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Article

Toxocara spp. Infection Influences on Eosinophil Levels: An Immunological Indicator of Severe Asthma and Allergy

by
Raphael Chagas Silva
1,*,
Márcia Barbosa da Silva
1,
Alana Alcantara Galvão
1,
Jamile Souza Fernandes
2,3,
Gabriela Pimentel Pinheiro
2,
Álvaro A. Cruz
2,
Carina da Silva Pinheiro
1 and
Neuza Maria Alcântara-Neves
1
1
Laboratory of Allergology and Acarology (LAA), Institute of Health Sciences, Universidade Federal da Bahia, Salvador 40110-902, Brazil
2
Program of Asthma and Rhinitis Control-Bahia (ProAR), Universidade Federal da Bahia, Salvador 41940-455, Brazil
3
Center for Biological and Health Sciences, Universidade Federal do Oeste da Bahia, Barreiras 47805-100, Brazil
*
Author to whom correspondence should be addressed.
Allergies 2025, 5(3), 24; https://doi.org/10.3390/allergies5030024
Submission received: 21 February 2025 / Revised: 1 April 2025 / Accepted: 30 June 2025 / Published: 3 July 2025
(This article belongs to the Section Asthma/Respiratory)
Browse Figure
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Abstract

Background/Objectives: Toxocara spp. infection has been associated with severe asthma and allergic manifestations due to the activation of eosinophils by the release of Th2 cell cytokines. The aim of this study was to investigate the association between Toxocara spp. infection and eosinophil levels in severe asthmatic patients. Methods: The socio-demographic, peripheral blood eosinophils counting total IgE, sIgE to aeroallergens and FEV1 results were acquired from the Program of Asthma and Rhinitis Control (ProAR) at the Salvador–Brazil databank; IgG anti-Toxocara spp. levels were measured in 176 severely asthmatic patients by indirect ELISA. Results: The Toxocara spp. seroprevalence was 50.6%. Eosinophilia was present in 54% of the population. The correlation between IgG anti-Toxocara spp. levels and eosinophils levels was positive. Eosinophilic individuals with SPT, sIgE for D. pteronyssinus, D. farinae and B. tropicalis showed positive results; IgE ≥ 160 UI/dL and uncontrolled asthma presented more positive results for IgG anti-Toxocara spp. Conclusions: Our findings suggest that eosinophil levels are influenced by the presence of IgG antibodies against Toxocara spp. Additionally, helminth infection may modulate immunological responses in allergies and uncontrolled asthma, which could help explain the exacerbation of asthma symptoms.

1. Introduction

Asthma is a multifactorial respiratory chronic disease distributed globally, mainly in developing countries [1,2]. Asthma is more frequent in atopic individuals; these atopic individuals produce a higher amount of Immunoglobulin E (IgE) when in contact with certain molecules (allergens) that are otherwise innocuous for non-atopic individuals. However, it is a multifactorial disease where genetic and environmental factors may play a part, such as genetic polymorphisms [3,4], hormones, lifestyle, adherence to treatment issues and helminth infections [5,6]. The majority of asthma cases are associated with sensitization to house dust mites (Dermatophagoides pteronyssinus, Dermatophagoides farinae and Blomia tropicalis) and pollens, depending on the geographic region, due to the environmental exposures to these allergens [7]. The severity of atopic asthma is related to immunological mechanisms that include a strong Th2 response characterized by eosinophils, elevated IgE, mast cells, macrophages and basophils levels, which together are able to produce an inflammatory process in the respiratory tract [8]. In tropical regions, the coexistence of helminth infections may enhance asthma prevalence and pathogenesis, worsening its morbidity as a result of increased Th2 immunological responses [9,10].
The roundworms Toxocara spp. (T. canis and T. cati) cause the most prevalent helminthic disease in humans, toxocariasis. Toxocariasis is a zoonosis where humans are paratenic hosts; it is one of the most neglected diseases worldwide [11]. This parasite infection is more prevalent in countries with lower incomes and poor sanitation conditions, which increases the necessity of studies in these regions in order to control their prevalence and morbidity [12]. Human infections by Toxocara spp. occur accidentally after the ingestion of embryonated eggs in the soil or contaminated food [13]; their larvae penetrate the small intestine and migrate to different body tissues for many years [12]. Many studies have shown that the migratory process of the larvae triggers Th2 cell activation, releasing leukotrienes, eotaxins and the proinflammatory cytokines IL-4, IL-5 and IL-13 [14,15]. In addition, the IL-5 cytokine acts by increasingly recruiting eosinophils in the blood and tissues, resulting in eosinophilic inflammation. Furthermore, patients who are seropositive for Toxocara spp. showed elevated serum IgE levels that may be due to the increased number and activity of T cells exhibiting a cytokine secretion profile; this is particularly true with IL-4 which promotes B cell class switching and leads to the production of parasite-specific IgE, specifically against the excretory–secretory antigen [16] present in the cuticle of T. canis larvae [8]. Moreover, the Th2 response orchestrates IgE-mediated defenses by activating mast cells, basophils and eosinophils through FcεRI crosslinking, leading to degranulation and helminth damage/expulsion. While this mechanism is protective against parasites, it is also exploited in allergic reactions (where harmless antigens trigger similar pathways) [17].
During T. canis infection, the high level of eosinophils is a potent controller of helminthiasis, playing a protective role by activating specific T-cell responses against the helminth infection [18]. Notwithstanding, some studies suggested that the protective mechanism and eosinophil levels decrease in chronic helminth infections is due to the release of IL-10 by Treg cells [19] in a mechanism called modified Th2 response [20]. The levels of eosinophil may be used to determine the timing of helminth infections, contributing to immunodiagnostic accuracy.
The participation of helminth infections in eosinophil production in severe asthmatic patients is not fully understood yet. In spite of all the groups of severe asthmatic patients in this study being under treatment with inhaled corticosteroids (Fluticasone or β-adrenergic), many of them showed high levels of blood eosinophil, and we believe that one of the reasons for this could be the co-morbidity of the Toxocara spp. infection. Thus, in this study, we investigated the association between toxocariasis and eosinophil levels and the association of this helminth infection with severe asthma and allergic markers in eosinophilic individuals assisted by the Programa para o Controle da Asma na Bahia (ProAR).

