A EuroPrevall review of factors affecting incidence of peanut allergy: priorities for research and policy

A EuroPrevall review of factors affecting incidence of peanut allergy: priorities for research and policy
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  EU Forum A EuroPrevall review of factors affecting incidence of peanutallergy: priorities for research and policy The peanut ( Arachis hypogaea ), also known as thegroundnut, earthnut, monkey nut or goober, is a legume(1). Archaeological records suggest it was first encoun-tered and used by humans in Peru between 2500 and 300 bc  (2, 3). At the time of the Spanish and Portugueseconquests of America, peanuts were being grown widelyin the West Indies and South America. Nowadays, thepeanut is widely distributed, with the most importantproducing countries being India, China, USA, Argentina,Western and Southern Africa, and Brazil (4).  Arachishypogaea  has four main cultivars, known as Virginia,Peruvian Runner, Valencia and Spanish (believed to havesrcinated from different locations in South America),though breeding programmes to improve yields anddisease resistance have subsequently produced manydifferent varieties [Maleki (5) numbers 14 000 of these].Peanut seeds are nutritious, containing many importantnutrients, such as vitamin E, niacin, folacin, calcium,phosphorus, magnesium, zinc, iron, riboflavin, thiamineand potassium. They are also a good source of proteinand a rich source of edible oil. Furthermore, peanuts arecheap to produce – an important factor in the context of world hunger.On the negative side, the prevalence of food allergyrelated to peanuts has reportedly increased in recentdecades, particularly in western countries (6). Peanutsare among the highest food producers of IgE-mediatedallergic reactions following ingestion (7) and they areone of the most common foods that cause an allergicreaction, both in children and adults (8–14). Allergicreactions arise as a result of immunological responsesto particular proteins: in peanuts these proteins are Arah 1 ( vicilin ) ,  Ara h 2 ( conglutin-homologue protein ), andAra h 3/Ara h 4 (  glycinin ). These proteins are consid-ered major allergens because they are recognized byover 50% of peanut-allergic patients in the USA (13,15), although interestingly, Ara h 1 may be only aminor allergen for some European patients (16). Morerecently three additional minor allergens – Ara h 6 andAra h 7 (both  conglutin-homologue proteins ) as well asAra h 5 (the plant  pan-allergen profilin ) – have beenidentified (17). Recently, Mittag et al. (18) identified,Peanuts are extensively cultivated around the world, providing a foodstuff that isboth cheap to produce and nutritious. However, allergy to peanuts is of growingglobal concern, particularly given the severity of peanut-allergic reactions, whichcan include anaphalaxis and death. Consequently, it is important to understandthe factors related to the prevalence of peanut allergy in order to inform effortsto ameliorate or pre-empt the condition. In this article we review evidence for therelevance of factors hypothesized to have some association with allergy preva-lence, including both genetic and environmental factors. Although our analysisdoes indicate some empirical support for the importance of a number of factors,the key finding is that there are significant data gaps in the literature thatundermine our ability to provide firm conclusions. We highlight these gaps,indicating questions that need to be addressed by future research. A. Boulay 1 , J. Houghton 1 ,V. Gancheva 2 , Y. Sterk 2 , A. Strada 3 ,M. Schlegel-Zawadzka 3 , B. Sora 4 ,R. Sala 4 , R. van Ree 5 , G. Rowe 1 1 Institute of Food Research, Norwich Research Park,Colney, Norwich, UK;  2 Association APPEL EUROPA,Sofia, Bulgaria;  3 Jagiellonian University MedicalCollege, Krakow, Poland;  4 Centro de InvestigacionesEnergeticas, Medioambientales y Technologicas,Madrid, Spain;  5 Department of ExperimentalImmunology, Academic Medical Centre, Amsterdam,the Netherlands Key words: allergy; peanuts; prevalence; sensitization. A. BoulayInstitute of Food ResearchNorwich Research ParkColneyNorwich NR4 7 UAUKAccepted for publication 27 March 2008 Allergy 2008: 63: 797–809    2008 The AuthorsJournal compilation  2008 Blackwell MunksgaardDOI: 10.1111/j.1398-9995.2008.01776.x 797  cloned and expressed a new peanut allergen, Ara h 8which is the Bet v 1 homologue in peanut