatar. We were able to identify Table 1 Characteristics of the study population Characteristic Total N = 1068 n (%) Anaphylaxis N = 574 n (%) GAR N = 132 n (%) P-value Age (Years) < 10 603 (56.3) 300 (52.2) 85 (64.3) 0.009 10–19 210 (19.7) 109 (18.9) 22 (16.6) 20–55 209 (19.6) 137 (23.8) 21 (15.9) >. 55 46 (4.3) 28 (4.8) 4 (3.0) Gender Male 612 (57.3) 315 (54.8) 83 (62.8) 0.095 Female 456 (42.7) 259 (45.2) 49 (37.1) Nationality, N = 1067 Qatari 438 (41.0) 251 (43.7) 63 (47.7) 0.009 Non-Qatari, Arab 303 (28.4) 162 (28.2) 25 (18.9) Asian 228 (21.4) 118 (20.5) 24 (18.1) Others 98 (9.2) 42 (7.3) 20 (15.1) Personal History Asthma 357 (36.4) 208 (36.2) 68 (51.5) < 0.001 Atopic dermatitis 326 (33.2) 195 (33.9) 66 (50) < 0.001 Urticaria/ angioedema 254 (25.9) 179 (31.1) 36 (27.2) 0.485 Allergic rhinitis 142 (14.5) 81 (14.1) 30 (22.7) 0.009 Family History, N = 123 Atopy 70 (56.9) 58 (10.1) 8 (6.1) 0.989 Anaphylaxis 6 (4.9) 5 (0.8) 1 (0.7) Consanguinity, N = 33 30 (90.9) 25 (4.3) 2 (1.5) 1.000 GAR generalized allergic reactions Chi-square for trend (linear by linear association) One patient had no listed nationality in the system Atopy includes asthma, atopic dermatitis, urticaria and allergic rhinitis *P-value is for Fischer test (exact significant 2-sided) Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 4 of 8 Table 2 Causative triggers of symptoms in the study population Causative triggers Total N = 1068 n (%) Anaphylaxis N = 574 n (%) GAR N = 132 n (%) P-value Food (All) 403 (37.7) 316 (55.0) 87 (65.9) < 0.001 Nuts 232 (21.7) 173 (30.1) 59 (44.6) < 0.001 Egg 113 (10.5) 89 (15.5) 24 (18.1) 0.171 Seafood 93 (8.7) 72 (12.5) 21 (15.9) 0.111 Peanuts 92 (8.6) 71 (12.3) 21 (15.9) 0.100 Cow’s milk 77 (7.2) 61 (10.6) 16 (12.1) 0.326 Sesame seeds 65 (6.1) 50 (8.7) 15 (11.3) 0.158 Wheat 38 (3.5) 35 (6.1) 3 (2.2) 0.130 Other food 150 (14.0) 126 (21.9) 24 (18.1) 0.933 Insects’ stings (All) 184 (17.2) 161 (28.0) 23 (17.4) 0.122 Black ant 153 (14.3) 135 (23.5) 18 (13.6) 0.101 Bee 3 (0.2) 3 (0.5) 0 (0.0) 1.000 Wasp 1 (0.1) 1 (0.1) 0 (0.0) 1.000 Unspecified 29 (2.7) 24 (4.1) 5 (3.7) 0.798 Drugs (All) 123 (11.5) 103 (17.9) 20 (16.2) 0.978 Antibiotics 58 (5.4) 49 (8.5) 9 (6.8) 0.883 Augmentin 19 (1.7) 16 (2.7) 3 (2.2) 1.000 Penicillin 14 (1.3) 11 (1.9) 3 (2.2) 0.484 Ceftriaxone 6 (0.5) 6 (1.0) 0 (0.0) 0.596 Amoxicillin 6 (0.5) 5 (0.8) 1 (0.7) 1.000 Other antibiotics 22 (2.0) 19 (3.3) 3 (2.2) 1.000 NSAID 36 (3.3) 30 (5.2) 6 (4.5) 0.938 Ibuprofen 28 (2.6) 23 (4.0) 5 (3.7) 0.794 Paracetamol 8 (0.7) 8 (1.3) 0 (0.0) 0.366 Diclofenac 8 (0.7) 7 (1.2) 1 (0.7) 1.000 Aspirin 3 (0.3) 3 (0.5) 0 (0.0) 1.000 Other NSAID 4 (0.3) 4 (0.6) 0 (0.0) 1.000 d * IvIg 4 (0.3) 4 (0.6) 0 (0.0) 1.000 Vaccines 3 (0.3) 3 (0.5) 0 (0.0) 1.000 Other drugs 41 (3.8) 35 (6.1) 6 (4.5) 0.779 Idiopathic (All) 49 (4.5) 44 (7.6) 5 (3.7) 0.245 Nuts included cashew, pistachio, tree nuts, coconuts and hazelnuts excluding peanuts which has been counted separately Other food included chickpeas, bean, lentil, strawberry, banana, kiwi, mango, chicken, beef, pineapple, apple, and watermelon NSAID non-steroidal anti-inflammatory drugs IvIg Intravenous immunoglobulin *P-value is for Fischer test (exact significant 2-sided) 574 cases of anaphylaxis out of 1068 records. Food was action plan and risk reduction. However, such avoidance the leading trigger of anaphylaxis in children regardless measures are neither easily nor strictly followed by of gender. Anaphylaxis induced by drugs and insects’ children of this age group [16, 17, 33]. stings was more common among female adults (Fig. 2). Anaphylaxis was common in two age/gender groups: Interestingly, 23.5% of patients had anaphylaxis by black male children (n = 224, 39.0%) and female adults (n =114, ants. 19.8%) (Fig. 2), which is consistent with other findings re- Our data showed a predominance of anaphylaxis ported by Alshami et al. where they found an incidence of among pediatrics (n = 300, 52.2%), which is reasonable anaphylaxis in pediatric emergency centers of 13.3 per since at a single time point anaphylaxis is initially diag- 100,000 visits with 69% of patients being males [34], and nosed at childhood, and relevant triggers avoidance is Mehdi et al. showed that the incidence among adults was recommended as preventive measures of a long-term 16.5 per 100,000 visits with 78% being females [35]. Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 5 of 8 Fig. 2 Distribution of anaphylaxis pattern among different age and gender groups. a Food triggers, b Insect stings triggers, c Drug triggers, d Idiopathic triggers Several studies in different ethnic groups showed similar In our patients’ cohort, we observed that the association age and gender distribution of anaphylaxis among differ- between the development of anaphylaxis compared to GAR ent age/gender groups; for example, an epidemiological and the national origin were statistically significant (p-value study based on measuring the anaphylaxis rates in emer- = 0.009) (Table 1). For instance, “Non-Qatari Arabs” had gency department visits in hospitals across Florida, USA, relatively higher prevalence of anaphylaxis compared to reported that the highest anaphylaxis incidence rate was GAR while “Others” such as European, American and among the youngest males (8.2/100,000 visits) and the African had relatively lower prevalence of anaphylaxis com- adult females (10.9/100,000 visits) [20]. Similar to this, pared to GAR. Such differences in the rates of anaphylaxis findings from the Rochester epidemiology project from compared to GAR associated with ethnic and national 1990 through 2000 showed that age-specific incidence rate groups can be explained by a number of factors, including of anaphylaxis was the highest for ages 0–19 years [8]. genetic and environmental exposure. Qatar is a melting pot Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 6 of 8 of hundreds of nationalities of migrant workers [36]that were of severe grade and manifested mainly in the form of may have different genetic predisposition to allergy and anaphylaxis [46]. This study suggested that the sesame seed anaphylaxis. In addition to potential differences in the gen- is the “Middle Eastern” peanut [46]. etic make-up, different life style and dietary patterns as well Anaphylaxis and GAR attributable to Hymenoptera as differential prevalence of illnesses and use of varying stings in our study demonstrated predominance in fe- medications may be some of the factors that may or may male adults (n = 50, 45.9%) and male children (n = 30, not contribute to such differences [18, 23]. In general, ana- 40.0%) (Fig. 1b). Interestingly, 135 anaphylactic patients phylaxis was common [7–9, 20, 21], more associated with (23.5%) developed anaphylaxis by the sting of black ant repeated use of epinephrine [27]and more fatal[23]among which is a widespread ant in tropical Africa and the Caucasians compared to Black, Latino/Hispanic and Asian Middle East and is a native insect in Arabian Desert ethnicities. In contrast, Mahdavinia et al. (2017) reported countries, including Qatar [47, 48]. Allergic reactions that Caucasians had a lower rate of food allergy associated due to black ant stings range from pain with local anaphylaxis than African American and Hispanic children itching at the sting site to severe anaphylactic shock. [37]. Additionally, Buka et al. (2015) reported that AlAnazi et al. (2009) showed that the diversity of mani- Caucasians had less incidence, and were less likely to festation and human response to black ant stings in four present with severe anaphylactic symptoms than South cases encountered in Al Riyadh, the capital city of Saudi Asian British children living in Birmingham [38]. Arabia, and three patients were adult females [49]. In Personal history of atopy for asthma (n = 208, p < 0.001), contrast to our findings, lower prevalence