Dietary habits and minerals intake in patients with grass pollen allergy

doi:10.21203/rs.3.rs-4958492/v1

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Dietary habits and minerals intake in patients with grass pollen allergy

https://doi.org/10.21203/rs.3.rs-4958492/v1

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Specific dietary components (e.g., fatty acids and micronutrients) are crucial in food allergy; however, their exact role in the diet in grass pollen allergy needs to be better established. Since specific macro- and microminerals (trace elements) can stimulate the immune system, this study aimed to estimate the dietary habits and mineral intake in patients with allergic diseases. Anthropometric, biochemical, serological, and nutritional habits analyses were done in patients with grass pollen allergy and compared to the healthy control group.

Daily food rations (DFR) were improperly balanced, and high intake of protein and fat and low carbohydrate were observed in both groups. Saturated fatty acids (SFA), phosphorus, and copper were supplied in high amounts, while mono- and polyunsaturated fatty acids, magnesium, and zinc were within the reference range and comparable in both analyzed groups. Insufficient calcium intake resulted in a low Ca:P ratio. A similar analysis showed higher macronutrients, SFA, sodium, magnesium, and copper intake and lower calcium and phosphorus consumption in allergic patients than in the control group. Total IgE positively correlated with platelet level and negatively with zinc intake. The diet of patients with grass pollen allergy needs to be better balanced regarding macronutrients and selected elements. Correcting and controlling the number of nutrients that increase the risk of immune system dysregulation in such patients (particularly reducing excessive SFA intake and increasing insufficient calcium intake) is advisable.

grass pollen allergy

dietary habits

minerals

trace elements

immunoglobulin E

After childhood, a constant increase in allergic responses worldwide is observed in the adult population. One of the examples is allergic rhinitis, which appears to decrease with age (1), while non-allergic rhinitis increases and has the highest prevalence in older people (2). Rhinitis, independently of etiology, is often stimulated by grass pollen allergens. Grasses are distributed worldwide and are one of the main sources of crucial allergens (3) (4). Moreover, grass pollen allergy affects almost 50% of patients with IgE-associated allergies, such as allergic rhinoconjunctivitis (i.e., hay fever) or asthma. The relation between multimorbid asthma and rhinitis shows IgE polysensitization results from several allergen sources, including grass pollen (5).

Over the last decade, research has emphasized food's role in regulating the immune response. The immune system activity can be controlled by the intake of specific nutritional components, such as zinc, iron, and copper, which play a synergistic or antagonistic influence on immune response (6) (7) (8). Moreover, the intake of various fatty acids modulates the allergic response. However, many inconsistencies exist regarding consuming fat and fatty acids in allergic patients. An example is the positive impact of PUFA (especially EPA and DHA) on the health of the fetus and children (9) (10), while in the case of adults, the data are ambiguous (9) (10). Dietary minerals and trace elements, particularly such as calcium, magnesium, zinc, and copper, play an important airborne allergy development (11) (12) (13)(14) (15) (16) (17) (18).

Allergic rhinitis (AR) caused by grass pollen affects daily life and work performance. Many attempts have been made to reduce the symptoms by specific treatment, including diet modifications. Even though the analysis of food components in dietary allergy is described well in the literature, including the cross-reactions between nutrients and aeroallergens, there needs to be more information about the impact of nutrients on immune pathways in grass pollen allergy. Since specific macro- and micronutrients can stimulate the immune system, we decided to estimate the dietary habits (with special consideration of macro- and microelements) in grass pollen allergy patients and compare them to healthy volunteers. Knowing that IgE plays a vital role in allergic diseases, we also planned the evaluation between IgE and nutritional components.

Characteristics of the group

A total of 63 adult patients aged 18–65 years old were selected from the Allergology Outpatient Clinic (Alergo-Med). All participants lived in Poznań and the vicinity of Greater Poland. Both groups (study and control) underwent anthropometrical, biochemical, and serological measurements. All participants enrolled in this study provided their written informed consent. The local Bioethics Committee approved this study of Poznan University of Medical Sciences (no. 07/12/2017), which was performed according to the Helsinki Declaration.

Anthropometric measurements

The measurements were performed after an overnight fast in underwear and without shoes. The anthropometric assessments included measurement of height and body mass, which were determined using the OMRON BF511 scale (Fig. 1). Body mass was measured to the nearest 0.1 kg, and height was estimated using a vertical ruler to the nearest 1 mm. Body mass index (BMI) was calculated as weight (kg) divided by squared height (m²) (19). The study staff measured all anthropometric components twice using a standardized protocol, averaging the values.