2. Materials and Methods

2.1. Study Population

The studied population was composed of 176 severely asthmatic patients aged 19–82 years old, residing in urban or rural areas of Salvador, Bahia, Brazil. They were recruited voluntarily from the Programa para o Controle da Asma na Bahia (ProAR) located in Salvador, an important health care center that treats people bearing allergic diseases (asthma and rhinitis). The case group consists of individuals who tested positive for IgG anti-Toxocara spp. (n = 89), whereas the control group comprises individuals who tested negative for IgG anti-Toxocara spp. (n = 87). These individuals were selected according to a severe asthma status confirmed by two specialized doctors following the Global Initiative Against Asthma questionaries’ (GINA, 2006) [21]. In addition, severely asthmatic patients were diagnosed according to the following symptoms: daily or continuous asthma symptoms (wheezing, cough, chest tightness); limited activities daily (symptoms with minor efforts); frequent exacerbation, or nocturnal asthma symptoms ≥ 2 times a week; FEV 1 or PEF ≤ 60%; or the use of bronchodilators ≥ 2 times a day. In contrast, uncontrolled asthma was determined by the following GINA criteria: the patient presented three or more episodes of the above-cited symptoms, a need for reliever/rescue treatment and FEV 1 ≤ 80% (GINA, 2012) [22]. In addition, all participants provided socio-demographic information as part of a questionnaire evaluation.
Ethical approvals were obtained from the Ethics Committee of the Maternidade Climatério de Oliveira of Bahia/Federal University of Bahia (MCOB/UFBA), CONEP 15782-n° 25000.013834/2010-96 as part of a project named “Risk factors, biomarkers and endophenotypes of severe asthma”. Written informed consent was obtained from each subject.

2.2. Blood Sample Collection, Total IgE and sIgE Measurements

Blood samples were collected in heparinized tubes (Benckton Dickson Company, Franklin Lakes, NJ, USA) and used to count the blood cell total. The total serum IgE measurements were carried out by fluorescence enzyme immunoassay (ImmunoCAP, Phadia, Uppsala, Sweden), and the quantifications of the specific IgE of Dermatophagoides farinae, Dermatophagoides pteronyssinus and Blomia tropicalis were determined by the Immunocap technique (Phadia Diagnostics AB, Uppsala, Sweden) [23]. The sIgE-positive results were categorized into three classes depending on the value (class 1: sIgE ≥ 0.35 KU/mL; class 2; sIgE ≥ 0.70 KU/mL; and class 3: sIgE ≥ 3.5 KU/mL); the used category in this study was sIgE ≥ 0.70 KU/mL, following the referent limits for age and sex [24,25], and the atopic status was determined when the individual presented one positive result for at least one of the tested aeroallergens. The adopted criteria to establish eosinophilia in this study was a value equal to or higher than 450 eosinophils/mm3. Furthermore, blood samples were used to detect IgG antibodies against Toxocara spp. by indirect ELISA.