of black ant atopic dermatitis (n = 195, p < 0.001) and allergic rhinitis induced anaphylaxis was reported in Saudi Arabia (3.2%) (n =81, p = 0.009) were noted among patients with ana- [14], and Singapore (12.9%) [50]. The unreported inci- phylaxis in Qatar (Table 1), and 56.9% cases had positive dence of black Samsum ant induced anaphylaxis was family history (Table 1). Although other studies showed no recognized in Iran where most stings result in mild aller- such significant association between atopy and anaphylaxis gic reactions [51]. However, in United Arab Emirates, [39, 40], atopy was frequently visualized as a risk factor that 4 deaths were recorded after the sting of this ant [52]. might worsen the clinical outcome of anaphylaxis [8, 18, Several studies attribute diversity of symptoms to the anti- 19, 21, 24, 41–43]. However, several studies stated that genicity variation of black ants’ toxin composition accord- anaphylaxis was common among patients with atopic dis- ing to geographical regions [51, 53]. Anaphylaxis in eases. In comparison to our study, different distribution of Najran, a city in southwestern Saudi Arabia, was triggered atopic diseases was observed [8, 18, 19, 21, 24, 41–43]. by a different species of black ant, Solenopsis richteri,in Our results showed that regardless of gender, food was non-Saudi expatriates (1997–1999) [54]. A Turkish retro- the culprit for anaphylaxis in children less than 10 years spective review defined prevalence of Hymenoptera stings (Fig. 2a). The major causative triggers of food-induced anaphylaxis among adult patients, however, the causative anaphylaxis in Qatar were nuts and eggs, a finding that triggers were mainly honey bees and different wasp was consistent with a Saudi finding reported in 2015 species [55]. In contrary to Qatar, the later Turkish study [14]. Peanuts, a major trigger of food-related anaphylaxis showed a predominance of Hymenoptera induced ana- in the United States [7, 9, 22], is ranked in the fourth phylaxis among male adults (57.1%) [55]. In light of the position after seafood in Qatar. In a prospective cohort absence of studies published about black Samsum ant study conducted in Qatar from 2007 to 2010, anaphyl- abundance, distribution, and its toxin antigenicity in axis induced by cow’s milk proteins (CMP) was found in Qatar, our results flag it as a public health hazard in Qatar 10 children out of 38 allergic subjects and suggested owing to its strong association with anaphylaxis. camel milk as a safer alternative choice after being experi- A key strength of this work includes the fact that mentally tested [30, 31]. With a larger study population, Hamad General Hospital, a member of Hamad Medical anaphylaxis induced by cow’s milk was accounted for 61 Corporation, is the only medical facility that dispenses (10.6%) from 2012 to 2016. In comparison, the prevalence EAIs in Qatar. Therefore, using dispensed (EAI) records of CMP anaphylaxis resulted in 6–9% of children hospital of outpatients in combination with medical coding system and emergency admission in the USA [7, 19, 21] and 10% (ICD-10 AM) of anaphylaxis for inpatients would be an in the UK [44]. CMP anaphylaxis accounted for 8 fatalities accurate estimation of the prevalence of anaphylaxis in in UK children during the period from 1992 to 2012 [13]. Qatar. Although, EAI dispense records were available for Our data showed that sesame seed accounted for 8.7% of 1year only(January – December 2016), EAIs as a refilled anaphylaxis cases in Qatar (Table 2). However, as a global drug included dispense records of previous years. allergen, sesame seed is affecting approximately 0.1% of North American population and is the third common food Conclusion allergen in Israel [45]. In Lebanon, a cross-sectional study Our study provides new data regarding the frequency of showed that allergic reactions triggered by sesame seed anaphylaxis in our geographical region; however, it is Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 7 of 8 prone to reporting bias due to its retrospective nature Ethics approval and consent to participate Ethical Approval: This retrospective study was ethically approved by the IRB and reliance on physician documentation. Besides that, committee of Medical Research Centre- Hamad Medical Corporation (IRB- we had 364 medical records (34.1%) with missing data HMC) (IRB#17122/17) with expedited status. For more information, kindly or incomplete charts and we cannot assume them as be- contact irb@hamad.qa, Tel: 00974–44,390,614. ing negative since there is the possibility of underreport- Consent to participate ing by physicians. Therefore, the presenting data should The study was a retrospective study. IRB-HMC approved the study for waiver be interpreted with caution stating that “within the of consent; provided that the methods used to protect patient confidentiality boundary of available data” registered in Cerner were judged to be adequate. power chart system and out of 1068 subjects, 574 Consent for publication (53.5%) patients had a definite diagnosis of anaphylaxis Not applicable. (2012–2016). Further studies are needed to confirm the medical diagnosis of the missing cases using another Competing interests method. This study will serve as a platform for clinicians The authors declare that they have no competing interests. in the allergy clinics in Qatar to improve patient care and for further epidemiological studies for understand- Publisher’sNote ing more about the prevalence of anaphylaxis in Qatar. Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Our data might provide the baseline for assessing future trends. We would recommend integrating entomology, Author details bioecology and medicine points of view to study black Biomedical Science Department, College of Health Science, Qatar University, P.O. Box 2713, Doha, Qatar. Allergy and Immunology Unit, Hamad Medical ant anaphylaxis in Qatar. Corporation, P.O. Box 3050, Doha, Qatar. College of Health Science, Qatar University, P.O. Box 2713, Doha, Qatar. Department, College of Health Additional file Science, Qatar University, P.O. Box 2713, Doha, Qatar. Allergy & Clinical Immunology Unit, Hamad Medical Corporation, P.O. Box 3050, Doha, Qatar. Pharmacy Department, Women’s Hospital, Hamad Medical Corporation, P.O. Additional file 1: Table S1. Anaphylactic patterns variation in relation Box 3050, Doha, Qatar. Hamad Medical Corporation, P.O. Box 3050, Doha, to age, gender and nationality. row percentage. Table S2. Symptoms of Qatar. the study population. (DOCX 19 kb) Received: 26 March 2018 Accepted: 26 July 2018 Abbreviations CMP: Cow’s milk proteins; EAIs: Epinephrine Auto-injectors; GAR: Generalized Allergic Reaction; HMC: Hamad Medical Corporation; ICD-10 AM: International References Classification of Diseases 10th revision-Australian Modification; IVIG: Intravenous 1. Keet C. Recognition and management of food-induced anaphylaxis. Pediatr Immunoglobulin; NSAID: Non-Steroidal Anti-Inflammatory Drugs; SPSS: Statistical Clin N Am. 2011;58(2):377–88. x Package for Social Sciences 2. Lee JK, Vadas P. Anaphylaxis: mechanisms and management. Clin Exp Allergy. 2011;41(7):923–38. 3. Simons FE, Ardusso LR, Bilò MB, Cardona V, Ebisawa M, El-Gamal YM, et al. Acknowledgements International consensus on (ICON) anaphylaxis. World Allergy Organ J. We would like to express our thanks to Dr. Dorra Gharbi and Mrs. Blessing 2014;7(1):9. Reena Dason for their assistance in data collection. 4. Boyce JA, Assa'ad A, Burks AW, Jones SM, Sampson HA, Wood RA, et al. Guidelines for the diagnosis and Management of Food Allergy in the Funding United States: summary of the NIAID-sponsored expert panel report. J No funds or financial supports were granted for this research work. Allergy Clin Immunol. 2010;126(6):1105–18. We received no sources of any outside support of the project. 