and a majorallergen in patients with combined birch pollen andpeanut allergy.Peanut allergy is one of the most severe food allergiesbecause of its sometimes life-threatening characteristics(14, 19) and also because it is rarely outgrown. Addi-tionally, people suffering from peanut allergy often reactto smaller doses of food than people with other foodallergies: peanut allergy can be triggered by a very smallamount, and even the smell of peanut can be enough totrigger an allergic reaction in extreme cases (20–23).Furthermore, diagnosing peanut allergy is difficult as theDouble Blind Placebo Controlled Food Challenge(DBPCFC) is expensive and time consuming, and hencemost recorded cases of peanut allergy are self-reported.Over the last 30 years, the prevalence of peanut allergy inthe western world is reported to have increased (6, 24)and has been estimated at from 1 in 10 000 up to 1 in 200(24–36). However, there is a lack of time series data anduniformity in data collection, making comparisons diffi-cult. Indeed, some researchers have argued against therehaving been such an increase, noting that similar rates of allergy exist in children and adults (27). Regardless,allergic diseases as a whole are now the most commonchronic disorders in childhood in the developed world(37), and the major increase over the last 25 years hashighlighted the need to develop more definitive preven-tative or curative strategies.The EuroPrevall project (a European multidisciplinaryand multicentre research project funded by the EU) hasbeen set up to study the prevalence, cost, and basis of food allergy and to ameliorate quality life for foodallergic people. After all, food allergy can have asignificant impact on an individual  s quality of life, andat the population level, there are economic consequencesin terms of medical costs and working days lost (38).While it would seem likely that the prevalence of foodallergy within a given population has some connection tothe eating behaviours within that population, causality isnot straightforward. Indeed, there appear to be manyfactors (both food-related and nonfood related) linked tothe development and incidence of food allergies. In thispaper we set out to identify factors linked to peanutallergy in particular, looking first at potential factorsinfluencing peanut sensitization, and then focusing onaspects of the peanut food chain that may be relevant toallergy incidence. In reviewing the research evidence, itmay be possible to identify patterns or trends in peanutproduction, processing and consumption that can be usedto create hypotheses about the causal factors influencingthe prevalence of peanut allergy, which may be tested at alater time. At the very least we hope this review exercisewill highlight data gaps, pointing to a series of researchquestions that need to be addressed in order to enhanceallergy prevention and management. We conclude ouranalysis with recommendations for future research. Method In order to identify factors related to the incidence of peanutallergy, a systematic literature review was undertaken. Relevantpublications from Science Direct, Blackwell Synergy, IngentaConnect, Web of Science, Taylor and Francis, Scopus, Medline,Google and Google scholar were identified between 16 May and 6July 2007. To select relevant articles, keywords used included  peanut   and its synonyms along with the terms:  Africa, aller- gen(s); allergenicity; allergic; allergy; Ara h 1; Ara h 2; Ara h 3;blanched; boiling; breast milk; consumer; consumption; cookingmethods; countries; crush; cultivars; cultivation; definition; earth-nut; Europe; export; fried; frying; geography; grinding; history;import; incidence; India; infant; lactation; milling; newborn; prevalence; processing; production; roasting; sensitization; temper-ature; time; tolerance; trade; UK; utilization; wean; weaning  andany combination of these terms. The literature search waslargely conducted on English language articles, but also includedarticles in French, Spanish, Polish and Bulgarian, reflecting thecomposition of members of our research project. The most rele-vant abstracts (related to peanut production/processing or con-sumption/utilization in relation to peanut allergy) were subjectedto a more detailed scrutiny. Publications (scientific and nonsci-entific) that did not focus exclusively on peanuts were excludedfrom the review. From the literature review, key factors wereidentified