Figure 1. The methodology and methods of the study – please insert here

CBC - complete blood count; erythrocyte sedimentation rate; CRP - C-reactive protein; BMI – body mass index

Protocol of the study

Skin prick tests confirmed allergy to grass pollen a minimum of two years before the study. These tests were performed using the standard method consisting of applying the Allergopharma grass mix to the skin in the volume of one drop (about 0.05 ml) and puncturing the epidermis to a depth of about 0.4 mm with a special metal lancet with a blade of 1 mm. Patients with essential diseases that could affect inflammatory markers, such as acute infections, hematological disorders, and systemic connective tissue diseases, were excluded from this analysis. Moreover, patients with Cushing's disease or syndrome, acute liver and renal disorders, neoplasm history in the past five years, nontreated thyroidal diseases, and smoking did also not participate in this study. Considering the inclusion criteria, thirty patients suffering from grass pollen allergy and 30 healthy volunteers were selected from this group.

The pollen season period (from May to the end of September) was determined based on the region's pollen calendar based on data from the Environmental Allergen Research Centre. All the patients were referred for biochemical and serological blood from January till March - two months before the pollen season. During pollen season, allergic symptoms (e.g., nose blockage and tiredness) may influence traditional dietary behavior.

Biochemical analysis

Blood samples were collected between 7:00 am and 8:00 am following an overnight fast. Venous blood samples were collected in EDTA or heparin-containing tubes and immediately centrifuged. Complete blood count (CBC) with a blood smear was assessed using the Sysmex XN of Siemens company. Enzymatic colorimetric assays were used to determine erythrocyte sedimentation rate (ESR) and C-reactive protein (CRP). CRP was evaluated by Architect C16000 apparatus of Abbot company ESR was measured by Halifax Test 1 apparatus of Biomedica company.

Serological evaluation

Total IgE was determined by ELISA. This was used in the test kit for the quantitative in vitro determination of human IgE antibodies in serum. The kit contained a microplate with microtube strips - each with 8 separately breakable reaction wells coated with anti-human IgE polyclonal antibodies. In the first step, diluted patient samples were incubated in the reaction wells. When IgE class antibodies were present in the sample, they were bound to the antibodies present on the surface of the well. Bound IgE antibodies were detected during a second incubation step with an enzyme-labeled anti-human IgE antibody (enzyme conjugate), which catalyzed the color reaction. IgE concentration was read from a standard curve made with calibrated sera.

Nutritional analysis

The food intake was assessed by the method of 24-hour recall of 7 days, and 420 nutritional interviews were collected (20). To determine the dietary habits accurately, each study participant was individually trained in the principles of the dietary interview for 24 hours, considering the weight of nutritional products. The data collected from the interview was analyzed by the Kcalmar program, which enables the calculation of energy and dietary components intake and evaluating compliance with nutritional recommendations. The daily food rations (DFR) assessment was carried out per the Warsaw Institute of Nutrition and Food guidelines (21).

Statistical analysis

Statistical analysis was performed using the Statistica program v.13-Dell Inc. (2016). The mean values, standard deviations, median, and quartile deviation were calculated. The differences between analyzed nutritional composition in DFRs in the study and control group were tested by the Student's t-test (normal distribution) or Wilcoxon or U Manna-Whitney's test (not normal distribution) at the significance level of α = 0.05. The Spearman correlation (data without normal distribution) or the Pearson correlation (data with normal distribution) were used to determine the relationship between the selected anthropometric biochemical, and nutritional parameters.

The biochemical analysis

The analyzed parameters of CBC were within the recommended values, and no statistically significant differences were observed between both analyzed groups, except for a higher level of neutrophils and lymphocytes in allergic patients (Table 1). An increased number of neutrophils usually is present in symptomatic individuals with allergic diseases(22) (23). A higher level of lymphocytes is related to increased activation of Th2 lymphocytes, which exacerbates the secretion of cytokines responsible for IgE production - mainly IL-4, IL-5, and IL-13. In turn, increased IgE synthesis is a reason for inflammation in allergy and asthma (24). In this study, patients with grass pollen allergy have higher IgE levels than healthy volunteers; however, in both groups, the IgE concentration was within the recommended level. It corresponds with the clinical practice, which shows that in the diagnosis of grass pollen allergy, the determination of total IgE is only one of the tests that are performed together with other clinical tests (e.g., skin prick tests, bronchial, intranasal, conjunctival provocation tests) (25).

