New Allergens of Relevance in Tropical Regions: The Impact of Ascaris lumbricoides Infections
© World Allergy Organization; licensee BioMed Central Ltd. 2011
Published: 15 May 2011
One of the many aspects of the relationships between parasite infections and allergic diseases is the possibility that allergens from parasites enhance the TH2 responses, especially IgE production, in allergic diseases such as asthma. In this review we discuss about the allergenic composition of the nematode Ascaris lumbricoides and their potential impact on allergy sensitization and asthma pathogenesis and prevalence in populations living in the tropics and naturally exposed to both, mite allergens and helminth infections.
KeywordsAscaris hygiene hypothesis asthma ABA-1 Asc l 3
I Blomia tropicalis and Dermatophagoides pteronyssinus are the most important sources of clinically relevant allergens sensitizing patients with asthma in the tropics, [1–7] although they are also important in some sub tropical areas. Even though several epidemiological and clinical studies show that mite exposure in the tropics is perennial[8–10] and this may induce a sustained and strong IgE response, 2 important points deserve further investigation: first, the high frequency and intensity of the IgE response to mite allergens, [2, 11–15] and second, the high prevalence of asthma observed in some urban zones of this region [16–26].
One possibility is that these observations are some of the many consequences of the complex relationships between mite sensitization and soil transmitted helminth infections. In the tropics parasitic infections are still very frequent; helminths cause great morbidity and are one of the main sources of public health problems in underdeveloped countries. In testinal worms, or soil transmitted helminths, infect more than 2 billion people and Ascaris lumbricoides alone infects more that 1.2 billion [27, 28]. The patterns of infection vary regionally but exposed people living in urban setting suffer mild, intermittent infections by Ascaris. Although, in the future, with the improvement of hygiene conditions and lifestyle, parasitic diseases are expected to be eradicated in the tropics, in the current historical moment they are still modifying the pathogenesis and presentation of allergic diseases.
The Impact of A. LumbricoidesInfection (Ascariasis) on the Allergic Responses
Issues Supporting the Hypothesis That Ascariasis Enhances IgE Responses to Environmental Allergens and Allergies
Natural infection is associated with high levels of total and anti-Ascaris IgE responses
In some individuals, natural infection induces IgE-mediated allergic respiratory and cutaneous symptoms
In experimental human and animal models, bronchial challenges with Ascaris extract induce asthma symptoms
Experimental ascariasis in animals enhances IgE response to bystander antigens
Several epidemiological surveys have found that ascariasis is a risk factor for asthma and atopy
IgE responses to Ascaris allergens is more frequent and stronger in mite-sensitized asthmatic patients
Nematode infections bring together, but in different proportions, immunomodulation and IgE hyper-responsiveness; the latter is also a feature of the allergic responses and depends on the genetic background of the host. However, to understand the mechanisms underlying this particular phenotype, it is also essential to know the antigenic and allergenic composition of both, domestic mites and Ascaris, because they do not have the same clinical relevance. The majority of allergens from D. pteronyssinus and B. tropicalis are already identified, although the clinical relevance, biologic functions and molecular structure of most of them are still under study [6, 31–33]. However, most of the allergens from A. lumbricoides are unknown, and for a long time, the evaluation of IgE response in humans has been based on the use of the whole parasite extract or preparations from corporal fluids.
Parasite Infections Associated with Allergic Symptoms
The possibility that nematode allergens have an important role in allergies has been suspected for a long time because there are helminth-infections associated with allergy, IgE-mediated symptoms. The most typical is anisakiasis that induces asthma-like syndrome, urticaria, and anaphylaxis [34–36]. In this case the relationship with allergy symptoms is so evident that some authors consider it more an allergy than an infection and the list of allergens of Anisakis simplex officially accepted by the WHO/IUIS Nomenclature Committee is the largest for any parasite. However, before anisakiasis was discovered, clinicians from distinct disciplines have been dealing with hydatidosis, also known as echinococcosis. The rupture of hydatidic cysts that may be located in different places of the body is a well known cause of anaphylaxis, bronchospasm, and urticaria [37–40]. In addition, allergy symptoms associated with the migration of Strongyloides spp. and Toxocara ssp. are frequently observed in endemic areas [41–43].
Ascariasis is also a recognized cause of allergy symptoms, including Loeffler's Syndrome [44–46]. In addition, there are several human and animal experimental models showing the capacity of Ascaris antigens to induce parasite-specific IgE response and allergy symptoms (Table 1) [46–49]. However, because the relationship with allergy is not as evident as in anisakiasis, and some reports have demonstrated the immunosuppresor effect of chronic, heavy load infections in rural populations, [50, 51] there is the belief that ascariasis only induces immunosuppression. Therefore, to better study this point, it is mandatory to identify those Ascaris molecules that induce allergy symptoms, those that generate a protective IgE immune response and those that promote both effects. This will help to elucidate the actual role of these allergens on the pathogenesis of asthma and other allergic diseases and on the associated phenotypes.
Cross reactivity between Ascaris and other nematodes, such as Ancylostoma duodenale, Strongyloides stercoralis, Trichuris trichiuria, Necator americanus, and Anisakis simplex[52–56] has been described and it is possible that it plays a role in the pathogenesis of allergic diseases in the tropics, especially in helminth-helminth coinfections. However, this deserves more investigation because so far it has been mainly studied in relation to the serologic diagnosis of helminthiasis.
The Allergens of A. lumbricoides
A systematic approach for identifying the complete antigens and allergens of A. lumbricoides inducing immune responses in humans has not been followed. The antigenic composition of Ascaris spp. has been investigated and some molecules (eg, As14, As16, As24, As37, PAS-1) have been analyzed [57, 58]. PAS-1 has immunoregulatory properties; As24 and As16 confer protection from migration of A. suum larvae through the lungs as demonstrated in experimental vaccination models [58, 59]. However, our knowledge on the allergenic composition of Ascaris and its clinical impact in humans is still very limited.
There are 2 officially accepted (WHO/IUIS) allergens from this nematode: Asc l 1, also known as ABA-1, and Asc l 3, a tropomyosin. In addition, several IgE binding components have been detected using one dimensional (1D) and two-dimensional polyacrylamide-gel electrophoreses (2D PAGE),  and some allergens from other sources, such as A. simplex or Ascaris suum may be present in A. lumbricoides. Furthermore, there are sequence homologies between various Ascaris translated-nucleotides entries and recognized allergens, suggesting that the allergenic composition of A. lumbricoides is wide-ranging.
We recently analyzed, using cross-inhibition ELISA, 1D and 2D immunoblottings and mass spectrometry, the immunochemical properties of Ascaris tropomyosin (Asc l 3). Very high allergenic cross-reactivity between the natural Asc l 3 and B. tropicalis tropomyosin, Blo t 10, was found using sera from asthmatic patients . These results were confirmed using a recombinant A. lumbricoides tropomyosin expressed in a bacterial system . This is the full-length sequence of Asc l 3 and has been classified as Asc l 3.0101. Amino acid sequence identity between mite and Ascaris tropomyosins ranges from 73 to 74% and some regions predicted to be IgE binding epitopes in shrimp tropomyosin, were found to be identical in these molecules.