5. Cox LS, Sanchez-Borges M, Lockey RF. World Allergy Organization Systemic Allergic Reaction Grading System: Is a Modification Needed? J Allergy Clin Availability of data and materials Immunol Pract. 2017;5(1):58–62.e5. The datasets used and/or analysed during the current study are available 6. Muraro A, Roberts G, Worm M, Bilò MB, Brockow K, Fernández Rivas M, et al. from the corresponding author on reasonable request. Anaphylaxis: guidelines from the European academy of allergy and clinical immunology. Allergy. 2014;69(8):1026–45. Authors’ contributions 7. Parlaman JP, Oron AP, Uspal NG, DeJong KN, Tieder JS. Emergency and We have participated sufficiently in the intellectual content, conception and Hospital Care for Food-Related Anaphylaxis in children. Hosp Pediatr. 2016; design of this work or the analysis and interpretation of the data (when 6(5):269–74. applicable), as well as the writing of the manuscript, to take public responsibility 8. Decker WW, Campbell RL, Manivannan V, Luke A, St Sauver JL, Weaver A, et for it and have agreed to have our name listed as contributors. Mainly, al. The etiology and incidence of anaphylaxis in Rochester, Minnesota: a TA collected data of EAIs and ICD-10 codes, analyzed the data and report from the Rochester epidemiology project. J Allergy Clin Immunol. wrote the maniscript as part of her master degree thesis, MAA and TA 2008;122(6):1161–5. designed the overall study and was a mjor contributor in the manscript, 9. Michelson KA, Monuteaux MC, Neuman MI. Variation and trends in LT guided the statistical analysis of the data and contributed to review anaphylaxis Care in United States Children's hospitals. Acad Emerg Med. of the manuscribt, RK analyzed the data using SPSS. SK reviewed collected data 2016;23(5):623–7. from power chart system for accuracy and helped in the final manuscribt review, 10. Diwakar L, Cummins C, Ryan R, Marshall T, Roberts T. Prescription rates of WE retrieved EAIs dispense list, reviewed collected data and helped in the final adrenaline auto-injectors for children in UK general practice: a retrospective manuscribt review, AND HZ H and HMM reviewed the maniscript critically several cohort study. Br J Gen Pract. 2017;67(657):e300–e5. times and helped during most of the steps. Please refere to above contribution 11. Gibbison B, Sheikh A, McShane P, Haddow C, Soar J. Anaphylaxis admissions table for further details of each contributor. All authors read and approved the to UK critical care units between 2005 and 2009. Anaesthesia. 2012;67(8): final manuscript. 833–9. Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 8 of 8 12. Sheikh A, Hippisley-Cox J, Newton J, Fenty J. Trends in national incidence, 36. Statistics Authority. Qatar Population Status 376 2012: Three Years After lifetime prevalence and adrenaline prescribing for anaphylaxis in England. J Launching the Population Policy, State of Qatar. https://www.ppc.gov.qa/ R Soc Med. 2008;101(3):139–43. en/Pages/default.aspx. 13. Turner PJ, Gowland MH, Sharma V, Ierodiakonou D, Harper N, Garcez T, et al. 37. Mahdavinia M, Fox SR, Smith BM, James C, Palmisano EL, Mohammed Increase in anaphylaxis-related hospitalizations but no increase in fatalities: A, et al. Racial Differences in Food Allergy Phenotype and Health Care an analysis of United Kingdom national anaphylaxis data, 1992–2012. J Utilization among US Children. J Allergy Clin Immunol Pract. 2017;5(2): Allergy Clin Immunol. 2015;135(4):956–63.e1. 352–7.e1. 38. Buka RJ, Crossman RJ, Melchior CL, Huissoon AP, Hackett S, Dorrian S, et al. 14. Sheikh F, Amin R, Rehan Khaliq AM, Al Otaibi T, Al Hashim S, Al GS. First Anaphylaxis and ethnicity: higher incidence in British south Asians. Allergy. study of pattern of anaphylaxis in a large tertiary care hospital in Saudi 2015;70(12):1580–7. Arabia. Asia Pac Allergy. 2015;5(4):216–21. 39. Ganapathy S, Lwin Z, Ting DH, Goh LS, Chong SL. Anaphylaxis in children: 15. Mobayed HM, Ali A-NM. Two cases of food-dependent exercise-induced experience of 485 episodes in 1,272,482 patient attendances at a tertiary anaphylaxis with different culprit foods. Ann Thorac Med. 2014;9(1):42–4. Paediatric emergency department from 2007 to 2014. Ann Acad Med 16. Alsalamah M, Makhajia M, Somers G, Marcon M, Hummel D, Upton J. Singap. 2016;45(12):542–8. Anaphylaxis to milk after elimination diet for eosinophilic gastrointestinal 40. Rebelo Gomes E, Geraldes L, Gaspar Â, Malheiro D, Cadinha S, Abreu C, et disease. Am J Gastroenterol. 2016;111(5):752–3. al. Hypersensitivity reactions to nonsteroidal anti-inflammatory drugs 17. Zapatero L, Baeza ML, Sierra Z, Molero MI. Anaphylaxis by fruits of the among adults: clinical features and risk factors for diagnosis confirmation. Fagaceae family: acorn and chestnut. Allergy. 2005;60(12):1542. Int Arch Allergy Immunol. 2016;171(3–4):269–75. 18. Taylor-Black S, Wang J. The prevalence and characteristics of food 41. Orhan F, Canitez Y, Bakirtas A, Yilmaz O, Boz AB, Can D, et al. Anaphylaxis in allergy in urban minority children. Ann Allergy Asthma Immunol. Turkish children: a multi-Centre, retrospective, case study. Clin Exp Allergy. 2012;109(6):431–7. 2011;41(12):1767–76. 19. Huang F, Chawla K, Järvinen KM, Nowak-Węgrzyn A. Anaphylaxis in a New 42. Al-Hammadi S, Zoubeidi T, Al-Maskari F. Predictors of childhood food York City pediatric emergency department: triggers, treatments, and allergy: significance and implications. Asian Pac J Allergy Immunol. outcomes. J Allergy Clin Immunol. 2012;129(1):162–8.e1–3. 2011;29(4):313–7. 20. Harduar-Morano L, Simon MR, Watkins S, Blackmore C. A population-based 43. Jares EJ, Baena-Cagnani CE, Sanchez-Borges M, Ensina LF, Arias-Cruz A, epidemiologic study of emergency department visits for anaphylaxis in Gomez M, et al. Drug-induced anaphylaxis in Latin American countries. J Florida. J Allergy Clin Immunol. 2011;128(3):594–600.e1. Allergy Clin Immunol Pract. 2015;3(5):780–8. 21. Rudders SA, Banerji A, Corel B, Clark S, Camargo CA. Multicenter study of 44. Capps JA, Sharma V, Arkwright PD. Prevalence, outcome and pre-hospital repeat epinephrine treatments for food-related anaphylaxis. Pediatrics. management of anaphylaxis by first aiders and paramedical ambulance staff 2010;125(4):e711–8. in Manchester, UK. Resuscitation. 2010;81(6):653–7. 22. Michelson KA, Monuteaux MC, Neuman MI. Glucocorticoids and Hospital 45. Adatia A, Clarke AE, Yanishevsky Y, Ben-Shoshan M. Sesame allergy: current Length of Stay for Children with Anaphylaxis: A Retrospective Study. J perspectives. J Asthma Allergy. 2017;10:141–51. Pediatr. 2015;167(3):719–24.e1–3. 46. Irani C, Maalouly G, Germanos M, Kazma H. Food allergy in Lebanon: is sesame 23. Jerschow E, Lin RY, Scaperotti MM, McGinn AP. Fatal anaphylaxis in the seed the “middle eastern” peanut. World Allergy Organ J. 2011;4(1):1–3. United States, 1999–2010: temporal patterns and demographic associations. 47. Wetterer JK. Geographic spread of the samsum or sword ant, Pachycondyla J Allergy Clin Immunol. 2014;134(6):1318–28.e7. (Brachyponera) sennaarensis (Hymenoptera: Formicidae). Myrmecological 24. Lertnawapan R, Maek-a-nantawat W. Anaphylaxis and biphasic phase in News. 2013;18:13–8. Thailand: 4-year observation. Allergol Int. 2011;60(3):283–9. 48. Al-Khalifa MS, Mashaly AM, Siddiqui MI, Al-Mekhlafi FA. Samsum ant, 25. Järvinen KM, Amalanayagam S, Shreffler WG, Noone S, Sicherer SH, Brachyponera sennaarensis (Formicidae: Ponerinae): distribution and Sampson HA, et al. Epinephrine treatment is infrequent and biphasic abundance in Saudi Arabia. Saudi J Biol Sci. 2015;22(5):575–9. reactions are rare in food-induced reactions during oral food challenges in 49. AlAnazi M, AlAshahrani M, AlSalamah M. Black ant stings caused by children. J Allergy Clin Immunol. 