as important with regard to their potential role inpeanut allergy.Figures 1–3 summarize the results of this literature review,highlighting the various factors potentially related to peanutallergy, and the strength of evidence for their association.Figure 1 indicates factors related to peanut sensitization, provid-ing a simplified representation of the main categories of factorsthat may influence this, without showing the potentially complexinterrelationships between these (e.g. it does not show links be-tween genetic and environmental factors, but these do, of course,exist). Our main interest is in the peanut food chain, as willbecome apparent later on. Figure 2 thus focuses on production,processing and uses (consumption), but provides an added levelof detail to show the strength of evidence that exists for therelationship of the identified factors to allergy. Figure 3 goes evenfurther in detailing the evidence of those factors in the peanutfood chain that may be more important for allergy. In the sub-sequent sections we elucidate the relationships shown in thesefigures, looking at genetic and environmental factors, as well asaspects of the peanut food chain (e.g. cultivars, processing, earlyexposure and dietary habits). Factors involved in peanut sensitization Research shows that prevalence of peanut allergy varies withgeographic location (39). This may be explained by differences ingenetics (between and within populations) and/or environments(including cultural differences in behaviour between differentpopulations, in terms of different processing/cooking methods anddifferent environmental patterns of utilization, consumption andexposure in terms of both food and nonfood uses, and in terms of the time at which peanuts are introduced into the diet, e.g.weaning practices) (see Fig. 1). Other factors underlyinggeographical variation may include different frequencies/preva-lence of transplants, variations in incidence of certain atopicdiseases, and different rates of transmission via caesarean sections.Our analysis therefore does not consider geography  per se  as arelevant factor for allergy, but attempts to identify the underlyingfactors that explain geographical variance. Boulay et al.   2008 The Authors 798  Journal compilation    2008 Blackwell Munksgaard  Allergy 2008: 63: 797–809  Genetic factors Genes and history of atopic disease . It has been established thatgenetic factors may exert an influence on the development of peanutallergy (see Fig. 1), although allergen-specific inheritance for peanutis less well known or accepted than nonspecific inheritance(e.g. asthma, atopic dermatitis and rhinitis). In studies carried outin the UK, the frequency of peanut allergy has been found to besignificantly higher in relatives of peanut allergy patients than in thegeneral population (7%  vs  0.5%) (40). Children of allergic mothersare more likely to develop allergies than children of allergic fathers,butifbothparentsareallergicthenthereisamuchhighertendencytodevelop allergies. A survey of the families of 622 peanut allergicprobands(thefirstpersonbeingallergicandstudiedinafamily)intheUK noted an increased prevalence of peanut allergy in succeedinggenerations. However, increased prevalence also occurs in those withno apparent family history of allergy (41), and so a geneticexplanation provides only part of the story. A study carried out in58pairsoftwinsshowedthat7% ofdizygotesand64%monozygotesshared peanut allergy, suggesting a significant genetic influence. Theprobability of inheriting peanut allergy was estimated to be 81.6%, apercentage similar to other allergic diseases, such as asthma (87%),atopic dermatitis (74%) and allergic rhinitis (74–82%) (42).There is also a possible association with Human LeucocyteAntigen (HLA) class II genes (43). Howell et al. (43) concluded thatwhile other genetic factors may be important, results from theirstudy (individuals from 37 families and nine unrelated patients)indicated that HLA class II genetic polymorphism may play a rolein determining susceptibility to peanut allergy. Ethnicity . Though it appears that peanut allergy is increasing inprevalence, little evidence speaks to theethnicity of children sufferingfrom it. It is unclear whether the general trend reflects changingreferral patterns, a change in all allergic conditions, or an effectspecific to peanut allergy. Anecdotally, over the past 10 years, therehas been a