It was also found that IgE antibodies to rAsc l 3 represent a high proportion (~50%) of the total IgE response to an unfractionated parasite extract and there was allergenic equivalence between rAsc l 3 and the native counterpart in the A. lumbricoides extract. Furthermore, antitropomyosin IgE antibodies from sensitized subjects reacted against A. lumbricoides tropomyosin and induced mediator release in effector cells, both in vivo and in vitro.
ABA-1, although present in other nematodes, is not cross-reactive with any of the B. tropicalis or D. pteronyssinus allergens, which means that it can be very useful for component-resolved diagnosis of allergic diseases in the tropics. ABA-1 (Asc l 1) is a member of the Nematode Polyprotein Allergen/Antigens [61–63]. Studies support that immune responses (IgG and IgE) to ABA-1 are associated with previous infection and immunity to Ascaris . In endemic regions the antibodies isotypes to ABA-1 correlate with the severity of infection, being IgE associated with low infection levels and IgG4 or seronegativity with higher susceptibility to the infection . This protein of 15 kDa has only been found in nematodes, has fatty acid binding properties and is synthesized as a polyprotein in gut of the worms and released into the pseudocelomic fluid of the parasite [61, 67]. Even though most Ascaris allergens have not been characterized, there are data suggesting that Asc l 1 and Asc l 3 play important roles inducing protective antibody immunity and allergy sensitization
Possible Effects of AscarisAllergens on the Clinical Evolution of Asthma
One potential mechanism to enhance the IgE responses to allergens in asthmatic patients living in the tropics is cross-reactivity (reviewed in). It can act at several points in the evolution of ascariasis or asthma, and the tropical environment provides particular conditions for this effect.
First, there is the possibility of early life coexposure to allergens and antigens from mites and A. lumbricoides. The complex interactions elicited by allergenic molecules from different sources acting together on the innate and adaptive immune responses are not yet clearly defined, but one possible outcome is the enhancement of the allergic responses . Early IgE responses to mites and Ascaris have been observed in children from tropical regions and some studies have found clinical relevance [68, 69].
Second, parasited children in underdeveloped tropical countries receive antihelminth drug therapy during intermittent mass de-worming programs in preschool and school-aged . Because the fundamental socioeconomic causes of the infections are not eliminated, children become reinfected several times with A. lumbricoides and this sort of modified secondary immune responses may be boosters of the IgE reactivity against cross-reactive allergens from other sources (eg, mites). In general, antihelminth therapy induces changes of the TH2 immune responses; however, the mechanisms involved remain to be elucidated. Repeated treatments significantly increase the production of TH2 cytokines, IL5, and IL13 and decrease the production of IL-10 by peripheral blood leukocytes after stimulation with Ascaris antigens, although no changes were observed when stimulating with D. pteronyssinus and cockroach; however, it was also found that long term periodic treatments in a community with various helminthiasis, including ascariasis, was associated with increase of allergen skin reactivity .
In schistosomiasis there is evidence that antihelminthic treatment influences the evolution of several mechanisms of immunity, including increasing of effector T cells proportion and the switch to protective antibody isotypes such as IgE, [73, 74] probably because of higher loads of antigens from death parasites, [73, 75] and the removal of immunosuppressive parasite products . Reinfections add more possibilities to stimulate memory cells,  and some of these mechanisms may work, not only in schistosomiasis but also in other helminthiasis such as ascariasis. For example, it has been reported that treatment of A. lumbricoides coinfection may delay HIV-1 disease progression by reducing helminth-induced, IL-10-mediated immunosuppression .
Third, as it is well known, mite-allergens exposure is perennial and very intense in the tropics; therefore, in the Ascaris-infected population (current or past) susceptible to asthma, this may be other cause of increasing the IgE responses to cross-reactive allergens. It can be speculated that patients predisposed to asthma, with a strong pro-TH2 genetic background, early age parasited, suffering several reinfections and permanently exposed to mite allergens probably have a stronger IgE responses to allergens and more severe clinical symptoms.
The Role of Asc l 1 and Asc l 3 in the Ascariasis/Allergy Relationships
As noted, in humans, the IgE and IgG responses to ABA-1 (Asc l 1) is more related with protection to A. lumbricoides infection than with allergy symptoms. However, studies addressed to evaluate directly the allergenic role of this molecule have not been done, and therefore, the possibility that it acts as an allergy-symptoms inducer has not been ruled out. In contrast, tropomyosin is a well recognized invertebrate pan-allergen and Asc l 3 has a high degree of homology and cross-reactivity with mite tropomyosins. Although a role as protective antigen, such as Onchocerca tropomyosin is also possible, we have data suggesting that it is associated with allergy symptoms,  which may be of epidemiological importance because a high percentage of the population living in the tropics have IgE reactivity to tropomyosins.
Our studies about the IgE responses to ABA-1 and Ascaris extract in humans suggest different roles for the allergens of this nematode. For example, in a case-control survey to evaluate the influence of Ascaris-specific IgE sensitization on asthma, we found a statistically significant association when the complete Ascaris extract was used (Caraballo et al, submitted). However, the significance disappeared when adjusting for total IgE or mite-specific IgE, which confirms the known role of these phenotypes as risk factors for asthma in the tropics. In addition, when ABA-1-specific IgE was investigated, there was no significance at all. Because this search was performed in a large population (421 asthmatics and 620 controls) living in the tropics, it is possible that the weak association detected with the Ascaris extract was because of mite-Ascaris cross-reactivity among several of their allergenic components. In contrast, ABA-1, which has been previously associated with immunity to Ascaris and is not cross-reactive with mite allergens, seems to induce an IgE response not associated with symptoms.
Among the cross-reactive allergens that may underlie the association between Ascaris/extract-specific IgE and asthma, Asc l 3 is a good candidate. Therefore, we further analyzed the role of Asc l 3 as a risk factor for asthma among the subjects with positive anti-Ascaris-extract IgE test from the same population. The frequency of sensitization to rAsc l 3 was greater in asthmatics (n = 175) than in controls (n = 170). This result was independent of age and sex. However, when adjusting for covariates such as specific IgE to mites, the significance disappeared, remaining a P value of 0.06 . When analyzed as a continuous variable, specific IgE levels to rAsc l 3 were significantly higher in asthmatic patients than in controls. These findings, although not define an independent association of Asc l 3 with asthma, suggest that it may be a risk factor for this disease in the tropics.
Because it is very difficult to define this point by cross-sectional epidemiologic surveys because of the variable origin of the primary sensitization (mites vs Ascaris), we are currently evaluating the early IgE responses to purified Ascaris and mite allergens in a birth cohort (Risk Factors for asthma and allergic diseases in the tropics, FRAAT) . This will help to better understand the actual role of different antigens and allergens in the pathogenesis of asthma and ascariasis. In addition, animal models analyzing the effects of allergen combinations on sensitization will be also useful.