2.3. Skin Prick Tests (SPTs)

The allergic reaction was confirmed by skin prick tests applied on one anterior forearm for the most common aeroallergens, which affect the Salvador population: Dermatophagoides farinae, Dermatophagoides pteronyssinus and Blomia tropicalis using commercial kits (ALK-Abello, Hørsholm, Denmark). Saline and histamine solutions were used as negative and positive controls, respectively. The reaction to each allergen was read after 15 min of application and it was considered positive if the papule diameter was at least 3 mm larger than the negative control papule.

2.4. Sera Absorption with A. lumbricoides Extract

The A. lumbricoides extract was obtained by trituration in liquid nitrogen-frozen adult worms in a phosphate-buffered saline (PBS), pH 7.4, by use of a blender (model 51BL30; Waring Commercial, Torrington, CT, USA). The PBS-soluble fraction obtained by centrifugation was depleted of endotoxin by treatment with Triton X-114 (Sigma, St. Louis, MO, USA), and the protein content was determined by the Lowry method [26]. The Ascaris antigen was stored at −70 °C until use. To prevent potential cross-reactions between IgG antibodies against A. lumbricoides and anti-Toxocara spp. antibodies, the sera underwent a pre-absorption process using 8.0 mg/mL of A. lumbricoides extract per sera. This absorption was conducted in the presence of polyethylene glycol (PEG 15.000—Sigma Chemical Co., San Louis, MO, USA) at a concentration of 3%, along with 0.1% sodium azide, diluted in PBS. Following an incubation period of 30 min at room temperature, the mixture was centrifuged, and the resulting supernatant was subjected to an additional round of absorption. The absorbed material was subsequently frozen at −20 °C until the immunodiagnostic procedure was carried out.

2.5. Detection of IgG Anti-Toxocara spp. Antibodies

Indirect ELISA (Enzyme-Linked Immunosorbent Assay) was carried out to detect IgG anti-Toxocara spp. using secreted–excreted antigens from Toxocara spp. [16] as antigen, produced according to Savigny (1975) [27] and modified by Alcantara-Neves et al. (2008) [16]. In summary, 96-well plates were sensitized, with 3 μg/mL of TES diluted in carbonate/bicarbonate buffer overnight at 4 °C. The plates were blocked with a solution of PBS containing 10% of fetal bovine serum (FBS—Thermo Fisher Scientific Inc, Waltham, MA, USA). The sera were diluted at 1:1000 in a solution of PBS/5% between 20 and 2.5% fetal bovine serum (PBS/T/FBS). After sera incubation, the biotinylated anti-human IgG conjugate was diluted at 1:4000 (BD Pharmingen, San Diego, CA, USA) in PBS/T/FBS, followed by Streptavidin-peroxidase (Streptoavidin-HRP, BD Pharmingen, San Diego, CA, USA) being diluted at 1:500 in PBS/T/FBS. Hydrogen peroxide (H2O2) and OPD (o-Phenylenediamine-Sigma Chemical Co., San Louis, MO, USA) were used as substrates and chromogens. The incubation time for the conjugate was 30 min at room temperature. The reaction was stopped with 2N sulfuric acid, and the optical density was determined using a 490 nm filter. In addition, washes were made between each step using PBS/5% between 20 (over three times) and PBS 1X (one time at the last wash).
After measuring the optical densities (ODs), the cut-off value of the assay was determined using 10 negative control sera (from individuals with total IgE ≤ 100 UI/mL, eosinophils ≤ 2% and no parasite infections detected by stool examination). The cut-off value was determined as the mean optical densities plus three times the standard deviation. The reached cut-off value for IgG antibodies to Toxocara spp. positivity was ≥0.29.

2.6. Statistical Analyses

Frequency rates and associations between each risk factor and seropositivity were achieved by performing univariate and multivariate logistic regression analyses, with age, gender, atopy status, salary and habitation used as confounding variables, respecting odds ratio values and the confidence interval (95%). For analyzing the blood eosinophil count and outcome associations, we used the following arbitrary eosinophil categorizations: low (≤100 mm3), intermediary (>100 mm3 ≤ 449 mm3) and high (≥450 mm3). The Pearson Qui-Square test (χ2) was performed using individual eosinophilic (≥450 mm3) and non-eosinophilic (<450 mm3) with complete data to reach the differences between IgG antibodies for Toxocara spp. outcomes proportion and clinical variables (skin prick test, sIgE ≥ 0.70 KU/L to D. farinae, sIgE ≥ 0.70 KU/L to D. pteronyssinus, sIgE ≥ 0.70 KU/L to B. tropicalis, total IgE ≥ 160 KU/L and uncontrolled asthma). In this analysis, only individuals who tested positive for sIgE to one specific aeroallergen were included. Those with positive results for more than one of the tested aeroallergen were excluded. The analyses were made by the Statistical Package for the Social Sciences (SPSS, v. 17.0).
For all 176 asthmatic individuals, we evaluated the correlation between the value of blood eosinophils (number of eosinophils) and the optical densities (ODs) of IgG anti-Toxocara spp. and then we built an Ordinary Least Square (OLS) linear simple regression model [28].