2009;124(6):1267–72. Pachycondyla sennaarensis: a significant health hazard. Annals of Saudi 26. Meng J, Rotiroti G, Burdett E, Lukawska JJ. Anaphylaxis during general Medicine. 2009;29(3):207–11. anaesthesia: experience from a drug allergy Centre in the UK. Acta 50. Thong BY, Leong KP, Chng HH. Insect venom hypersensitivity: experience in Anaesthesiol Scand. 2017;61(3):281–9. a clinical immunology/allergy service in Singapore. Singap Med J. 2005; 27. Manivannan V, Campbell RL, Bellolio MF, Stead LG, Li JT, Decker WW. 46(10):535–9. Factors associated with repeated use of epinephrine for the treatment 51. Nikbakhtzadeh MRAK, Tirgari S. Bioecology and chemical diversity of of anaphylaxis. Ann Allergy Asthma Immunol. 2009;103(5):395–400. abdominal glands in the iranian samsum ant Pachycondyla sennaarensis 28. Cardona V, Ferré-Ybarz L, Guilarte M, Moreno-Pérez N, Gómez-Galán C, (Formicidae: Ponerinae). J Venom Anim Toxins Incl Trop Dis. 2009;15(3): Alcoceba-Borràs E, et al. Safety of adrenaline use in anaphylaxis: a 509–26. multicentre register. Int Arch Allergy Immunol. 2017;173(3):171–7. 52. Dib G, Guerin B, Banks WA, Leynadier F. Systemic reactions to the Samsum 29. Mobayed H, Ibrahim W, Al-Nesf M. Delayed clavulanic acid-induced ant: An IgE-mediated hypersensitivity. Journal of Allergy and Clinical anaphylaxis in a patient undergoing bariatric surgery. Ann Allergy Asthma Immunology. 1995;96(4):465–72. Immunol. 2014;113(3):324–5. 53. Akbarzadeh MN K, Tirgari S, Abaei MR. Medical Importnace of Fire Ant 30. Ehlayel M, Bener A, Abu Hazeima K, Al-Mesaifri F. Camel milk is a safer Pachycondyla sennaarensis (Hymenoptera: Formicidae) in Iranshahr and choice than goat milk for feeding children with cow milk allergy. ISRN Sarbaz Counties, Southeastern of Iran. J Med Sci. 2006;6:866–9. Allergy. 2011;2011:391641. 54. Khan SA, Shelleh HH, Khan LA, Shah H. Black fire ant (Solenopsis richteri) 31. Ehlayel MS, Hazeima KA, Al-Mesaifri F, Bener A. Camel milk: an alternative for sting producing anaphylaxis: a report of 10 cases from Najran. Ann Saudi cow's milk allergy in children. Allergy Asthma Proc. 2011;32(3):255–8. Med. 1999;19(5):462–4. 32. Simons FER, Ardusso LRF, Bilò MB, El-Gamal YM, Ledford DK, Ring J, et al. 55. Gelincik A, Demirtürk M, Yılmaz E, Ertek B, Erdogdu D, Çolakoğlu B, et al. World allergy organization guidelines for the assessment and Management Anaphylaxis in a tertiary adult allergy clinic: a retrospective review of 516 of Anaphylaxis. World Allergy Organ J. 2011;4(2):13–37. patients. Ann Allergy Asthma Immunol. 2013;110(2):96–100. 33. Boyano-Martínez T, García-Ara C, Pedrosa M, Díaz-Pena JM, Quirce S. Accidental allergic reactions in children allergic to cow's milk proteins. J Allergy Clin Immunol. 2009;123(4):883–8. 34. Alshami A, Adeli M, Alyafei K, Nisar S. Anaphylaxis presenting to the Pediatric Emergency Centers in Qatar. J Allergy Clin Immunol. 2018; 141(2):AB156. 35. Adeli M, Alyafei K, Chaudhry SI, Nisar S. Incidence, Etiology and characteristics of adult onset anaphylaxis in Qatar. J Allergy Clin Immunol. 2018;141(2):AB161. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png World Allergy Organization Journal Springer Journals

Anaphylaxis triggers in a large tertiary care hospital in Qatar: a retrospective study

Loading next page...
 
/lp/springer-journals/anaphylaxis-triggers-in-a-large-tertiary-care-hospital-in-qatar-a-sLvQqAERdV

References (60)

Publisher
Springer Journals
Copyright
Copyright © 2018 by The Author(s).
Subject
Medicine & Public Health; Allergology; Immunology
eISSN
1939-4551
DOI
10.1186/s40413-018-0200-9
Publisher site
See Article on Publisher Site

Abstract

Background: Anaphylaxis is a serious allergic disease that may lead to death if not immediately recognized and treated. Triggers of anaphylaxis including food, drugs, and insect stings can vary widely. The incidence of anaphylaxis seems to be affected by age, sex, atopy, and geographic location. This study aims to examine the common triggers of anaphylaxis in Qatar. Methods: A total of 1068 electronic medical records were audited using power chart system: 446 from the medical coding system of anaphylaxis and 622 from the epinephrine auto-injectors (EAIs) dispensed during January 2012– December 2017. Results: Of 1068 patients, 574 (53.5%) had anaphylaxis; male to female ratio was 1.2, and 300 patients (77.9%) were less than 10 years old. The common triggers were food (n = 316, 55.0%), insect stings (n = 161, 28.0%), and drugs (n = 103, 17.9%). Common anaphylaxis food triggers were nuts (n = 173, 30.1%), eggs (n = 89, 15.5%), and seafood (n = 72, 12.5%), and common anaphylaxis medication triggers were antibiotics (n = 49, 8.5%) and nonsteroidal anti-inflammatory drugs (n = 30, 5.2%). Interestingly, 135 anaphylactic patients (23.5%) were due to black ant stings. The anaphylaxis triggers varied significantly between children and adults. Among children (less than 10 years), three quarters of the events were triggered by food (223, 74.3%) while among adults (20–55 years), insect stings (n = 59, 43.0%) and drugs (n = 44, 32.0%) were dominant. Discussion: This is the first national study stratifying anaphylaxis triggers among different age groups in Qatar. This study will serve as a guide for clinical practice in allergy clinics in Qatar and will help to assess future trends of anaphylaxis in Qatar. Keywords: Anaphylaxis, Allergy, Triggers, Qatar Background Although it is difficult to characterize anaphylaxis Anaphylaxisisa serioussystemic allergic reaction that is incidence due to its transient acute nature and rapid in onset and may be fatal if not immediately recog- under-recognition especially in case of cutaneous symp- nized and treated [1–3]. Triggers of anaphylaxis vary widely toms absence (20% of the cases) [3, 5, 6]. Several studies and include food, drugs, and insect stings. Once triggered, from USA, UK, and Australia suggested that the inci- the disease manifests itself by compromising the function dence of anaphylaxis is on a gradual rise over the last of multiple organs, including skin (90%), respiratory (70%), two decades [7–14]. To estimate the incidence, preva- gastrointestinal (30–45%), cardiovascular (35%) and central lence, and triggers, scientists have used different meth- nervous system (10–15%) [2, 4]. Personal predisposition odologies including patients’ case reports [15–17], and family history of atopy usually worsen the course of international medical coding systems [7–9, 18–24], hos- anaphylaxis in affected subjects [2–4]. pital admission rates [11, 13, 25, 26], public surveys and epinephrine dispense records [10, 12, 21, 25, 27, 28]. These studies have demonstrated that distribution of * Correspondence: mariamali@hamad.qa anaphylaxis tends to fluctuate based on age, gender, race, Allergy and Immunology Unit, Hamad Medical Corporation, P.O. Box 3050, Doha, Qatar Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 2 of 8 geographical residence, and socioeconomic status of hypotension (minutes to several hours) after exposure to a involved subjects. likely allergen; or (3) reduced blood pressure after exposure Anaphylaxis was described in a few case-reports in to a known allergen (minutes to several hours). Generalized Qatar [15, 29–31], however, its triggers have not been Allergic Reaction (GAR) was identified as patients who thoroughly studied. The aim of this study is to retrospect- were exposed to triggers that resulted in symptoms of aller- ively estimate and describe the distribution of anaphylaxis gic reaction without fulfilling the clinical criteria of anaphyl- triggers in different age and gender groups in Qatar from axis. Patients with GAR may have underlying allergic January 2012 to December 2016. diseases such as asthma, atopic dermatitis, urticaria, angio- edema or allergic rhinitis. Anaphylaxis and GAR definitions Method were applied to the records that were reviewed. Demo- Data collection