The possibility of particular roles of ABA-1 and other allergens from Ascaris in terms of resistance to the infection and inducing allergic symptoms are also supported by genetic epidemiology studies. There is important evidence that resistance to ascariasis (as evaluated by eggs count in faeces) is probably determined by genes in Chromosome 13q33-34 . Because this region harbor several immune related genes, it was suggested TNFSF13B (coding for BAFF cytokine) as a good candidate for explaining the positive linkage results. Therefore, we performed an association study in a population of asthmatics and normal subjects living in the tropics, to investigate the relationships between polymorphisms of 3 genes in that region and the IgE responses to Ascaris, B. tropicalis, and D. pteronyssinus extracts, the recombinant ABA-1 and asthma . Interestingly, we found association between the IgE response to ABA-1 and the SNP G3980C of TNFSF13B. In addition, there was significant association between the variant G299A of LIG4 (Ligase IV), and IgE to Ascaris extract. However, we found no association between any of the studied markers and the immune responses to mite allergens or asthma. These findings support that antibody responses to ABA-1 is associated with resistance while the IgE responses to other allergens may be associated with allergy. Of course, more studies are needed to dissect the antibody responses against the complete set of Ascaris antigens and allergens.
Why is it Useful for Allergology to Characterize the Allergens of A. lumbricoides?
In this review, we argument in pro of the hypothesis that, in the current conditions of socio-economic development of urban areas of tropical countries, ascariasis enhances the IgE responses to mite allergens and, in consequence, influence asthma symptoms. Testing this hypothesis is an important reason to characterize the allergenic components of Ascaris and mite extracts, not only because of its potential basic and clinical impact but, in addition, it may explain the high prevalence of asthma in some tropical regions, where viral and bacterial respiratory and gastrointestinal infections are still prevalent, a topic of special interest in regard of the hygiene hypothesis.
Parasite Infections, Allergy, and the Hygiene Hypothesis
As in its first version, the hygiene hypothesis, raised after some epidemiologic findings, [83, 84] predicts that allergic diseases are more frequent in those places where the improvement of hygiene conditions has been really successful, making bacterial and virus infections infrequent in early childhood. The idea is widely accepted and has stimulated several theoretical and experimental approaches to discover basic mechanisms explaining the effects of infections on immune polarization, the inception of IgE sensitization[85, 86] and the observed increase of the prevalence of allergic diseases in industrialized countries.
Several factors and conditions influencing the immune system have been proposed to understand how the hygiene hypothesis works. For example, immune deviation to a predominant TH1 response because of bacterial and viral infections was, at the beginning, the most obvious explanation; but there is also the suggestion that, instead of infections, there are other elements determining the evolution of the immune responses in children, and, in consequence, acting on the inception of IgE-mediated diseases, among them, the colonization of gut by commensal microbes[87–89] and inhaling cell wall products during infancy [88, 90].
An important point is that, according to the immunoregulatory mechanisms proposed to support the hygiene hypothesis, it is expected that allergic diseases have low prevalence in those places where hygiene conditions are poor, and that seem to be true, at least in some particular places, but there are reasons to believe that this is because of chronic helminth infections[50, 91–96] and not a result of microbe infections. More interestingly, as it is becoming increasingly known, in several mid- to low-income countries of the tropical zone, the prevalence of asthma and other allergic diseases is high and concur with early bacterial and viral infections [16–26]. And here again, the helminth-infections/allergy relationships may explain why the increasing trend in the prevalence of allergies is more general and not restricted to affluent countries with good hygiene conditions [97, 98].
Typically, soil transmitted helminth infections are susceptible to change in frequency when modifying hygiene conditions. During the last decade the immunosuppressive effects of chronic, heavy loads helminth infections have been described in both humans and animals, resulting more evident than any immunomodulatory phenomenon accompanying bacterial or viral infections different from HIV infection. These findings have reinforced the idea that parasite infections have played a major role in controlling the allergic responses; and the lack of this control, because of the improvement of hygiene conditions, has lead to the current figures of allergy prevalence [99, 100].
Therefore, the high prevalence of asthma that is currently observed in some urbanized zones of the tropics, where helminth infections, such as ascariasis, are still present but with less intensity than in the past, may be explained, among other factors, as a consequence of the particular historical moment of the ancient and complex relationships between parasites and the immune system: a point where, because of several reasons, the immunostimulating effects of helminths on the IgE responses predominate.
As noted, the type and distribution of parasites, and the frequency, intensity, and immunomodulatory effects of helminth infections, are not the same through the world. In the tropics, both the immunosuppressive and the TH2-immunopotentiating effects can be detected, being the latter more frequent at the population level. Then, in this dynamic and changing world, 3 distinct relationships between helminths and the human immune system can be recognized: One with chronic heavy parasite-load infections and mainly immunosuppressive, other of intermittent low parasite-load infections, predominantly IgE-enhancer and associated with urbanization; and a third, with absence of infections, where there is no parasite-derived immunoregulation.
The possible consequences of each of these relationships on the development of allergic diseases have been already analyzed, but 2 additional comments are pertinent. First, a comprehensive study of the human-helminth relationships should include their genetic and evolutionary aspects, which is out of the scope of this review. Here it is just necessary to mention that, because the pathogenesis of ascariasis and other helminth infections, and that of asthma, are highly influenced by genetic factors, these will affect the proportions of individuals that establish any of the proposed relationships in a given population. Second, as suggested by some investigators, the potential effects of other changes associated with urbanization, for instance, differences in diet and lifestyle, physical activity and housing should also be considered.
One of the multiple faces of the relationships between ascariasis and allergic diseases in tropical environments is specific IgE hyper-responsiveness, mainly induced by As caris allergens, mite allergens, and Ascaris-mite cross-reactive allergens. As it may affect, not only the evolution of asthma in individual patients, but asthma prevalence at the population level, specific IgE hyper-responsiveness also impacts theoretical aspects of allergology, such as the hygiene hypothesis. Analyzing the various possibilities that may explain these particular host-parasite relationships, demands important basic, clinical, and epidemiological research. The availability of well characterized A. lumbricoides and mite allergens will be very helpful.
Funded by the Administrative Department of Science, Technology and Innovation (Colciencias-Colombia); Grants 325-2006, 093-2007, and 680-2009.
Part of the data were presented at International Symposium of Molecular Allergology (ISMA), 2010-10-31, Munich.