3. Results

3.1. Characteristics of the Study Population

We evaluated 176 patients, including the case group of IgG anti-Toxocara-positive individuals (n = 89) and the control group of IgG anti-Toxocara-negative individuals (n = 87) (Table 1). The groups were composed of a majority of females, and the ages between the case and control groups were similar (median; 50 and 49, respectively), but it is worth noting that the subjects from the case group showed a higher frequency of clinical variables. In the case group, the median of the number of eosinophils per cells/mm3 in the peripheral blood was 659 cells per mm3 (83–2.088); the total IgE was 360 UI/dl (8.86–3.000); the skin prick test results were positive; and the interquartile range of FEV 1, FVC predict values, inhaled corticoid treatment, exacerbation and hospitalization frequencies were higher in the case group. In addition, uncontrolled asthma was more frequent in the case group as well (Table 1).
The results from the seroprevalence showed that 89 participants (50.6%) tested positive for IgG anti-Toxocara spp. Most of the participants in this study were women, 135/176 (76%), and in this group, 67 (49%) presented positive for the serum reagent for IgG anti-Toxocara spp. The outcomes showed that 119 participants were more than 45 years old and 67 (56%) were serum reagents for the IgG anti-Toxocara spp. antigen (Table 2). Living in a rural area was found to be associated with a lower probability of acquiring the Toxocara spp. infection. No more significant associations were observed in these analyses (Table 2).

3.2. Risk Factors Between Seropositivities and Eosinophils

The results from the serum reagent to Toxocara spp. showed an association with low eosinophils (<100 mm3). On the other hand, serum reagents for IgG anti-Toxocara spp. displayed a risk factor for eosinophils equal to or higher than 450 mm3. Among the 26 severely asthmatic patients bearing intermediary eosinophils (>100 < 450 mm3), no association was found (Table 3).

3.3. Influence of Toxocara spp. Antibody on Eosinophil Numbers

The analysis of the optical density values of the IgG antibody and the number of eosinophils showed that for IgG anti-Toxocara spp., the positive effect had a Pearson r of 0.4359, explaining 19% of the variance of the number of eosinophils (Figure 1). Nonetheless, it was evident that the number of positive individuals for Toxocara spp. (see the number of dots above the red line in Figure 1) is higher than the number of negative individuals.

3.4. Association Between Clinical Indicators of Asthma Severity and Toxocara spp. (Under Eosinophilia)

As we show in Table 3, a significantly higher number of eosinophils were associated with individuals who reacted positively to IgG anti-Toxocara spp. The individuals were stratified into two groups based on eosinophil counts: those with eosinophils ≥ 450 mm3 and those with eosinophils < 450 mm3. We then assessed the association between IgG anti-Toxocara spp. seropositivity and the clinical markers of severe asthma using the chi-square test. Among eosinophilic individuals, a significantly higher proportion of IgG anti-Toxocara spp. positivity was observed in those with specific clinical indicators. The positive proportion of skin prick test-positive individuals was 65% (χ2 = 4.749, p = 0.03); sIgE ≥ 0.70 KU/L to D. farinae was 67% (χ2 = 5.565, p = 0.01); sIgE ≥ 0.70 KU/L to D. pteronyssinus was 67% (χ2 = 5.233, p = 0.02); sIgE ≥ 0.70 KU/L to B. tropicalis was 65% (χ2 = 4.083, p = 0.04); and the total IgE ≥ 160 UI/dl of the proportion was 67% (8.667, p = 0.003). Additionally, among participants with uncontrolled asthma, 64% exhibited serum reactivity to Toxocara antigens (χ2 = 3.769, p = 0.05). In contrast, no significant associations were found in the non-eosinophilic group (Table 4).