graphic information and clinical diagnosis of patients were Between January 2012–December 2016, electronic medical retrieved, reviewed, and documented anonymously, and records were reviewed retrospectively using Cerner power then sub-categorized to be analyzed based on gender, age, chart system. This includes patients admitted and regis- history of atopy, symptoms, and triggers. tered in Cerner power chart system with the International Classification of Diseases 10th revision-Australian Modifi- Triggers cation (ICD10-AM) and discharged with diagnostic codes Triggers were defined as etiological agents that may lead of anaphylaxis: T 78.0 (anaphylactic shock due to adverse to either GAR or anaphylaxis [1, 3] . Triggers were clas- food reactions), T 78.1 (other adverse food reactions, not sified into food, drugs, insect stings, or idiopathic fac- elsewhere classified), T78.2 (anaphylactic shock, unspeci- tors. All the triggers of allergic reactions and anaphylaxis fied), T80.5 (anaphylactic shock due to serum), or T88.6 were identified based on patient’s history of exposure to (anaphylactic shock due to adverse effect of correct drug the triggers and the circumstances accompanying the or medication properly administered) and patients who reactions that have been recognized and confirmed by had Epinephrine Auto-Injector (EAIs) dispensed from the treating physician. These details were documented Hamad General Hospital pharmacy (Fig. 1). by the treating physicians in the electronic medical records. When possible triggers of the reactions were Sample selection not clearly recognized by the patients or physicians, they The study was approved by Hamad Medical Corporation were classified to be idiopathic. (HMC) local ethics committee (IRB 17122/17). Anaphyl- axis was defined based on physician diagnosis and the clinical protocols of HMC that are in accordance with Statistical analysis the clinical criteria of anaphylaxis guidelines [32]. Our Data analysis was performed using Statistical Package for inclusion criteria patients with anaphylaxis were either Social Sciences (SPSS Chicago IL, USA). Groups were one of the following: (1) acute onset of illness (minutes compared using chi-square test and the Fisher’s exact test to several hours) with involvement of the skin, mucosal (two-tailed) replaced the chi-square in case of small tissue or both, and at least respiratory compromise or sample size, where the expected frequency is less than 5 in reduced blood pressure; (2) involvement of two or more: any of the cells. The level where P < 0.05 (two-tailed) was skin-mucosal, respiratory, gastrointestinal and/ or considered as the cut-off for significance. Fig. 1 Flowchart of the study design Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 3 of 8 Results are detailed in Table 2. Other triggers that contributed to Characteristics of the study population anaphylaxis were cold (3, 0.5%), latex (2, 0.3%), contrast Out of 1068 electronic medical records audited using media (2, 0.3%), exercises (1, 0.1%) and food-dependent Cerner power chart system; 446 inpatients registered exercise-induced anaphylaxis (1, 0.1%) (Table 2). with ICD-10 codes of anaphylaxis and 622 outpatients had EAIs dispensed. Five hundred seventy-four patients Age and gender variation in anaphylaxis (53.5%) had anaphylaxis; 315 (54.8%) were males and Insects’ stings, food, and drug were significantly different 300 (52.2%) were children less than 10 years old, 251 between the different age groups (P < 0.001), while only patients (43.7%) were Qatari, 162 patients (28.2%) were the food and insects’ stings showed significance among gen- non-Qatari Arabs, and 118 patients (20.5%) were Asian. der groups (P < 0.001). The nationality of patients with Personal history of asthma, atopic dermatitis, urticaria anaphylaxis showed no such significant difference in rela- and allergic rhinitis were determined in 208 (36.2%), 195 tion to anaphylaxis triggers (Additional file 1:Table S1). (33.9%), 179 (31.1%), and 81 (14.1%) respectively. The distribution of anaphylaxis and GAR among different One-fifth of the study population had a positive family age and gender groups is shown in Fig. 2. history of atopy (Table 1). Discussion Triggers This study stratifies anaphylaxis triggers among different Overall, triggers were not identified in 44 cases (7.6%) of age and gender groups and provides a profile of the anaphylaxis and five cases (3.7%) of GAR. Food accounted common allergens that trigger anaphylaxis, to alert clini- for 403 (37.7%), followed by insects’ stings 184 (17.2%) and cians and serve as a baseline to assess future trends of drugs 123 (11.5%). The common triggers of anaphylaxis anaphylaxis triggers in Qatar. We were able to identify Table 1 Characteristics of the study population Characteristic Total N = 1068 n (%) Anaphylaxis N = 574 n (%) GAR N = 132 n (%) P-value Age (Years) < 10 603 (56.3) 300 (52.2) 85 (64.3) 0.009 10–19 210 (19.7) 109 (18.9) 22 (16.6) 20–55 209 (19.6) 137 (23.8) 21 (15.9) >. 55 46 (4.3) 28 (4.8) 4 (3.0) Gender Male 612 (57.3) 315 (54.8) 83 (62.8) 0.095 Female 456 (42.7) 259 (45.2) 49 (37.1) Nationality, N = 1067 Qatari 438 (41.0) 251 (43.7) 63 (47.7) 0.009 Non-Qatari, Arab 303 (28.4) 162 (28.2) 25 (18.9) Asian 228 (21.4) 118 (20.5) 24 (18.1) Others 98 (9.2) 42 (7.3) 20 (15.1) Personal History Asthma 357 (36.4) 208 (36.2) 68 (51.5) < 0.001 Atopic dermatitis 326 (33.2) 195 (33.9) 66 (50) < 0.001 Urticaria/ angioedema 254 (25.9) 179 (31.1) 36 (27.2) 0.485 Allergic rhinitis 142 (14.5) 81 (14.1) 30 (22.7) 0.009 Family History, N = 123 Atopy 70 (56.9) 58 (10.1) 8 (6.1) 0.989 Anaphylaxis 6 (4.9) 5 (0.8) 1 (0.7) Consanguinity, N = 33 30 (90.9) 25 (4.3) 2 (1.5) 1.000 GAR generalized allergic reactions Chi-square for trend (linear by linear association) One patient had no listed nationality in the system Atopy includes asthma, atopic dermatitis, urticaria and allergic rhinitis *P-value is for Fischer test (exact significant 2-sided) Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 4 of 8 Table 2 Causative triggers of symptoms in the study population Causative triggers Total N = 1068 n (%) Anaphylaxis N = 574 n (%) GAR N = 132 n (%) P-value Food (All) 403 (37.7) 316 (55.0) 87 (65.9) < 0.001 Nuts 232 (21.7) 173 (30.1) 59 (44.6) < 0.001 Egg 113 (10.5) 89 (15.5) 24 (18.1) 0.171 Seafood 93 (8.7) 72 (12.5) 21 (15.9) 0.111 Peanuts 92 (8.6) 71 (12.3) 21 (15.9) 0.100 Cow’s milk 77 (7.2) 61 (10.6) 16 (12.1) 0.326 Sesame seeds 65 (6.1) 50 (8.7) 15 (11.3) 0.158 Wheat 38 (3.5) 35 (6.1) 3 (2.2) 0.130 Other food 150 (14.0) 126 (21.9) 24 (18.1) 0.933 Insects’ stings (All) 184 (17.2) 161 (28.0) 23 (17.4) 0.122 Black ant 153 (14.3) 135 (23.5) 18 (13.6) 0.101 Bee 3 (0.2) 3 (0.5) 0 (0.0) 1.000 Wasp 1 (0.1) 1 (0.1) 0 (0.0) 1.000 Unspecified 29 (2.7) 24 (4.1) 5 (3.7) 0.798 Drugs (All) 123 (11.5) 103 (17.9) 20 (16.2) 0.978 Antibiotics 58 (5.4) 49 (8.5) 9 (6.8) 0.883 Augmentin 19 (1.7) 16 (2.7) 3 (2.2) 1.000 Penicillin 14 (1.3) 11 (1.9) 3 (2.2) 0.484 Ceftriaxone 6 (0.5) 6 (1.0) 0 (0.0) 0.596 Amoxicillin 6 (0.5) 5 (0.8) 1 (0.7) 1.000 Other antibiotics 22 (2.0) 19 (3.3) 3 (2.2) 1.000 NSAID 36 (3.3) 30 (5.2) 6 (4.5) 0.938 Ibuprofen 28 (2.6) 23 (4.0) 5 (3.7) 0.794 Paracetamol 8 (0.7) 8 (1.3) 0 (0.0) 0.366 Diclofenac 8 (0.7) 7 (1.2) 1 (0.7) 1.000 Aspirin 3 (0.3) 3 (0.5) 0 (0.0) 1.000 Other NSAID 4 (0.3) 4 (0.6) 0 (0.0) 1.000 d * IvIg 4 (0.3) 4 (0.6) 0 (0.0) 1.000 Vaccines 3 (0.3) 3 (0.5) 0 (0.0) 1.000 Other drugs 41 (3.8) 35 (6.1) 6 (4.5) 0.779 Idiopathic (All) 49 (4.5) 44 (7.6) 5 (3.7) 0.245 Nuts included cashew, pistachio, tree nuts, coconuts and hazelnuts excluding peanuts which has been counted separately Other food included chickpeas, bean, lentil, strawberry, banana, kiwi, mango, chicken, beef, pineapple, apple, and watermelon NSAID non-steroidal anti-inflammatory drugs IvIg Intravenous immunoglobulin *P-value is for Fischer test (exact significant 2-sided) 574 cases of anaphylaxis out of 1068 records. Food was action plan and risk reduction. However, such avoidance the leading trigger of anaphylaxis in children regardless measures are neither easily nor strictly followed by of gender. Anaphylaxis induced by drugs and insects’ children of this age group [16, 17, 33]. stings was more common among female adults (Fig. 2). Anaphylaxis was common in two age/gender groups: Interestingly, 23.5% of patients had anaphylaxis by black male children (n = 224, 39.0%) and female adults (n =114, ants. 19.8%) (Fig. 2), which is consistent with other findings re- Our data showed a predominance of anaphylaxis ported by Alshami et al. where they found an incidence of among pediatrics (n = 300, 52.2%), which is reasonable anaphylaxis in pediatric emergency centers of 13.3 per since at a single time point anaphylaxis is initially diag- 100,000 visits with 69% of patients being males [34], and nosed at childhood, and relevant triggers avoidance is Mehdi et al. showed that the incidence among adults was recommended as preventive measures of a long-term 16.5 per 100,000 visits with 78% being females [35]. Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 5 of 8 Fig. 2 Distribution of anaphylaxis pattern among different age and gender groups. a Food triggers, b Insect stings triggers, c Drug triggers, d Idiopathic triggers Several studies in different ethnic groups showed similar In our patients’ cohort, we observed that the association age and gender distribution of anaphylaxis among differ- between the development of anaphylaxis compared to GAR ent age/gender groups; for example, an epidemiological and the national origin were statistically significant (p-value study based on measuring the anaphylaxis rates in emer- = 0.009) (Table 1). For instance, “Non-Qatari Arabs” had gency department visits in hospitals across Florida, USA, relatively higher prevalence of anaphylaxis compared to reported that the highest anaphylaxis incidence rate was GAR while “Others” such as European, American and among the youngest males (8.2/100,000 visits) and the African had relatively lower prevalence of anaphylaxis com- adult females (10.9/100,000 visits) [20]. Similar to this, pared to GAR. Such differences in the rates of anaphylaxis findings from the Rochester epidemiology project from compared to GAR associated with ethnic and national 1990 through 2000 showed that age-specific incidence rate groups can be explained by a number of factors, including of anaphylaxis was the highest for ages 0–19 years [8]. genetic and environmental exposure. Qatar is a melting pot Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 6 of 8 of hundreds of nationalities of migrant workers [36]that were of severe grade and manifested mainly in the form of may have different genetic predisposition to allergy and anaphylaxis [46]. This study suggested that the sesame seed anaphylaxis. In addition to potential differences in the gen- is the “Middle Eastern” peanut [46]. etic make-up, different life style and dietary patterns as well Anaphylaxis and GAR attributable to Hymenoptera as differential prevalence of illnesses and use of varying stings in our study demonstrated predominance in fe- medications may be some of the factors that may or may male adults (n = 50, 45.9%) and male children (n = 30, not contribute to such differences [18, 23]. In general, ana- 40.0%) (Fig. 1b). Interestingly, 135 anaphylactic patients phylaxis was common [7–9, 20, 21], more associated with (23.5%) developed anaphylaxis by the sting of black ant repeated use of epinephrine [27]and more fatal[23]among which is a widespread ant in tropical Africa and the Caucasians compared to Black, Latino/Hispanic and Asian Middle East and is a native insect in Arabian Desert ethnicities. In contrast, Mahdavinia et al. (2017) reported countries, including Qatar [47, 48]. Allergic reactions that Caucasians had a lower rate of food allergy associated due to black ant stings range from pain with local anaphylaxis than African American and Hispanic children itching at the sting site to severe anaphylactic shock. [37]. Additionally, Buka et al. (2015) reported that AlAnazi et al. (2009) showed that the diversity of mani- Caucasians had less incidence, and were less likely to festation and human response to black ant stings in four present with severe anaphylactic symptoms than South cases encountered in Al Riyadh, the capital city of Saudi Asian British children living in Birmingham [38]. Arabia, and three patients were adult females [49]. In Personal history of atopy for asthma (n = 208, p < 0.001), contrast to our findings, lower prevalence of black ant atopic dermatitis (n = 195, p < 0.001) and allergic rhinitis induced anaphylaxis was reported in Saudi Arabia (3.2%) (n =81, p = 0.009) were noted among patients with ana- [14], and Singapore (12.9%) [50]. The unreported inci- phylaxis in Qatar (Table 1), and 56.9% cases had positive dence of black Samsum ant induced anaphylaxis was family history (Table 1). Although other studies showed no recognized in Iran where most stings result in mild aller- such significant association between atopy and anaphylaxis gic reactions [51]. However, in United Arab Emirates, [39, 40], atopy was frequently visualized as a risk factor that 4 deaths were recorded after the sting of this ant [52]. might worsen the clinical outcome of anaphylaxis [8, 18, Several studies attribute diversity of symptoms to the anti- 19, 21, 24, 41–43]. However, several studies stated that genicity variation of black ants’ toxin composition accord- anaphylaxis was common among patients with atopic dis- ing to geographical regions [51, 53]. Anaphylaxis in eases. In comparison to our study, different distribution of Najran, a city in southwestern Saudi Arabia, was triggered atopic diseases was observed [8, 18, 19, 21, 24, 41–43]. by a different species of black ant, Solenopsis richteri,in Our results showed that regardless of gender, food was non-Saudi expatriates (1997–1999) [54]. A Turkish retro- the culprit for anaphylaxis in children less than 10 years spective review defined prevalence of Hymenoptera stings (Fig. 2a). The major causative triggers of food-induced anaphylaxis among adult patients, however, the causative anaphylaxis in Qatar were nuts and eggs, a finding that triggers were mainly honey bees and different wasp was consistent with a Saudi finding reported in 2015 species [55]. In contrary to Qatar, the later Turkish study [14]. Peanuts, a major trigger of food-related anaphylaxis showed a predominance of Hymenoptera induced ana- in the United States [7, 9, 22], is ranked in the fourth phylaxis among male adults (57.1%) [55]. In light of the position after seafood in Qatar. In a prospective cohort absence of studies published about black Samsum ant study conducted in Qatar from 2007 to 2010, anaphyl- abundance, distribution, and its toxin antigenicity in axis induced by cow’s milk proteins (CMP) was found in Qatar, our results flag it as a public health hazard in Qatar 10 children out of 38 allergic subjects and suggested owing to its strong association with anaphylaxis. camel milk as a safer alternative choice after being experi- A key strength of this work includes the fact that mentally tested [30, 31]. With a larger study population, Hamad General Hospital, a member of Hamad Medical anaphylaxis induced by cow’s milk was accounted for 61 Corporation, is the only medical facility that dispenses (10.6%) from 2012 to 2016. In comparison, the prevalence EAIs in Qatar. Therefore, using dispensed (EAI) records of CMP anaphylaxis resulted in 6–9% of children hospital of outpatients in combination with medical coding system and emergency admission in the USA [7, 19, 21] and 10% (ICD-10 AM) of anaphylaxis for inpatients