disproportionate increase in the proportion of childrendiagnosed with peanut allergy from nonCaucasian ethnic groups inthe UK (44). In contrast, it has been noted that the high occurrenceof peanut allergy in the UK may not be typical of all countries in theworld, with peanut allergy reported only rarely in countries in Africaand Asia (45). The lower occurrence in these countries could beexplained by differences in the genes of the population, or they couldbe due to some other environmental factor, such as different types of infections or consumption practices (see  Environmental factors ). Environmental factors Environmental exposure to peanut . It has been observed that incountries in Africa and Asia where environmental exposure topeanuts is high, there is nevertheless a low reported prevalence of peanut allergy (45). One possible explanation is that oral toleranceinduction through early infant feeding protects these populationsagainst allergic sensitization (46, 47). Some data suggest that Transplant Caesarean section Link to other atopic diseases Genetic Environmental factors Microbes/hygiene History of atopic disease in family Early exposure : In utero Breast milk Formula milk Weaning Dietary habits (cultural and individual): Increased peanut consumption Increased vegetarian/vegan Healthy eating Domestic cooking methods Application (Nonfood): Medicine Cosmetics Eczema/nipple cream Others Immune system Peanut sensitisation Products containing peanutsConsumption (Food) Peanut cultivars Industrial processing :Food matrix Cross reactivity with other allergens Cross contamination: Eating out (restaurants, school, friends, family)Food processing ‘ready meal’ Ethnicity Genes Environmental exposure Peanut sensitisation Factors influencing peanut sensitisation Sub factors Categories Pathway Figure 1.  Factors influencing peanut sensitization. EuroPrevall review of factors for peanut allergy   2008 The AuthorsJournal compilation    2008 Blackwell Munksgaard  Allergy 2008: 63: 797–809  799  exposure to environmental peanuts during infancy promotessensitization and that low levels may be protective in atopicchildren (see Fig. 3). This supports the hypothesis that peanutsensitization occurs as a results of environmental exposure (44). Nospecial effect of maternal consumption during pregnancy orlactation has been observed.Perry et al. (48) describe the presence of environmental peanutallergen, which could potentially represent another source of topicalexposure. Perry et al. (48) measured by enzyme-linked immuno-sorbent assay (ELISA), the Ara h 1 peanut content on cafeteriatables and on hands and tabletops, as well as aerosolized peanutallergen during the consumption of peanut. Whereas Ara h 1 wasundetectable on hands after washing with soap and water, it wasdetectable on a quarter of hands after washing with water alone andhalf of hands after washing with a hand sanitizer. Most cleaningagents removed peanut allergen from tabletops, but Ara h 1 wasdetectable after dishwashing liquid cleansing on a third of tabletops.Interestingly, airborne Ara h 1 was undetectable in simulated real- Food processing (‘ready meal’, ethnic food) Food Nonfood Eating out ( restaurants,school, friends,family)Cross contaminationEarly exposure In utero Breast / formulae milk Peanut varieties: Cultivars: Runner, Virginia, Spanish Valencia Origin: America Africa Asia Australia Europe Low impact processing: Drying (naturally or dryers) High impact processing: Industrial processing Milling Grinding Blanching Boiling Frying Roasting Peanut uses P r o d u c t i o n P r o c e s s i n g U s e s Cosmetics Medicine Eczema/nipple creams Cross reactivity with other aller g ens Weaning Consumers’ profiles (Age; gender; region; socio-economic category) Increased peanut consumption Increased vegetarian/vegansHealthy eating Domesticcooking methods Dietary habits No or less significant impact on peanut allergy More significant impact on peanut allergy   Food matrix Pathway • • • • • • • • • Figure 2.  Generic peanut food chain schema. Boulay et al.   2008 The Authors 800  Journal compilation    2008 Blackwell Munksgaard  Allergy 2008: 63: 797–809  Figure 3.  Literature review finding of factors influencing peanut sensitization. EuroPrevall review of factors for peanut allergy   2008 The AuthorsJournal compilation    2008 Blackwell Munksgaard  Allergy 2008: 63: 797–809  801
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