Table 1. Anthropometric and biochemical characteristics in the study and control group

Table 1. Anthropometric and biochemical characteristics in the study and control group

The analysis of total IgE with CBC parameters showed a positive correlation with platelet levels (Table 2). Platelets play a potential role in immune-mediated responses to allergy because they release mediators (e.g., platelet-activating factor – PAF) that can be recognized by other cell types, such as endothelial cells, macrophages, T lymphocytes, neutrophils, and mast cells (26). PAF is a mediator that acts as a potent activator of human eosinophils (21) and can mimic the allergic induction of leukocyte-dependent histamine release from platelets (27) (28). Therefore, the positive correlation between IgE and PLT levels reflects the relation between both parameters, primarily since PLT can interact with immune cells and increase immune mediators (29). Platelets are a rich source of spasmogens and mediators, stimulating leucocyte activation and recruitment in allergy and asthma. PLT isolated from allergic donors express both the high and the low-affinity IgE receptors on their surface, and after contact with antigens (allergens), stimulate the inflammatory various pro0inflammatory mediators. Simulation of the high-affinity IgE receptor can cause platelet chemotaxis characterized by mild hemostatic defect rather than an increased incidence of thrombosis (30).

Table 2

**The correlation between IgE and biochemical and nutritional parameters** – please insert here
Spearman correlation between the concentration of total IgE and biochemical or nutritional parameters
Spearman correlation	Coefficient R_S	P velue
total IgE and WBC	-0,1212	0,5234
total IgE and lymphocytes	0,0274	0,8855
total IgE and eosinophils	0,1245	0,5120
total IgE and PLT	-0,4902	0,0060
total IgE and CRP	0,0550	0,7728
total IgE and ESR	0,0970	0,6102
total IgE and PUFA intake	0,1752	0,3545
total IgE and omega-3	0,0698	0,7138
total IgE and zinc intake	-0,4720	0,0084
IgE – immunoglobulin E; WBC – white blood cells, PLT – platelets; CRP – C-reactive protein; ESR – erythrocyte sedimentation rate; PUFA – polyunsaturated fatty acids

Table 2. The correlation between IgE and biochemical and nutritional parameters – please insert here

Dietary analysis

Recent data highlight the role of nutrients, such as dietary minerals (including macro- and micro-/trace elements), in the immune response (6) (7) (8). Therefore, we decided to analyze the diet by assessing the level of macronutrients and minerals consumption in the group of patients with grass pollen allergy and healthy volunteers, considering the current nutritional standards for the Polish population and WHO recommendations (21).

The analysis of daily food rations showed that the energy value of the diet in patients with grass pollen allergy and the control group was comparable. Unfortunately, the food rations were poorly balanced (Table 3). According to the dietary recommendations, the amount of energy derived from protein should not exceed 10–15% of energy intake; however, in this study, the protein intake was higher in allergic patients (WHO recommendation) (21). The Institute of Medicine, in turn, suggests that a high-protein diet is characterized by an intake of more than 35% of energy from protein. Such protein amount is based on the acceptable macronutrient distribution range (AMDR), set at 10–35% of total energy intake (31). The percentage of carbohydrate intake in allergic patients and the control group did not achieve the recommended minimum of 400 grams/day (55–75% of the total energy) and was associated with a high fat intake, which exceeded the recommended 15–30% of the daily energy supply in the analyzed diets (21) (32) (33).

Table 3. Nutritional analysis of daily food rations in grass pollen allergy patients and control group

* non-parametric Wilcoxon test; SD –standard deviation, Me – median, – QD – quartile deviation, SFA –Saturated Fatty Acids, MUFA – Monounsaturated Fatty Acids, PUFA –Polyunsaturated Fatty Acids), n-3 PUFA – polyunsaturated fatty acids, n-6 PUFA – n-6 polyunsaturated fatty acids; Ca – calcium; P – phosphorus;

Table 3. Nutritional analysis of daily food rations in grass pollen allergy patients and control group – please insert here

Despite many unsolved problems and clinical questions, it is increasingly apparent that dietary intake of fatty acids may influence the development of inflammatory and tolerogenic immune responses (34). One is saturated fatty acids (SFA), which were supplied in high amounts and exceeded the recommended 10% of total energy intake in the allergic group(35) (36). Unfortunately, the SFA consumption was higher in allergic patients. Excessive SFA increases the risk of improper immune system activation in the respiratory tract. The immune stimulation is initiated by adipose tissue macrophages, which release pro-inflammatory mediators (such as TNFα and IL-6). Moreover, SFA activates the domain-like protein receptor 3, which affects the release of IL-1β (a marker of inflammation) and increases granulocytosis in the respiratory tract (37).