would be an in the UK [44]. CMP anaphylaxis accounted for 8 fatalities accurate estimation of the prevalence of anaphylaxis in in UK children during the period from 1992 to 2012 [13]. Qatar. Although, EAI dispense records were available for Our data showed that sesame seed accounted for 8.7% of 1year only(January – December 2016), EAIs as a refilled anaphylaxis cases in Qatar (Table 2). However, as a global drug included dispense records of previous years. allergen, sesame seed is affecting approximately 0.1% of North American population and is the third common food Conclusion allergen in Israel [45]. In Lebanon, a cross-sectional study Our study provides new data regarding the frequency of showed that allergic reactions triggered by sesame seed anaphylaxis in our geographical region; however, it is Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 7 of 8 prone to reporting bias due to its retrospective nature Ethics approval and consent to participate Ethical Approval: This retrospective study was ethically approved by the IRB and reliance on physician documentation. Besides that, committee of Medical Research Centre- Hamad Medical Corporation (IRB- we had 364 medical records (34.1%) with missing data HMC) (IRB#17122/17) with expedited status. For more information, kindly or incomplete charts and we cannot assume them as be- contact irb@hamad.qa, Tel: 00974–44,390,614. ing negative since there is the possibility of underreport- Consent to participate ing by physicians. Therefore, the presenting data should The study was a retrospective study. IRB-HMC approved the study for waiver be interpreted with caution stating that “within the of consent; provided that the methods used to protect patient confidentiality boundary of available data” registered in Cerner were judged to be adequate. power chart system and out of 1068 subjects, 574 Consent for publication (53.5%) patients had a definite diagnosis of anaphylaxis Not applicable. (2012–2016). Further studies are needed to confirm the medical diagnosis of the missing cases using another Competing interests method. This study will serve as a platform for clinicians The authors declare that they have no competing interests. in the allergy clinics in Qatar to improve patient care and for further epidemiological studies for understand- Publisher’sNote ing more about the prevalence of anaphylaxis in Qatar. Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Our data might provide the baseline for assessing future trends. We would recommend integrating entomology, Author details bioecology and medicine points of view to study black Biomedical Science Department, College of Health Science, Qatar University, P.O. Box 2713, Doha, Qatar. Allergy and Immunology Unit, Hamad Medical ant anaphylaxis in Qatar. Corporation, P.O. Box 3050, Doha, Qatar. College of Health Science, Qatar University, P.O. Box 2713, Doha, Qatar. Department, College of Health Additional file Science, Qatar University, P.O. Box 2713, Doha, Qatar. Allergy & Clinical Immunology Unit, Hamad Medical Corporation, P.O. Box 3050, Doha, Qatar. Pharmacy Department, Women’s Hospital, Hamad Medical Corporation, P.O. Additional file 1: Table S1. Anaphylactic patterns variation in relation Box 3050, Doha, Qatar. Hamad Medical Corporation, P.O. Box 3050, Doha, to age, gender and nationality. row percentage. Table S2. Symptoms of Qatar. the study population. (DOCX 19 kb) Received: 26 March 2018 Accepted: 26 July 2018 Abbreviations CMP: Cow’s milk proteins; EAIs: Epinephrine Auto-injectors; GAR: Generalized Allergic Reaction; HMC: Hamad Medical Corporation; ICD-10 AM: International References Classification of Diseases 10th revision-Australian Modification; IVIG: Intravenous 1. Keet C. Recognition and management of food-induced anaphylaxis. Pediatr Immunoglobulin; NSAID: Non-Steroidal Anti-Inflammatory Drugs; SPSS: Statistical Clin N Am. 2011;58(2):377–88. x Package for Social Sciences 2. Lee JK, Vadas P. Anaphylaxis: mechanisms and management. Clin Exp Allergy. 2011;41(7):923–38. 3. Simons FE, Ardusso LR, Bilò MB, Cardona V, Ebisawa M, El-Gamal YM, et al. Acknowledgements International consensus on (ICON) anaphylaxis. World Allergy Organ J. We would like to express our thanks to Dr. Dorra Gharbi and Mrs. Blessing 2014;7(1):9. Reena Dason for their assistance in data collection. 4. Boyce JA, Assa'ad A, Burks AW, Jones SM, Sampson HA, Wood RA, et al. Guidelines for the diagnosis and Management of Food Allergy in the Funding United States: summary of the NIAID-sponsored expert panel report. J No funds or financial supports were granted for this research work. Allergy Clin Immunol. 2010;126(6):1105–18. We received no sources of any outside support of the project. 5. Cox LS, Sanchez-Borges M, Lockey RF. World Allergy Organization Systemic Allergic Reaction Grading System: Is a Modification Needed? J Allergy Clin Availability of data and materials Immunol Pract. 2017;5(1):58–62.e5. The datasets used and/or analysed during the current study are available 6. Muraro A, Roberts G, Worm M, Bilò MB, Brockow K, Fernández Rivas M, et al. from the corresponding author on reasonable request. Anaphylaxis: guidelines from the European academy of allergy and clinical immunology. Allergy. 2014;69(8):1026–45. Authors’ contributions 7. Parlaman JP, Oron AP, Uspal NG, DeJong KN, Tieder JS. Emergency and We have participated sufficiently in the intellectual content, conception and Hospital Care for Food-Related Anaphylaxis in children. Hosp Pediatr. 2016; design of this work or the analysis and interpretation of the data (when 6(5):269–74. applicable), as well as the writing of the manuscript, to take public responsibility 8. Decker WW, Campbell RL, Manivannan V, Luke A, St Sauver JL, Weaver A, et for it and have agreed to have our name listed as contributors. Mainly, al. The etiology and incidence of anaphylaxis in Rochester, Minnesota: a TA collected data of EAIs and ICD-10 codes, analyzed the data and report from the Rochester epidemiology project. J Allergy Clin Immunol. wrote the maniscript as part of her master degree thesis, MAA and TA 2008;122(6):1161–5. designed the overall study and was a mjor contributor in the manscript, 9. Michelson KA, Monuteaux MC, Neuman MI. Variation and trends in LT guided the statistical analysis of the data and contributed to review anaphylaxis Care in United States Children's hospitals. Acad Emerg Med. of the manuscribt, RK analyzed the data using SPSS. SK reviewed collected data 2016;23(5):623–7. from power chart system for accuracy and helped in the final manuscribt review, 10. Diwakar L, Cummins C, Ryan R, Marshall T, Roberts T. Prescription rates of WE retrieved EAIs dispense list, reviewed collected data and helped in the final adrenaline auto-injectors for children in UK general practice: a retrospective manuscribt review, AND HZ H and HMM reviewed the maniscript critically several cohort study. Br J Gen Pract. 2017;67(657):e300–e5. times and helped during most of the steps. Please refere to above contribution 11. Gibbison B, Sheikh A, McShane P, Haddow C, Soar J. Anaphylaxis admissions table for further details of each contributor. All authors read and approved the to UK critical care units between 2005 and 2009. Anaesthesia. 2012;67(8): final manuscript. 833–9. Abunada et al. World Allergy Organization Journal (2018) 11:20 Page 8 of 8 12. Sheikh A, Hippisley-Cox J, Newton J, Fenty J. Trends in national incidence, 36. Statistics Authority. Qatar Population Status 376 2012: Three Years After lifetime prevalence and adrenaline prescribing for anaphylaxis in England. J Launching the Population Policy, State of Qatar. https://www.ppc.gov.qa/ R Soc Med. 2008;101(3):139–43. en/Pages/default.aspx. 13. Turner PJ, Gowland MH, Sharma V, Ierodiakonou D, Harper N, Garcez T, et al. 37. Mahdavinia M, Fox SR, Smith BM, James C, Palmisano EL, Mohammed Increase in anaphylaxis-related hospitalizations but no increase in fatalities: A, et al. Racial Differences in Food Allergy Phenotype and Health Care an analysis of United Kingdom national anaphylaxis data, 1992–2012. J Utilization among US Children. J Allergy Clin Immunol Pract. 