4. Discussion

It is known that the active immunological responses of helminth infections culminate with Th2 cell activation and increase blood eosinophil levels, mainly during the larvae migration process and tissue invasions [19]. The increased eosinophil levels are intrinsically associated with the severity of many allergic diseases including allergic dermatitis and asthma [29]. In addition, helminth infections are capable of modulating immunological responses, influencing atopic features by increasing IgE levels and, thus, worsening the asthma and allergic conditions [30]. To supplement the scarcity of data on the baseline of serological helminth infections in humans, in this study, we explored the influence of the Toxocara spp. infection on blood eosinophils and the relationship between infections and severe asthma and allergy markers among eosinophilic individuals.
Studies showed that cases of Toxocara spp. infection occur mostly in males during childhood due to frequent contact with contaminated soils and foods and less hygienic habits [31,32]. Our results showed that elderly women were the group more often infected by Toxocara spp. which may be explained by the fact that elderly people often become pet owners, which increases their exposure to Toxocara spp. antigens [33]. Despite this, we could not perform any analyses using the presence of pets at home due to the lack of information in the PROAR databank; however, in a previous study on our group, we found an association between pets and Toxocara spp. infection which may explain the results we reached; the previous study was also developed in the Salvador-Ba city. The association for those living in small cities was negative (a protective factor for avoiding the infection), which could be indicative of a lower amount of contaminated soil available compared to those living in big cities where there are more parks and green areas that are contaminated with Toxocara spp. eggs because of people walking their pets and stray dogs and cats [32,34]. Furthermore, a common habit shared by individuals who live in big cities is to raise domestic animals at home; the outdoor behavior of these animals allows them to carry infective eggs on their fur into homes, increasing human exposure to Toxocara spp. eggs [35].
Moreover, helminth infections are associated with the modulation of immunological responses, including a raised number of eosinophils in the blood and in tissues during the larvae migration [18,36]. Eosinophils participate in directing the inflammation process as a mediator of cytokine production being directly associated with the severity of asthma disease [29]. In addition, for the majority of helminth infections, the appearance of symptoms depends on time of infection, parasitic load and infection degree, especially in ascariasis cases [37,38]. Most toxocariasis cases remain asymptomatic and the IgG antibody dosages are not always capable of giving an accurate diagnosis for this infection; for instance, even in serum reacting with IgG anti-Toxocara spp., it is not possible to identify the infection phase by applying an IgG antibody investigation [39]. Therefore, eosinophils evaluation could be used as an additional but secondary tool for the diagnosis of toxocariasis.
According to Rodolpho and collaborators (2018) [19], in vitro eosinophil activation and increasing levels occur differently, depending on helminth loads, longer exposure of antigens, stimulatory signals between MHC and T cell receptors, a second co-stimulatory signal between MHCII and professional APCs or conventional APCs to activate different eosinophil phenotypes in different locations. This information may explain why some helminth-infected individuals did not present blood eosinophilia at early infection.
The majority of individuals in this study had eosinophil levels higher than 450 mm3 and the presence of the helminth was considered a risk factor for raised eosinophil levels; these findings were observed in other helminth studies [40,41]. As many studies have described, these increased eosinophil levels in the blood are often related to the larvae stage due to tissue infiltration during the migration process [42,43]. The continuous release of Toxocara spp. antigens in the body modulate the immune system by orchestrating Th2 responses and prompting with IL-4, IL-5 and IL-13 proinflammatory cytokine production by T cells, following hypereosinophilia, which attacks the Toxocara spp. somatic larvae causing eosinophilic granulomas [44]. The long-term effect of larvae migration in the lungs arises due to the development of asthma and pulmonary fibrosis. Moreover, some studies found proteins released by Toxocara spp. [16] inside of granulomas instead of larvae; in other words, the immunological response attempts are not restricted to larvae but also include proteins produced by Toxocara spp. which may enhance the mechanisms of eosinophil activation and inflammatory pathways related to asthma severity [45,46].
Even though in this particular population we observed that helminth infection is a risk factor for increased eosinophils, we explored the relationship between optical densities for IgG for Toxocara spp. antibodies as a way to modulate the number of eosinophils. The results showed a slight increase of eosinophils in a dependent manner of the increase in IgG antibodies, which may be a consequence of the inhibition of the inflammatory features of the corticosteroid usage [47,48]. Many studies have attributed this correlation not only to the fact that helminthiasis can activate Th2 cells but also to the presence of IgG receptors in eosinophils that may activate and enhance their functionality [49,50]. As we minimized the cross-reaction through the sera absorption step, our results were not biased by the IgG anti-A. lumbricoides and anti-Toxocara spp. antibodies cross-reactivity.
Furthermore, since parasitic infections polarize naïve T cells toward a Th2 immune response, it is well established that the IL-4 cytokine released by Th2 cells induces B lymphocytes to undergo immunoglobulin class switching from IgG to IgE. Consequently, elevated IgE levels are frequently observed in the blood of infected individuals, which is also associated with the onset of asthma, eosinophilia and atopic diseases [11,51]. Atopy is a condition characterized by raised total and specific IgE levels and eosinophilia; both inflammatory elements have been associated with Toxocara spp. infection in previous studies [52]. The FcεRI receptor of IgE is also highly expressed in mast cells and basophils, and the exposure to the multivalent antigen (allergens) is sufficient to cross-link FcεRI-bound IgE triggering rapid cell activation; hence, in immediate mast cells and basophils degranulation, releasing histamine, inflammatory mediators and vasodilators elicit acute allergic and inflammatory responses [17]. However, it is still controversial; many studies have demonstrated a negative association between helminth infections and allergic asthma onset and atopy [53,54]. Moreover, stratification by eosinophilia revealed that proportionally asthmatic patients with positive antibodies to Toxocara spp. were frequently individuals with positive skin prick test results, specific IgE to D. farinae, D. pteronyssinus and B. tropicalis. A study performed by Magnaval and collaborators (2006) [55] in a French population suggested that individuals with asymptomatic atopy conditions could have a silenced atopic genotype and after being boosted by Toxocara spp. infection they started to develop atopic symptoms.
Additionally, Silva and collaborators (2017) [56], evaluating the association of Toxocara spp. infection and allergy at Brazil, observed a positive association between seropositivity to Toxocara spp. and specific IgE to aeroallergen to B. tropicalis. Moreover, it was demonstrated that the existence of cross-reactivity between IgE to helminth epitopes and several allergens, especially to house dust mites, has been attributed to the fact that tropomyosin and glutathione-S transferase epitopes are as present in helminth group as in aeroallergens [57]. Fragoso and collaborators (2011) [58] cited another important finding about cross-reactions between helminths and specific aeroallergens; the IgE production could be induced by carbohydrate epitopes present in both pathogens.
It is worth noting that despite all severe asthmatic individuals in this study having used inhaled corticosteroids as a treatment, our results found proportionally more individual IgG anti-Toxocara spp. reagents being uncontrolled in those eosinophilic individuals. The presence of helminths has been associated with the exacerbation of asthmatic symptoms and the diminished effect of asthma treatment by immunological response modulations [59]. As asthma is a multifactorial disease and many immunological mechanisms are involved in asthma exacerbation, Toxocara spp. participation in this mechanism goes beyond increasing eosinophil levels [60]. It has been associated with the fact that individuals with acute helminth infections present more allergic signals stimulated by polyclonal IgE production and the consequential switch from Th0 to Th2 cells and releases of proinflammatory cytokines IL-4, IL-5 and IL-13, inducing a chronic pulmonary inflammation and airway hyper-reactivity and thus worsening the asthma symptoms [61].