Other fatty acids that have a crucial influence on the immune system are mono- and polyunsaturated fatty acids (MUFA and PUFA), which were within the reference range and comparable in both the allergic group and healthy control (reference range 10–14% and 6–10% of total energy intake, respectively) (21). It is beneficial, particularly that the low levels of long-chain PUFA (LC-PUFA) influence the development of allergic processes (e.g., asthma, allergic rhinitis, and atopic inflammation) in infants and young children (38). Moreover, n-3 and n-6 fatty acids belong to PUFA and are critical in allergic mechanisms.

The consumption of n-3 fatty acids was within the reference norms (1–2% of total energy). However, available data on the amount of PUFA in the diet are still being established, as most data available relate to their intake and effects in infants and children. Studies in adults showed that three weeks of dietary omega-3 supplementation does not provide the available beneficial impact in the short-term treatment of asthma and does not improve a test for bronchial hyperresponsiveness to mannitol or decrease sputum eosinophil counts (9). However, such short supplementation might not be sufficient to reduce the inflammatory state of chronic disease. Nevertheless, n-3 LCPUFA (mainly eicosapentaenoic acid - EPA and docosahexaenoic acid - DHA) reduces the production of pro-inflammatory cytokines such as IL-4 and IL-13 by decreasing reactive oxygen species levels (39). EPA and DHA target specific receptors or signaling cascades, act as eicosanoid precursors, and exhibit anti-inflammatory properties (40). Thus, since n-3 PUFAs regulate the immune system, their proper participation in the analyzed diets can be considered beneficial.

Fish and fish oils are sources of long-chain n-3 PUFA, and these fatty acids oppose the unbeneficial effect of high consumption of n-6 PUFA (41). In this study, n-6 acids were supplied in 4.35% of the energy intake in allergic patients and 4,07% in the control group. Nevertheless, their amount was lower than the recommended 5–8% of the total energy supply. Recent epidemiological and cross-sectional evidence suggests that an unbalanced high intake of n-6 PUFA (e.g., linoleic acid – LA) may contribute to the incidence of allergic sensitization and asthma (reviewed in (41) (42). Fortunately, the omega-6 to omega-3 ratio in our study was about 3/1. Compared to a Western diet, this ratio varies from 15/1 to 16/1. Thus, the analyzed ratio in allergic patients is advantageous, considering the role of these fatty acids in the autoimmune processes. It was proved that a ratio of 5/1 and lower positively affects patients with asthma, while a ratio of 10/1 causes adverse consequences (exacerbates inflammatory state) (43).

In allergic and atopic processes, dietary minerals (e.g., calcium, zinc, selenium) play an important role in their development. The analysis of dietary intake of macro and microelements showed statistically significant differences between the analyzed grass pollen allergy patients and the control group. Higher sodium, phosphorus, and copper and a lower calcium and magnesium intake were observed in allergic patients compared to the control group.

The detailed analysis has shown that the dietary sodium exceeded the adequate intake of 1500 mg/day and was higher in allergic patients. Potassium intake was lower than recommended AI = 4700 mg/day. Low potassium and high sodium increase the risk of hypertension development (44). Moreover, insufficient calcium intake (which was lower than AI = 1000 mg/day) and high phosphorus amount (exceeding the recommended 700 mg/day) were observed in both analyzed groups. In most Western diets, dietary phosphorus overload is due to the high amount of processed food intake, which is rich in phosphate additives(45) (46). Phosphorus overconsumption can result in increased parathyroid hormone (PTH) secretion, which leads to bone loss/resorption, and these adverse effects increase when dietary calcium intake is low (47). Moreover, some allergic conditions, such as childhood eczema and milk allergy, are associated with significantly lower calcium intake(11) (48). Animal studies proved that proper calcium consumption reduces reactive oxygen species (ROS) and pro-inflammatory cytokines (tumor necrosis factor-α - TNF-α, and IL-6 in obese mice (49). Additionally, casein and whey protein in milk products reveal anti-inflammatory effects and beneficially modulate immune response (12). Thus, low calcium intake in allergic patients could cause worsening of allergic symptoms, particularly during the allergic season.

Magnesium is another macro-mineral important in the immune function, which regulates leukocyte activation and modulates the stimulation of peripheral blood neutrophils and eosinophils in patients with eosinophilia (16) (17). Thus, proper magnesium intake in both analyzed groups can be an important component that might prevent stimulation or exacerbation of clinical symptoms in allergic patients.