2017;5(2): Allergy Clin Immunol. 2015;135(4):956–63.e1. 352–7.e1. 38. Buka RJ, Crossman RJ, Melchior CL, Huissoon AP, Hackett S, Dorrian S, et al. 14. Sheikh F, Amin R, Rehan Khaliq AM, Al Otaibi T, Al Hashim S, Al GS. First Anaphylaxis and ethnicity: higher incidence in British south Asians. Allergy. study of pattern of anaphylaxis in a large tertiary care hospital in Saudi 2015;70(12):1580–7. Arabia. Asia Pac Allergy. 2015;5(4):216–21. 39. Ganapathy S, Lwin Z, Ting DH, Goh LS, Chong SL. Anaphylaxis in children: 15. Mobayed HM, Ali A-NM. Two cases of food-dependent exercise-induced experience of 485 episodes in 1,272,482 patient attendances at a tertiary anaphylaxis with different culprit foods. Ann Thorac Med. 2014;9(1):42–4. Paediatric emergency department from 2007 to 2014. Ann Acad Med 16. Alsalamah M, Makhajia M, Somers G, Marcon M, Hummel D, Upton J. Singap. 2016;45(12):542–8. Anaphylaxis to milk after elimination diet for eosinophilic gastrointestinal 40. Rebelo Gomes E, Geraldes L, Gaspar Â, Malheiro D, Cadinha S, Abreu C, et disease. Am J Gastroenterol. 2016;111(5):752–3. al. Hypersensitivity reactions to nonsteroidal anti-inflammatory drugs 17. Zapatero L, Baeza ML, Sierra Z, Molero MI. Anaphylaxis by fruits of the among adults: clinical features and risk factors for diagnosis confirmation. Fagaceae family: acorn and chestnut. Allergy. 2005;60(12):1542. Int Arch Allergy Immunol. 2016;171(3–4):269–75. 18. Taylor-Black S, Wang J. The prevalence and characteristics of food 41. Orhan F, Canitez Y, Bakirtas A, Yilmaz O, Boz AB, Can D, et al. Anaphylaxis in allergy in urban minority children. Ann Allergy Asthma Immunol. Turkish children: a multi-Centre, retrospective, case study. Clin Exp Allergy. 2012;109(6):431–7. 2011;41(12):1767–76. 19. Huang F, Chawla K, Järvinen KM, Nowak-Węgrzyn A. Anaphylaxis in a New 42. Al-Hammadi S, Zoubeidi T, Al-Maskari F. Predictors of childhood food York City pediatric emergency department: triggers, treatments, and allergy: significance and implications. Asian Pac J Allergy Immunol. outcomes. J Allergy Clin Immunol. 2012;129(1):162–8.e1–3. 2011;29(4):313–7. 20. Harduar-Morano L, Simon MR, Watkins S, Blackmore C. A population-based 43. Jares EJ, Baena-Cagnani CE, Sanchez-Borges M, Ensina LF, Arias-Cruz A, epidemiologic study of emergency department visits for anaphylaxis in Gomez M, et al. Drug-induced anaphylaxis in Latin American countries. J Florida. J Allergy Clin Immunol. 2011;128(3):594–600.e1. Allergy Clin Immunol Pract. 2015;3(5):780–8. 21. Rudders SA, Banerji A, Corel B, Clark S, Camargo CA. Multicenter study of 44. Capps JA, Sharma V, Arkwright PD. Prevalence, outcome and pre-hospital repeat epinephrine treatments for food-related anaphylaxis. Pediatrics. management of anaphylaxis by first aiders and paramedical ambulance staff 2010;125(4):e711–8. in Manchester, UK. Resuscitation. 2010;81(6):653–7. 22. Michelson KA, Monuteaux MC, Neuman MI. Glucocorticoids and Hospital 45. Adatia A, Clarke AE, Yanishevsky Y, Ben-Shoshan M. Sesame allergy: current Length of Stay for Children with Anaphylaxis: A Retrospective Study. J perspectives. J Asthma Allergy. 2017;10:141–51. Pediatr. 2015;167(3):719–24.e1–3. 46. Irani C, Maalouly G, Germanos M, Kazma H. Food allergy in Lebanon: is sesame 23. Jerschow E, Lin RY, Scaperotti MM, McGinn AP. Fatal anaphylaxis in the seed the “middle eastern” peanut. World Allergy Organ J. 2011;4(1):1–3. United States, 1999–2010: temporal patterns and demographic associations. 47. Wetterer JK. Geographic spread of the samsum or sword ant, Pachycondyla J Allergy Clin Immunol. 2014;134(6):1318–28.e7. (Brachyponera) sennaarensis (Hymenoptera: Formicidae). Myrmecological 24. Lertnawapan R, Maek-a-nantawat W. Anaphylaxis and biphasic phase in News. 2013;18:13–8. Thailand: 4-year observation. Allergol Int. 2011;60(3):283–9. 48. Al-Khalifa MS, Mashaly AM, Siddiqui MI, Al-Mekhlafi FA. Samsum ant, 25. Järvinen KM, Amalanayagam S, Shreffler WG, Noone S, Sicherer SH, Brachyponera sennaarensis (Formicidae: Ponerinae): distribution and Sampson HA, et al. Epinephrine treatment is infrequent and biphasic abundance in Saudi Arabia. Saudi J Biol Sci. 2015;22(5):575–9. reactions are rare in food-induced reactions during oral food challenges in 49. AlAnazi M, AlAshahrani M, AlSalamah M. Black ant stings caused by children. J Allergy Clin Immunol. 2009;124(6):1267–72. Pachycondyla sennaarensis: a significant health hazard. Annals of Saudi 26. Meng J, Rotiroti G, Burdett E, Lukawska JJ. Anaphylaxis during general Medicine. 2009;29(3):207–11. anaesthesia: experience from a drug allergy Centre in the UK. Acta 50. Thong BY, Leong KP, Chng HH. Insect venom hypersensitivity: experience in Anaesthesiol Scand. 2017;61(3):281–9. a clinical immunology/allergy service in Singapore. Singap Med J. 2005; 27. Manivannan V, Campbell RL, Bellolio MF, Stead LG, Li JT, Decker WW. 46(10):535–9. Factors associated with repeated use of epinephrine for the treatment 51. Nikbakhtzadeh MRAK, Tirgari S. Bioecology and chemical diversity of of anaphylaxis. Ann Allergy Asthma Immunol. 2009;103(5):395–400. abdominal glands in the iranian samsum ant Pachycondyla sennaarensis 28. Cardona V, Ferré-Ybarz L, Guilarte M, Moreno-Pérez N, Gómez-Galán C, (Formicidae: Ponerinae). J Venom Anim Toxins Incl Trop Dis. 2009;15(3): Alcoceba-Borràs E, et al. Safety of adrenaline use in anaphylaxis: a 509–26. multicentre register. Int Arch Allergy Immunol. 2017;173(3):171–7. 52. Dib G, Guerin B, Banks WA, Leynadier F. Systemic reactions to the Samsum 29. Mobayed H, Ibrahim W, Al-Nesf M. Delayed clavulanic acid-induced ant: An IgE-mediated hypersensitivity. Journal of Allergy and Clinical anaphylaxis in a patient undergoing bariatric surgery. Ann Allergy Asthma Immunology. 1995;96(4):465–72. Immunol. 2014;113(3):324–5. 53. Akbarzadeh MN K, Tirgari S, Abaei MR. Medical Importnace of Fire Ant 30. Ehlayel M, Bener A, Abu Hazeima K, Al-Mesaifri F. Camel milk is a safer Pachycondyla sennaarensis (Hymenoptera: Formicidae) in Iranshahr and choice than goat milk for feeding children with cow milk allergy. ISRN Sarbaz Counties, Southeastern of Iran. J Med Sci. 2006;6:866–9. Allergy. 2011;2011:391641. 54. Khan SA, Shelleh HH, Khan LA, Shah H. Black fire ant (Solenopsis richteri) 31. Ehlayel MS, Hazeima KA, Al-Mesaifri F, Bener A. Camel milk: an alternative for sting producing anaphylaxis: a report of 10 cases from Najran. Ann Saudi cow's milk allergy in children. Allergy Asthma Proc. 2011;32(3):255–8. Med. 1999;19(5):462–4. 32. Simons FER, Ardusso LRF, Bilò MB, El-Gamal YM, Ledford DK, Ring J, et al. 55. Gelincik A, Demirtürk M, Yılmaz E, Ertek B, Erdogdu D, Çolakoğlu B, et al. World allergy organization guidelines for the assessment and Management Anaphylaxis in a tertiary adult allergy clinic: a retrospective review of 516 of Anaphylaxis. World Allergy Organ J. 2011;4(2):13–37. patients. Ann Allergy Asthma Immunol. 2013;110(2):96–100. 33. Boyano-Martínez T, García-Ara C, Pedrosa M, Díaz-Pena JM, Quirce S. Accidental allergic reactions in children allergic to cow's milk proteins. J Allergy Clin Immunol. 2009;123(4):883–8. 34. Alshami A, Adeli M, Alyafei K, Nisar S. Anaphylaxis presenting to the Pediatric Emergency Centers in Qatar. J Allergy Clin Immunol. 2018; 141(2):AB156. 35. Adeli M, Alyafei K, Chaudhry SI, Nisar S. Incidence, Etiology and characteristics of adult onset anaphylaxis in Qatar. J Allergy Clin Immunol. 2018;141(2):AB161.

Journal

World Allergy Organization JournalSpringer Journals

Published: Sep 4, 2018

There are no references for this article.