- Sanchez-Borges M, Capriles-Hulett A, Caballero-Fonseca F, Fernan dez-Caldas E: Mite and cockroach sensitization in allergic patients from Caracas, Venezuela. Ann Allergy Asthma Immunol. 2003, 90: 664-668. 10.1016/S1081-1206(10)61873-X.PubMedView ArticleGoogle Scholar
- Puerta L, Fernandez-Caldas E, Lockey RF, Caraballo LR: Mite allergy in the tropics: sensitization to six domestic mite species in Cartagena, Colombia. J Investig Allergol Clin Immunol. 1993, 3: 198-204.PubMedGoogle Scholar
- Chew FT, Lim SH, Goh DY, Lee BW: Sensitization to local dust-mite fauna in Singapore. Allergy. 1999, 54: 1150-1159. 10.1034/j.1398-9995.1999.00050.x.PubMedView ArticleGoogle Scholar
- Ferrandiz R, Casas R, Dreborg S: Sensitization to Dermatophagoides siboney, Blomia tropicalis, and other domestic mites in asthmatic patients. Allergy. 1996, 51: 501-505.PubMedView ArticleGoogle Scholar
- Caraballo L, Puerta L, Fernandez-Caldas E, Lockey RF, Martinez B: Sensitization to mite allergens and acute asthma in a tropical environment. J Investig Allergol Clin Immunol. 1998, 8: 281-284.PubMedGoogle Scholar
- Chua KY, Cheong N, Kuo IC, Lee BW, Yi FC, Huang CH, Liew LN: The Blomia tropicalis allergens. Protein Pept Lett. 2007, 14: 325-333. 10.2174/092986607780363862.PubMedView ArticleGoogle Scholar
- Sanchez Palacios A, Schamann Medina F, Garcia Marrero JA, Sanchez Palacios MA, Perez Griera J, Lamas-Figueroa A: Prevalence of sensitization to Blomia in Gran Canaria. Allergol Immunopathol (Madr). 1995, 23: 105-110.Google Scholar
- Fernandez-Caldas E, Puerta L, Caraballo L, Mercado D, Lockey RF: Sequential determinations of Dermatophagoides spp. allergens in a tropical city. J Investig Allergol Clin Immunol. 1996, 6: 98-102.PubMedGoogle Scholar
- Fernandez-Caldas E, Puerta L, Mercado D, Lockey RF, Caraballo LR: Mite fauna, Der p I, Der f I and Blomia tropicalis allergen levels in a tropical environment. Clin Exp Allergy. 1993, 23: 292-297. 10.1111/j.1365-2222.1993.tb00325.x.PubMedView ArticleGoogle Scholar
- Puerta L, Fernandez-Caldas E, Mercado D, Lockey RF, Caraballo LR: Sequential determinations of Blomia tropicalis allergens in mattress and floor dust samples in a tropical city. J Allergy Clin Immunol. 1996, 97: 689-691. 10.1016/S0091-6749(96)70315-9.PubMedView ArticleGoogle Scholar
- Puerta L, Fernandez-Caldas E, Lockey RF, Caraballo LR: Sensitization to Chortoglyphus arcuatus and Aleuroglyphus ovatus in Dermatophagoides spp. allergic individuals. Clin Exp Allergy. 1993, 23: 117-123. 10.1111/j.1365-2222.1993.tb00306.x.PubMedView ArticleGoogle Scholar
- Puerta L, Lagares A, Mercado D, Fernandez-Caldas E, Caraballo L: Allergenic composition of the mite Suidasia medanensis and cross-reactivity with Blomia tropicalis. Allergy. 2005, 60: 41-47. 10.1111/j.1398-9995.2004.00636.x.PubMedView ArticleGoogle Scholar
- Puerta Llerena L, Fernandez-Caldas E, Caraballo Gracia LR, Lockey RF: Sensitization to Blomia tropicalis and Lepidoglyphus destructor in Dermatophagoides spp-allergic individuals. J Allergy Clin Immunol. 1991, 88: 943-950. 10.1016/0091-6749(91)90252-J.PubMedView ArticleGoogle Scholar
- Puccio FA, Lynch NR, Noya O, Noda A, Hagel I, et al: Importance of including Blomia tropicalis in the routine diagnosis of Venezuelan patients with persistent allergic symptoms. Allergy. 2004, 59: 753-757. 10.1111/j.1398-9995.2004.00454.x.PubMedView ArticleGoogle Scholar
- Acevedo NEA, Briza P, Puccio F, Ferreira F, Caraballo L: Allergenicity of Ascaris lumbricoides Tropomyosin and IgE sensitization among asthmatic patients in a tropical environment. Int Arch of Allergy Immunol. 2011, 154: 195-206. 10.1159/000321106.View ArticleGoogle Scholar
- Chatkin MN, Menezes AM, Victora CG, Barros FC: High prevalence of asthma in preschool children in Southern Brazil: a population-based study. Pediatr Pulmonol. 2003, 35: 296-301. 10.1002/ppul.10229.PubMedView ArticleGoogle Scholar
- Pitrez PM, Stein RT: Asthma in Latin America: the dawn of a new epidemic. Curr Opin Allergy Clin Immunol. 2008, 8: 378-383. 10.1097/ACI.0b013e32830fb911.PubMedView ArticleGoogle Scholar
- Caraballo L, Cadavid A, Mendoza J: Prevalence of asthma in a tropical city of Colombia. Ann Allergy. 1992, 68: 525-529.PubMedGoogle Scholar
- Dennis R, Caraballo L, García E, Caballero A, Aristizabal G, et al: Asthma and other allergic conditions in Colombia: a study in 6 cities. Ann Allergy Asthma Immunol. 2004, 93: 568-574. 10.1016/S1081-1206(10)61265-3.PubMedView ArticleGoogle Scholar
- Wördemann M, Polman K, Diaz RJ, Menocal Heredia LT, Madurga A, et al: The challenge of diagnosing atopic diseases: outcomes in Cuban children depend on definition and methodology. Allergy. 2006, 61: 1125-1131. 10.1111/j.1398-9995.2006.01129.x.PubMedView ArticleGoogle Scholar
- Sharma SK, Banga A: Prevalence and risk factors for wheezing in children from rural areas of north India. Allergy Asthma Proc. 2007, 28: 647-653. 10.2500/aap.2007.28.3059.PubMedView ArticleGoogle Scholar
- Pearce N, Aït-Khaled N, Beasley R, Mallol J, Keil U, et al: Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax. 2007, 62: 758-766. 10.1136/thx.2006.070169.PubMedPubMed CentralView ArticleGoogle Scholar
- Solé D, Melo KC, Camelo-Nunes IC, Freitas LS, Britto M: Changes in the prevalence of asthma and allergic diseases among Brazilian school children (13-14 years old): comparison between ISAAC Phases One and Three. J Trop Pediatr. 2007, 53: 13-21.PubMedView ArticleGoogle Scholar
- Kuschnir FC, Alves da Cunha AJ: Environmental and socio-demographic factors associated to asthma in adolescents in Rio de Janeiro, Brazil. Pediatr Allergy Immunol. 2007, 18: 142-148. 10.1111/j.1399-3038.2006.00477.x.PubMedView ArticleGoogle Scholar