For proper immune function, it is necessary to have adequate micronutrient intake. One of them is zinc. The low concentration of this microelement in the serum in asthma patients correlates with the disease's severity (13). Adequate zinc level regulates hyperresponsive immune reactions by diminishing the synthesis of pro-inflammatory Th17 and Th9 cells and reveals antioxidant properties (8) (14) (15). Fortunately, in this study, the average zinc consumption slightly exceeded the recommended values of RDA in allergic patients and the control group. Moreover, a negative correlation between total IgE level and zinc intake was observed (Table 2), which confirms that this microelement should be considered in nutritional recommendations for grass pollen allergies.

Another microelement is copper, whose intake was higher than RDA (0.9 mg/day), particularly in the group with a grass allergy. Copper plays a crucial role in inflammatory response as a free-radical scavenger (8), and maintains intracellular antioxidant balance (43); however, taken in excess reveals cellular toxicity due to its redox properties and ability to disrupt active sites of metalloproteins (18). Thus, copper excess may exacerbate allergic response, and its consumption should be reduced in patients with grass pollen allergy.

In summary, this research shows that nutritional factors can potentially be associated with developing allergic processes. A similar conclusion is in line with research by Han et al., who determined that none of the analyzed macronutrients of the diet, fatty acids or minerals, is exclusively associated with asthma or allergies, but a well-balanced diet is more crucial in diminishing allergic symptoms (50). Thus, dietary interventions based on detailed analysis of the whole diet, including basic nutrients and essential components as well as macro- and micronutrient intakes, are advisable to prevent allergic processes. The analyzed data in this study indicates the need to modify and maintain a properly balanced diet, particularly in allergic patients. Despite small groups in numbers, the presented data allow us to show the dietary insufficiencies and excess of specific components and show in which direction nutritional modifications should be made. Nevertheless, large groups are needed to confirm the revealed tendencies and to create nutritional recommendations for allergic patients in the Polish population.

The dietary intake of analyzed patients requires nutritional modification, including proper macro-nutrient intake (decreeing the energy from protein and fat and increasing the energy from complex carbohydrates). The nutritional modification should be based mainly on a properly balanced diet, which is much more critical than specific modifications to individual dietary components. Nevertheless, the reduced SFA, sodium, and phosphorus supply and increased calcium intake can improve the immune system's function. Ensuring adequate intake of zinc, omega-3, and omega-6 PUFA acids is crucial to minimize the risk of grass allergies.

Well-balanced diet modification is much more advisable based on existing evidence to prevent allergic processes and good health, much more than specific component modification. Thus, DFR should be adequately balanced. Nevertheless, the amount of nutrients that increase the risk of improper immune system activation in grass pollen allergy (e.g., excessive SFA and insufficient calcium intake) should be corrected and controlled in the diet of the analyzed allergic group.

The study was conducted in a small group. Still, small-group studies are crucial to explore avenues in a relatively new field of research as they hold promise for the value of nutritional assessment of allergic patients. More extensive studies are needed to cover larger groups of patients, which can precisely determine the relationship between biochemical, serological, and nutritional factors. The comparison of dietary intake in groups of patients with other allergic diseases can also be interesting, as it could allow for a more precise formulation of nutritional guidelines for specific allergy types. It is worth noting that a properly balanced diet affects the activity of the immune system, and accurate determination of dietary patterns, which influence inflammatory response, still arouses the curiosity of scientists.

Acknowledgment

We thank Professor Mariusz Puszczewicz for enabling us to conduct the study and for his advisory help.

Author’s contribution: All authors contributed to the final version of the manuscript. The patient samples and data collection, analysis of the data, and formed part of the conclusion were performed by Natalia Rogacka. Critical comments on the interpretation of the data, partial statistical analysis, and preparation of the whole draft of the manuscript were performed by Bogna Grygiel-Górniak. All authors commented on previous versions of the manuscript. Joanna Jagielska conducted a critical statistical analysis of all data. All authors read and approved the final manuscript for submission.

Ethics approval

This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the local Bioethics Committee of Poznan University of Medical Sciences (no. 07/12/2017). Informed consent was obtained from all individual participants included in the study.

Funding

The study was not founded.

Competing Interests The authors have no relevant financial or non-financial interests to disclose.

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No competing interests reported.

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Dietary habits and minerals intake in patients with grass pollen allergy

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Abstract

Figures

Introduction

Material and methods

Characteristics of the group

Anthropometric measurements

Protocol of the study

Biochemical analysis

Serological evaluation

Nutritional analysis

Statistical analysis

Results and discussion

The biochemical analysis

Dietary analysis

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1