5. Conclusions

In conclusion, the serological immunodiagnostics in this study revealed a small difference between the prevalence of individuals testing positive for IgG of Toxocara spp. Overall, gender and age were distinct risk factors in acquiring this infection. Furthermore, the helminthiasis in this study was associated with eosinophilia, which affected the severity of asthma for patients in our group, mainly because our eosinophilic population was associated with asthma exacerbation markers, such as atopy and sIgE for aeroallergens, which may increase the severity of the uncontrolled asthma condition. The understanding of helminth modulations in the immunological responses over eosinophils levels could provide insights regarding how to prevent asthma exacerbation.

Author Contributions

R.C.S., Conceptualization; Methodology; Formal analysis; Writing—original draft; Writing—review and editing. M.B.d.S., Methodology; Formal analysis; Investigation. A.A.G., Methodology; Formal analysis; Investigation. J.S.F., Methodology; Formal analysis; Investigation. G.P.P., Methodology; Investigation; Visualization. Á.A.C., Resources; Investigation; Methodology; Writing—review and editing. C.d.S.P., Formal analysis; Investigation; Methodology; Writing—review and editing. N.M.A.-N., Project administration; Funding acquisition; Resources; Investigation, Writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by Brazilian agencies: CNPQ (307192/2022-9) and CAPES scholarship (88882.452912/2019-01) are acknowledged for funding this project.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Ethics Committee of the Maternidade Climatério de Oliveira of Bahia/Federal University of Bahia (MCOB/UFBA), CONEP 15782-n° 25000.013834/2010-96 as part of a project named “Risk factors, biomarkers and endophenotypes of severe asthma”.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data presented in this study are available on request from the corresponding authors.