- Garcia E, Aristizabal G, Vasquez C, Rodriguez-Martinez CE, Sarmiento OL, Satizabal CL: Prevalence of and factors associated with current asthma symptoms in school children aged 6 -7 and 13-14 yr old in Bogota Colombia. Pediatr Allergy Immunol. 2008, 19: 307-314. 10.1111/j.1399-3038.2007.00650.x.PubMedView ArticleGoogle Scholar
- Nicolaou N, Siddique N, Custovic A: Allergic disease in urban and rural populations: increasing prevalence with increasing urbanization. Allergy. 2005, 60: 1357-1360. 10.1111/j.1398-9995.2005.00961.x.PubMedView ArticleGoogle Scholar
- Bethony J, Brooker S, Albonico M, Geiger S, Loukas A, Diemert D, Hotez P: Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006, 367: 1521-1532. 10.1016/S0140-6736(06)68653-4.PubMedView ArticleGoogle Scholar
- Brooker S: Estimating the global distribution and disease burden of intestinal nematode infections: adding up the numbers-a review. Int J Parasitol. 2010, 40: 1137-1144. 10.1016/j.ijpara.2010.04.004.PubMedPubMed CentralView ArticleGoogle Scholar
- Cooper PJ: Interactions between helminth parasites and allergy. Curr Opin Allergy Clin Immunol. 2009, 9: 29-37. 10.1097/ACI.0b013e32831f44a6.PubMedPubMed CentralView ArticleGoogle Scholar
- Caraballo L, Acevedo N: Allergy in the tropics: the impact of cross-reactivity between mites and ascaris. Front Biosci. 2011, 3: 51-64. 10.2741/e219.View ArticleGoogle Scholar
- Fernandez-Caldas E, Puerta L, Caraballo L, Lockey RF: Mite allergens. Clin Allergy Immunol. 2008, 21: 161-182.PubMedGoogle Scholar
- Thomas WR, Hales BJ, Smith WA: House dust mite allergens in asthma and allergy. Trends Mol Med. 2010, 16: 321-328. 10.1016/j.molmed.2010.04.008.PubMedView ArticleGoogle Scholar
- Zakzuk J, Jiménez S, Cheong N, Puerta L, Lee BW, Chua KY, Caraballo L: Immunological characterization of a Blo t 12 isoallergen: identification of immunoglobulin E epitopes. Clin Exp Allergy. 2009, 39: 608-616. 10.1111/j.1365-2222.2008.03193.x.PubMedView ArticleGoogle Scholar
- Daschner A, Alonso-Gomez A, Cabanas R, Suarez-de-Parga JM, Lopez-Serrano MC: Gastroallergic anisakiasis: borderline between food allergy and parasitic disease-clinical and allergologic evaluation of 20 patients with confirmed acute parasitism by Anisakis simplex. J Allergy Clin Immunol. 2000, 105: 176-181. 10.1016/S0091-6749(00)90194-5.PubMedView ArticleGoogle Scholar
- Nieuwenhuizen N, Lopata AL, Jeebhay MF, Herbert DR, Robins TG, Brombacher F: Exposure to the fish parasite Anisakis causes allergic airway hyperreactivity and dermatitis. J Allergy Clin Immunol. 2006, 117: 1098-1105. 10.1016/j.jaci.2005.12.1357.PubMedView ArticleGoogle Scholar
- Audicana MT, Kennedy MW: Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clin Microbiol Rev. 2008, 21: 360-379. 10.1128/CMR.00012-07. table of contentsPubMedPubMed CentralView ArticleGoogle Scholar
- Pump KK: Echinococcosis (hydatid disease): a review and report of a case of secondary echinococcosis. Can Med Assoc J. 1963, 89: 73-78.PubMedPubMed CentralGoogle Scholar
- Gelincik A, Ozseker F, Buyukozturk S, Colakoglu B, Dal M, Alper A: Recurrent anaphylaxis due to non-ruptured hepatic hydatid cysts. Int Arch Allergy Immunol. 2007, 143: 296-298. 10.1159/000100576.PubMedView ArticleGoogle Scholar
- Vuitton DA: Echinococcosis and allergy. Clin Rev Allergy Immunol. 2004, 26: 93-104. 10.1007/s12016-004-0004-2.PubMedView ArticleGoogle Scholar
- Chandrasekhar S, Parija SC: Serum antibody & Th2 cytokine profiles in patients with cystic echinococcosis. Indian J Med Res. 2009, 130: 731-735.PubMedGoogle Scholar
- Ravi V, Ramachandran S, Thompson RW, Andersen JF, Neva FA: Characterization of a recombinant immunodiagnostic antigen (NIE) from Strongyloides stercoralis L3-stage larvae. Mol Biochem Parasitol. 2002, 125: 73-81. 10.1016/S0166-6851(02)00214-1.PubMedView ArticleGoogle Scholar
- Neva FA, Gam AA, Maxwell C, Pelletier LL: Skin test antigens for immediate hypersensitivity prepared from infective larvae of Strongyloides stercoralis. Am J Trop Med Hyg. 2001, 65: 567-572.PubMedGoogle Scholar
- Leighton PM, MacSween HM: Strongyloides stercoralis. The cause of an urticarial-like eruption of 65 years' duration. Arch Intern Med. 1990, 150: 1747-1748. 10.1001/archinte.1990.00040031747027.PubMedView ArticleGoogle Scholar
- Spillmann RK: Pulmonary ascariasis in tropical communities. Am J Trop Med Hyg. 1975, 24: 791-800.PubMedGoogle Scholar
- Joubert JR, de Klerk HC, Malan C: Ascaris lumbricoides and allergic asthma: a new perspective. S Afr Med J. 1979, 56: 599-602.PubMedGoogle Scholar
- Joubert JR, van Schalkwyk DJ, Turner KJ: Ascaris lumbricoides and the human immunogenic response: enhanced IgE-mediated reactivity to common inhaled allergens. S Afr Med J. 1980, 57: 409-412.PubMedGoogle Scholar
- Patterson R, Harris KE, Pruzansky JJ: Induction of IgE-mediated cutaneous, cellular, and airway reactivity in rhesus monkeys by Ascaris suum infection. J Lab Clin Med. 1983, 101: 864-872.PubMedGoogle Scholar
- Patterson R, Harris KE: IgE-mediated rhesus monkey asthma: natural history and individual animal variation. Int Arch Allergy Immunol. 1992, 97: 154-159. 10.1159/000236111.PubMedView ArticleGoogle Scholar
- Tsuji M, Hayashi T, Yamamoto S, Sakata Y, Toshida T: IgE-type antibodies to Ascaris antigens in man. Int Arch Allergy Appl Immunol. 1977, 55: 78-81. 10.1159/000231912.PubMedView ArticleGoogle Scholar
- Cooper PJ, Chico ME, Rodrigues LC, Ordonez M, Strachan D, Griffin GE, Nutman TB: Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics. J Allergy Clin Immunol. 2003, 111: 995-1000. 10.1067/mai.2003.1348.PubMedView ArticleGoogle Scholar
- Cooper PJ, Barreto ML, Rodrigues LC: Human allergy and geohelminth infections: a review of the literature and a proposed conceptual model to guide the investigation of possible causal associations. Br Med Bull. 2006, 79-80: 203-218. 10.1093/bmb/ldl015.PubMedView ArticleGoogle Scholar