Acknowledgments

We are thankful to Brazilian agencies for supporting this study. We are grateful to all individuals who contributed to this work. We are thankful to all the support provided by PROAR.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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Allergies 05 00024 g001
Figure 1. Correlation between anti-Toxocara spp. IgG and the number of blood eosinophils. All points below the red line are negative reagents and all points above the red line are positive reagents. Values of Pearson r, the variance explained by the model (R2), the significance value (p) and the resulting model are also shown.
Figure 1. Correlation between anti-Toxocara spp. IgG and the number of blood eosinophils. All points below the red line are negative reagents and all points above the red line are positive reagents. Values of Pearson r, the variance explained by the model (R2), the significance value (p) and the resulting model are also shown.
Allergies 05 00024 g001
Table 1. Characteristics of the subjects enrolled in the study groups.
Table 1. Characteristics of the subjects enrolled in the study groups.
VariablesIgG Anti-Toxocara spp. Positives (n = 89)IgG Anti-Toxocara spp. Negatives (n = 87)
Male–N (%)22 (25)19 (21.8)
Female–N (%)67 (75)68 (78.2)
Age (years)–median/SD a (IQ range) b50/1.32 (19–82)49/1.4 (20–78)
Total IgE UI/dl–median/SD a (IQ range) b360/65.6 (8.86–3.000)257/77.7 (3.32–3.000)
IgE > 160 UI/dl–N (%)66 (74)54 (62)
Positive SPT c–N (%)60 (67)43 (49)
Blood eosinophil count cells/mm3 -median/SD a (IQ range) b659/46.98 (83.0–2.088)132/21.16 (29–778)
Blood eosinophils < 100 cells/mm3–N (%)23 (27)35 (40)
Blood eosinophils ≥ 100 ≤ 450 cells/mm3–N (%)12 (13)14 (16)
Blood eosinophils ≥ 450 cells/mm3–N (%)54 (60)38 (44)
FEV1 percent of predicted value post-BD–median (IQ range) b86% (43–86)86% (55–62)
FVC percent of predicted value post-BD–median (IQ range) b69% (32–74)74% (38–72)
FVE1/FVC post-BD–median (IQ range) b0.6% (0.42–0.89)0.72% (0.36–0.95)
Age of asthma onset–median/SD b (IQ range) b5/1.4 (1–71)12/1.5 (1–55)
Use of > 880 μg of inhaled Fluticasone/day–N (%)37 (39)31 (35)
Use of inhaled Beta-2 agonists/day–N (%)83 (93)80 (92)
Exacerbation/year (one or more times)–N (%)62 (70)51 (58)
Hospitalization/year (one or more times)–N (%)7 (7)2 (2)
Uncontrolled asthma d–N (%)55 (62)40 (46)
a Standard Deviation. b Interquartile range. c Skin prick test to relevant aeroallergens. d According to GINA criteria.
Table 2. Socio-demographic characteristics of the study population, antibody responses for Toxocara spp. and the association of risk factors for the infection.
Table 2. Socio-demographic characteristics of the study population, antibody responses for Toxocara spp. and the association of risk factors for the infection.
Variables (N)IgG Anti-Toxocara spp.
Negative (n = 87)Positive (n = 89)
n/N (%)		OR crudeOR adjusted
n/N (%)
Gender
Female 68/135 (51)67/135 (49)11
Male 19/41 (46)22/41 (54)1.17 (0.58–2.36)0.99 (0.47–2.07)
Age
≤44 35/57 (61)22/57 (39)11
≥45 52/119 (44)67/119 (56)2.05 (1.07–3.90) *2.35 (1.11–4.96) *
Rural area
No 33/78 (42)45/78 (58)11
Yes 53/97 (55)44/97 (45)0.62 (0.34–1.14)0.50 (0.26–0.95) *
Salary
≤1 salary 45/88 (51)43/88 (49)11
>1 salary 42/88 (48)46/88 (52)1.14 (0.63–2.07)1.09 (0.57–2.07)
Scholarity
1st grade incomplete21/48 (44)27/48 (56)11
1st grade to 2nd complete60/116 (52)56/116 (48)0.76 (0.40–1.42)0.85 (0.61–1.92)
Superior complete6/12 (50)6/12 (50)0.97 (0.30–3.15)1.09 (0.71–1.71)
OR crude: univariate analysis; OR-adjusted: logistic regression analysis adjusted by all variables in the table. * Statistically significant values (CI: 0.05%; p < 0.05).
Table 3. Association between number of eosinophils and antibodies responses for Toxocara spp.
Table 3. Association between number of eosinophils and antibodies responses for Toxocara spp.
Toxocara Infectionn/N =176 (%)OR adjustedn/N = 176 (%)OR adjustedn/N = 176 (%)OR adjusted
Eosinophils
≤ 100 mm3		 Eosinophils
> 100 < 450 mm3		 Eosinophils
≥ 450 mm3
No35/87 (40)114/87 (16)138/87 (43)1
Yes23/89 (26)0.51 (0.27–0.98) *12/89 (13)0.81 (0.35–1.87)54/89 (60)1.98 (1.09–3.62) *
OR adjusted: logistic regression analysis adjusted by age, gender, atopy, outcomes and countryside living. * Statistically significant values (CI: 0.05%; p < 0.05).
Table 4. Proportion of reacting sera for IgG to Toxocara spp. and clinical indicators of asthma severity and allergy in patients with non-eosinophilia and under eosinophilia.
Table 4. Proportion of reacting sera for IgG to Toxocara spp. and clinical indicators of asthma severity and allergy in patients with non-eosinophilia and under eosinophilia.
VariablesEosinophilia Negative.Eosinophilia Positive.
Toxocara spp. Infections (n)Toxocara spp. Infections (n)
N n/N (%)χ2 (p-Value) n/N (%)χ2 (p-Value)
Skin Prick TestNo24/49 (49)0.020 (0.88)No19/54 (35)4.749 (0.03) *
Yes25/49 (51)Yes35/54 (65)
sIgE ≥ 0.70 KU/L to D. farinaeNo21/38 (55)0.421 (0.51)No15/46 (33)5.565 (0.01) *
Yes17/38 (45)Yes31/46 (67)
sIgE ≥ 0.70 KU/L to D. pteronyssinusNo20/37 (54)0.243 (0.62)No14/43 (33)5.233 (0.02) *
Yes17/37 (46)Yes29/43 (67)
sIgE ≥ 0.70 KU/L to B. tropicalisNo23/42 (55)0.381 (0.53)No17/48 (35)4.083 (0.04) *
Yes19/42 (45)Yes31/48 (65)
IgE ≥ 160 UI/dlNo23/43 (53)0.381 (0.53)No26/78 (33)4.083 (0.04) *
Yes20/43 (46)0.209 (0.64)Yes52/78 (67)8.667 (0.003) *
Uncontrolled asthma No20/40 (50)0.00 (1.00)No19/52 (36)3.769 (0.05) *
Yes20/40 (50)Yes33/52 (64)
Frequency rates (%) for categorical variables are shown. χ2 = chi-square value. * Statistically significant values (CI: 0.05%; p < 0.05).
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Silva, R.C.; da Silva, M.B.; Galvão, A.A.; Fernandes, J.S.; Pinheiro, G.P.; Cruz, Á.A.; Pinheiro, C.d.S.; Alcântara-Neves, N.M. Toxocara spp. Infection Influences on Eosinophil Levels: An Immunological Indicator of Severe Asthma and Allergy. Allergies 2025, 5, 24. https://doi.org/10.3390/allergies5030024