- Oliver-Gonzalez J, Hurlbrink P, Conde E, Kagan IG: Serologic activity of antigen isolated from the body fluid of Ascaris suum. J Immunol. 1969, 103: 15-19.PubMedGoogle Scholar
- Pritchard DI, Quinnell RJ, McKean PG, Walsh L, Leggett KV, et al: Antigenic cross-reactivity between Necator americanus and Ascaris lumbricoides in a community in Papua New Guinea infected predominantly with hookworm. Trans R Soc Trop Med Hyg. 1991, 85: 511-514. 10.1016/0035-9203(91)90239-U.PubMedView ArticleGoogle Scholar
- McWilliam AS, Stewart GA, Turner KJ: An immunochemical investigation of the allergens from Ascaris suum perienteric fluid. Cross-reactivity, molecular weight distribution and correlation with phospho-rylcholine-containing components. Int Arch Allergy Appl Immunol. 1987, 82: 125-132. 10.1159/000234177.PubMedView ArticleGoogle Scholar
- Lozano MJ, Martin HL, Diaz SV, Manas AI, Valero LA, Campos BM: Cross-reactivity between antigens of Anisakis simplex s.l. and other ascarid nematodes. Parasite. 2004, 11: 219-223.PubMedView ArticleGoogle Scholar
- Bhattacharyya T, Santra A, Majumder DN, Chatterjee BP: Possible approach for serodiagnosis of ascariasis by evaluation of immunoglobulin G4 response using Ascaris lumbricoides somatic antigen. J Clin Microbiol. 2001, 39: 2991-2994. 10.1128/JCM.39.8.2991-2994.2001.PubMedPubMed CentralView ArticleGoogle Scholar
- Araujo CA, Perini A, Martins MA, Macedo MS, Macedo-Soares MF: PAS-1, a protein from Ascaris suum, modulates allergic inflammation via IL-10 and IFN-gamma, but not IL-12. Cytokine. 2008, 44: 335-341. 10.1016/j.cyto.2008.09.005.PubMedView ArticleGoogle Scholar
- Tsuji N, Miyoshi T, Islam MK, Isobe T, Yoshihara S, et al: Recombinant Ascaris 16-Kilodalton protein-induced protection against Ascaris suum larval migration after intranasal vaccination in pigs. J Infect Dis. 2004, 190: 1812-1820. 10.1086/425074.PubMedView ArticleGoogle Scholar
- Islam MK, Miyoshi T, Tsuji N: Vaccination with recombinant Ascaris suum 24-kilodalton antigen induces a Th1/Th2-mixed type immune response and confers high levels of protection against challenged Ascaris suum lung-stage infection in BALB/c mice. Int J Parasitol. 2005, 35: 1023-1030. 10.1016/j.ijpara.2005.03.019.PubMedView ArticleGoogle Scholar
- Acevedo N, Sánchez J, Erler A, Mercado D, Briza P, et al: IgE cross-reactivity between Ascaris and domestic mite allergens: the role of tropomyosin and the nematode polyprotein ABA-1. Allergy. 2009, 64: 1635-1643. 10.1111/j.1398-9995.2009.02084.x.PubMedView ArticleGoogle Scholar
- Kennedy MW: The nematode polyprotein allergens/antigens. Parasitol Today. 2000, 16: 373-380. 10.1016/S0169-4758(00)01743-9.PubMedView ArticleGoogle Scholar
- Xia Y, Spence HJ, Moore J, Heaney N, McDermott L, et al: The ABA-1 allergen of Ascaris lumbricoides: sequence polymorphism, stage and tissue-specific expression, lipid binding function, and protein biophysical properties. Parasitology. 2000, 120 (Pt 2): 211-224.PubMedView ArticleGoogle Scholar
- Christie JF, Dunbar B, Kennedy MW: The ABA-1 allergen of the nematode Ascaris suum: epitope stability, mass spectrometry, and N-terminal sequence comparison with its homologue in Toxocara canis. Clin Exp Immunol. 1993, 92: 125-132.PubMedPubMed CentralView ArticleGoogle Scholar
- McSharry C, Xia Y, Holland CV, Kennedy MW: Natural immunity to Ascaris lumbricoides associated with immunoglobulin E antibody to ABA-1 allergen and inflammation indicators in children. Infect Immun. 1999, 67: 484-489.PubMedPubMed CentralGoogle Scholar
- Turner JD, Faulkner H, Kamgno J, Kennedy MW, Behnke J, Boussinesq M, Bradley JE: Allergen-specific IgE and IgG4 are markers of resistance and susceptibility in a human intestinal nematode infection. Microbes Infect. 2005, 7: 990-996. 10.1016/j.micinf.2005.03.036.PubMedView ArticleGoogle Scholar
- Kennedy MW, Brass A, McCruden AB, Price NC, Kelly SM, Cooper A: The ABA-1 allergen of the parasitic nematode Ascaris suum: fatty acid and retinoid binding function and structural characterization. Biochemistry. 1995, 34: 6700-6710. 10.1021/bi00020a015.PubMedView ArticleGoogle Scholar
- Christie JF, Dunbar B, Davidson I, Kennedy MW: N-terminal amino acid sequence identity between a major allergen of Ascaris lumbricoides and Ascaris suum, and MHC-restricted IgE responses to it. Immunology. 1990, 69: 596-602.PubMedPubMed CentralGoogle Scholar
- Hagel I, Cabrera M, Hurtado MA, Sanchez P, Puccio F, Di Prisco MC, Palenque M: Infection by Ascaris lumbricoides and bronchial hyper reactivity: an outstanding association in Venezuelan school children from endemic areas. Acta Trop. 2007, 103: 231-241. 10.1016/j.actatropica.2007.06.010.PubMedView ArticleGoogle Scholar
- Lopez N, de Barros-Mazon S, Vilela MM, Condino Neto A, Ribeiro JD: Are immunoglobulin E levels associated with early wheezing? A prospective study in Brazilian infants. Eur Respir J. 2002, 20: 640-645. 10.1183/09031936.02.00219302.PubMedView ArticleGoogle Scholar
- WHO Weekly Epidemiological Records. Soil-transmitted helminthiasis. 2008, Geneva, 83: 237-252.Google Scholar
- Cooper PJ, Moncayo AL, Guadalupe I, Benitez S, Vaca M, Chico M, Griffin GE: Repeated treatments with albendazole enhance Th2 responses to Ascaris Lumbricoides, but not to aeroallergens, in children from rural communities in the Tropics. J Infect Dis. 2008, 198: 1237-1242. 10.1086/591945.PubMedPubMed CentralView ArticleGoogle Scholar
- Endara P, Vaca M, Chico ME, Erazo S, Oviedo G, et al: Long-term periodic anthelmintic treatments are associated with increased allergen skin reactivity. Clin Exp Allergy. 2010, 40: 1669-1677. 10.1111/j.1365-2222.2010.03559.x.PubMedPubMed CentralView ArticleGoogle Scholar