AMA Style

Silva RC, da Silva MB, Galvão AA, Fernandes JS, Pinheiro GP, Cruz ÁA, Pinheiro CdS, Alcântara-Neves NM. Toxocara spp. Infection Influences on Eosinophil Levels: An Immunological Indicator of Severe Asthma and Allergy. Allergies. 2025; 5(3):24. https://doi.org/10.3390/allergies5030024

Chicago/Turabian Style

Silva, Raphael Chagas, Márcia Barbosa da Silva, Alana Alcantara Galvão, Jamile Souza Fernandes, Gabriela Pimentel Pinheiro, Álvaro A. Cruz, Carina da Silva Pinheiro, and Neuza Maria Alcântara-Neves. 2025. "Toxocara spp. Infection Influences on Eosinophil Levels: An Immunological Indicator of Severe Asthma and Allergy" Allergies 5, no. 3: 24. https://doi.org/10.3390/allergies5030024

APA Style

Silva, R. C., da Silva, M. B., Galvão, A. A., Fernandes, J. S., Pinheiro, G. P., Cruz, Á. A., Pinheiro, C. d. S., & Alcântara-Neves, N. M. (2025). Toxocara spp. Infection Influences on Eosinophil Levels: An Immunological Indicator of Severe Asthma and Allergy. Allergies, 5(3), 24. https://doi.org/10.3390/allergies5030024

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