- Watanabe K, Mwinzi PN, Black CL, Muok EM, Karanja DM, Secor WE, Colley DG: T regulatory cell levels decrease in people infected with Schistosoma mansoni on effective treatment. Am J Trop Med Hyg. 2007, 77: 676-682.PubMedPubMed CentralGoogle Scholar
- Mutapi F, Hagan P, Woolhouse ME, Mduluza T, Ndhlovu PD: Chemotherapy-induced, age-related changes in antischistosome antibody responses. Parasite Immunol. 2003, 25: 87-97. 10.1046/j.1365-3024.2003.00610.x.PubMedView ArticleGoogle Scholar
- Mutapi F, Ndhlovu PD, Hagan P, Woolhouse ME: Changes in specific anti-egg antibody levels following treatment with praziquantel for Schistosoma haematobium infection in children. Parasite Immunol. 1998, 20: 595-600. 10.1046/j.1365-3024.1998.00192.x.PubMedView ArticleGoogle Scholar
- Maizels RM, Yazdanbakhsh M: Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol. 2003, 3: 733-744. 10.1038/nri1183.PubMedView ArticleGoogle Scholar
- Woolhouse ME, Hagan P: Seeking the ghost of worms past. Nat Med. 1999, 5: 1225-1227. 10.1038/15169.PubMedView ArticleGoogle Scholar
- Blish CA, Sangare L, Herrin BR, Richardson BA, John-Stewart G, Walson JL: Changes in plasma cytokines after treatment of ascaris lumbricoides infection in individuals with HIV-1 infection. J Infect Dis. 2010, 201: 1816-1821. 10.1086/652784.PubMedPubMed CentralView ArticleGoogle Scholar
- Jenkins RE, Taylor MJ, Gilvary NJ, Bianco AE: Tropomyosin implicated in host protective responses to microfilariae in onchocerciasis. Proc Natl Acad Sci USA. 1998, 95: 7550-7555. 10.1073/pnas.95.13.7550.PubMedPubMed CentralView ArticleGoogle Scholar
- Acevedo N, Sanchez J, Zakzuk J, Quiroz C, Martínez D, et al: Identification of risk factors for asthma and allergic sensitization in a tropical environment. Allergy. 2010, 65: 661-Google Scholar
- Williams-Blangero S, VandeBerg JL, Subedi J, Aivaliotis MJ, Rai DR, et al: Genes on chromosomes 1 and 13 have significant effects on Ascaris infection. Proc Natl Acad Sci USA. 2002, 99: 5533-5538. 10.1073/pnas.082115999.PubMedPubMed CentralView ArticleGoogle Scholar
- Acevedo N, Mercado D, Vergara C, Sánchez J, Kennedy MW, et al: Association between total immunoglobulin E and antibody responses to naturally acquired Ascaris lumbricoides infection and polymorphisms of immune system-related LIG4, TNFSF13B and IRS2 genes. Clin Exp Immunol. 2009, 157: 282-290. 10.1111/j.1365-2249.2009.03948.x.PubMedPubMed CentralView ArticleGoogle Scholar
- Gerrard JW, Geddes CA, Reggin PL, Gerrard CD, Horne S: Serum IgE levels in white and metis communities in Saskatchewan. Ann Allergy. 1976, 37: 91-100.PubMedGoogle Scholar
- Strachan DP: Hay fever, hygiene, and household size. BMJ. 1989, 299: 1259-1260. 10.1136/bmj.299.6710.1259.PubMedPubMed CentralView ArticleGoogle Scholar
- Strachan DP: Family size, infection and atopy: the first decade of the "hygiene hypothesis.". Thorax. 2000, 55 (Suppl 1): S2-S10.PubMedPubMed CentralView ArticleGoogle Scholar
- von Mutius E, Radon K: Living on a farm: impact on asthma induction and clinical course. Immunol Allergy Clin North Am. 2008, 28: 631-647. 10.1016/j.iac.2008.03.010. ix-xPubMedView ArticleGoogle Scholar
- Holt PG: Environmental factors and primary T-cell sensitisation to inhalant allergens in infancy: reappraisal of the role of infections and air pollution. Pediatr Allergy Immunol. 1995, 6: 1-10. 10.1111/j.1399-3038.1995.tb00250.x.PubMedView ArticleGoogle Scholar
- Gereda JE, Leung DY, Thatayatikom A, Streib JE, Price MR, Klinnert MD, Liu AH: Relation between house-dust endotoxin exposure, type 1 T-cell development, and allergen sensitisation in infants at high risk of asthma. Lancet. 2000, 355: 1680-1683. 10.1016/S0140-6736(00)02239-X.PubMedView ArticleGoogle Scholar
- Bjorksten B: Genetic and environmental risk factors for the development of food allergy. Curr Opin Allergy Clin Immunol. 2005, 5: 249-253. 10.1097/01.all.0000168790.82206.17.PubMedView ArticleGoogle Scholar
- Von Ehrenstein OS, Von Mutius E, Illi S, Baumann L, Bohm O, von Kries R: Reduced risk of hay fever and asthma among children of farmers. Clin Exp Allergy. 2000, 30: 187-193. 10.1046/j.1365-2222.2000.00801.x.PubMedView ArticleGoogle Scholar
- Turner JD, Jackson JA, Faulkner H, Behnke J, Else KJ, et al: Intensity of intestinal infection with multiple worm species is related to regulatory cytokine output and immune hyporesponsiveness. J Infect Dis. 2008, 197: 1204-1212. 10.1086/586717.PubMedView ArticleGoogle Scholar
- van den Biggelaar AH, van Ree R, Rodrigues LC, Lell B, Deelder AM, Kremsner PG, Yazdanbakhsh M: Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet. 2000, 356: 1723-1727. 10.1016/S0140-6736(00)03206-2.PubMedView ArticleGoogle Scholar
- Holt PG: Parasites, atopy, and the hygiene hypothesis: resolution of a paradox?. Lancet. 2000, 356: 1699-1701. 10.1016/S0140-6736(00)03198-6.PubMedView ArticleGoogle Scholar
- Cooper PJ, Chico ME, Bland M, Griffin GE, Nutman TB: Allergic symptoms, atopy, and geohelminth infections in a rural area of Ecuador. Am J Respir Crit Care Med. 2003, 168: 313-317. 10.1164/rccm.200211-1320OC.PubMedView ArticleGoogle Scholar
- Turner KJ, Quinn EH, Anderson HR: Regulation of asthma by intestinal parasites. Investigation of possible mechanisms. Immunology. 1978, 35: 281-288.PubMedPubMed CentralGoogle Scholar
- Lynch NR, Lopez RI, Di Prisco-Fuenmayor MC, Hagel I, Medouze L, et al: Allergic reactivity and socio-economic level in a tropical environment. Clin Allergy. 1987, 17: 199-207. 10.1111/j.1365-2222.1987.tb02004.x.PubMedView ArticleGoogle Scholar
- Yazdanbakhsh M, van den Biggelaar A, Maizels RM: Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol. 2001, 22: 372-377. 10.1016/S1471-4906(01)01958-5.PubMedView ArticleGoogle Scholar
- Yazdanbakhsh M, Kremsner PG, van Ree R: Allergy, parasites, and the hygiene hypothesis. Science. 2002, 296: 490-494. 10.1126/science.296.5567.490.PubMedView ArticleGoogle Scholar
- Yazdanbakhsh M, Matricardi PM: Parasites and the hygiene hypothesis: regulating the immune system?. Clin Rev Allergy Immunol. 2004, 26: 15-24. 10.1385/CRIAI:26:1:15.PubMedView ArticleGoogle Scholar
- Scrivener S, Yemaneberhan H, Zebenigus M, Tilahun D, Girma S, et al: Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: a nested case-control study. Lancet. 2001, 358: 1493-1499. 10.1016/S0140-6736(01)06579-5.PubMedView ArticleGoogle Scholar
- Platts-Mills TA, Cooper PJ: Differences in asthma between rural and urban communities in South Africa and other developing countries. J Allergy Clin Immunol. 2010, 125: 106-107. 10.1016/j.jaci.2009.10.068.PubMedView ArticleGoogle Scholar
- Johansson SG, Mellbin T, Vahlquist B: Immunoglobulin levels in Ethiopian preschool children with special reference to high concentrations of immunoglobulin E (IgND). Lancet. 1968, 1: 1118-1121.PubMedView ArticleGoogle Scholar
- Nutman TB, Hussain R, Ottesen EA: IgE production in vitro by peripheral blood mononuclear cells of patients with parasitic helminth infections. Clin Exp Immunol. 1984, 58: 174-182.PubMedPubMed CentralGoogle Scholar
- Kojima S, Yokogawa M, Tada T: Raised levels of serum IgE in human helminthiases. Am J Trop Med Hyg. 1972, 21: 913-918.PubMedGoogle Scholar
- Turner KJ, Feddema L, Quinn EH: Non-specific potentiation of IgE by parasitic infections in man. Int Arch Allergy Appl Immunol. 1979, 58: 232-236. 10.1159/000232197.PubMedView ArticleGoogle Scholar
- Turner KJ, Baldo BA, Anderson HR: Asthma in the highlands of New Guinea Total IgE levels and incidence of IgE antibodies to house dust mite and Ascaris lumbricoides. Int Arch Allergy Appl Immunol. 1975, 48: 784-799. 10.1159/000231367.PubMedView ArticleGoogle Scholar
- Lynch NR, Lopez R, Isturiz G, Tenias-Salazar E: Allergic reactivity and helminthic infection in Amerindians of the Amazon Basin. Int Arch Allergy Appl Immunol. 1983, 72: 369-372. 10.1159/000234899.PubMedView ArticleGoogle Scholar
- Gelpi AP, Mustafa A: Seasonal pneumonitis with eosinophilia. A study of larval ascariasis in Saudi Arabs. Am J Trop Med Hyg. 1967, 16: 646-657.PubMedGoogle Scholar
- Loffler W: Transient lung infiltrations with blood eosinophilia. Int Arch Allergy Appl Immunol. 1956, 8: 54-59. 10.1159/000228268.PubMedView ArticleGoogle Scholar
- Stromberg BE: Potentiation of the reaginic (IgE) antibody response to ovalbumin in the guinea pig with a soluble metabolic product from Ascaris suum. J Immunol. 1980, 125: 833-836.PubMedGoogle Scholar
- Marretta J, Casey FB: Effect of Ascaris suum and other adjuvants on the potentiation of the IgE response in guinea-pigs. Immunology. 1979, 37: 609-613.PubMedPubMed CentralGoogle Scholar
- Lee TD, McGibbon A: Potentiation of IgE responses to third-party antigens mediated by Ascaris suum soluble products. Int Arch Allergy Immunol. 1993, 102: 185-190. 10.1159/000236570.PubMedView ArticleGoogle Scholar
- Holland MJ, Harcus YM, Riches PL, Maizels RM: Proteins secreted by the parasitic nematode Nippostrongylus brasiliensis act as adjuvants for Th2 responses. Eur J Immunol. 2000, 30: 1977-1987. 10.1002/1521-4141(200007)30:7<1977::AID-IMMU1977>3.0.CO;2-3.PubMedView ArticleGoogle Scholar
- Leonardi-Bee J, Pritchard D, Britton J: Asthma and current intestinal parasite infection: systematic review and meta-analysis. Am J Respir Crit Care Med. 2006, 174: 514-523. 10.1164/rccm.200603-331OC.PubMedView ArticleGoogle Scholar
- Palmer LJ, Celedon JC, Weiss ST, Wang B, Fang Z, Xu X: Ascaris lumbricoides infection is associated with increased risk of childhood asthma and atopy in rural China. Am J Respir Crit Care Med. 2002, 165: 1489-1493. 10.1164/rccm.2107020.PubMedView ArticleGoogle Scholar
- Takeuchi H, Zaman K, Takahashi J, Yunus M, Chowdhury HR, et al: High titre of anti-Ascaris immunoglobulin E associated with bronchial asthma symptoms in 5-year-old rural Bangladeshi children. Clin Exp Allergy. 2008, 38: 276-282.PubMedView ArticleGoogle Scholar
- Hunninghake GM, Soto-Quiros ME, Avila L, Ly NP, Liang C, et al: Sensitization to Ascaris lumbricoides and severity of childhood asthma in Costa Rica. J Allergy Clin Immunol. 2007, 119: 654-661. 10.1016/j.jaci.2006.12.609.PubMedView ArticleGoogle Scholar
- Obihara CC, Beyers N, Gie RP, Hoekstra MO, Fincham JE, et al: Respiratory atopic disease, Ascaris-immunoglobulin E and tuberculin testing in urban South African children. Clin Exp Allergy. 2006, 36: 640-648. 10.1111/j.1365-2222.2006.02479.x.PubMedView ArticleGoogle Scholar
- Dold S, Heinrich J, Wichmann HE, Wjst M: Ascaris-specific IgE and allergic sensitization in a cohort of school children in the former East Germany. J Allergy Clin Immunol. 1998, 102: 414-420. 10.1016/S0091-6749(98)70129-0.PubMedView ArticleGoogle Scholar
- Alcantara-Neves NM, Badaro SJ, dos Santos MC, Pontes-de-Carvalho L, Barreto ML: The presence of serum anti-Ascaris lumbricoides IgE antibodies and of Trichuris trichiura infection are risk factors for wheezing and/or atopy in preschool-aged Brazilian children. Respir Res. 2010, 11: 114-10.1186/1465-9921-11-114.PubMedPubMed CentralView ArticleGoogle Scholar
- Lynch NR, Hagel IA, Palenque ME, Di Prisco MC, Escudero JE, et al: Relationship between helminthic infection and IgE response in atopic and nonatopic children in a tropical environment. J Allergy Clin Immunol. 1998, 101: 217-221. 10.1016/S0091-6749(98)70386-0.PubMedView ArticleGoogle Scholar
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