WORMWOOD: SPECIES DIVERSITY, REGIONAL FEATURES OF SENSITIZATION IN MONGOLIA. NEW POSSIBILITIES OF SPECIFIC TREATMENT.


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Abstract

This article discusses different species of Artemisia and their importance in seasonal allergic diseases, especially pollinosis. Artemisia pollen allergens are a major cause of sensitisation in late summer and autumn worldwide, including Europe, the Asian-European Silk Road and the northwestern USA. About 10-14% of allergic individuals worldwide react to wormwood pollen allergen, and about 25% of these patients develop hypersensitivity to certain foods such as celery, honey, sunflower seeds, chamomile and pistachios.

Mugwort pollen allergens range from 350 to 500 species worldwide, with 187 species found in China alone. Some of these species, such as Artemisia annua, are invasive species in Europe and the Americas and are potentially serious sources of allergies. The major allergens of Artemisia pollen are species v 1 and v 3, which are found worldwide.

In Mongolia, the pollen load of wormwood pollen allergens was analysed from 1980 to 2000. Artemisia pollen allergens is an important allergen in Mongolia, especially Artemisia siversiana and Artemisia macrocephala species. The wormwood pollen season in Mongolia lasts from mid-July to mid-August.

Allergen-specific immunotherapy (ASIT) is a key component of the treatment of wormwood pollen allergy. It effectively relieves symptoms and reduces the risk of asthma and sensitisation to new allergens. ASIT can achieve prolonged remission and reduce the need for baseline and symptomatic therapy. Currently, sublingual immunotherapy (SLIT) is preferred over subcutaneous immunotherapy (SCIT) due to its better safety profile and higher compliance.

In summary, the article shows the importance of wormwood pollen allergen as a major allergen and progress in specific immunotherapy for the treatment of wormwood sensitisation.

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Wormwood pollen is one of the main causes of seasonal allergic diseases in late summer and autumn worldwide, covering areas from Eastern Europe to the Northwestern United States [22, 26, 31, 34]. The high clinical significance of wormwood pollen in the formation of specific sensitivity is confirmed by statistical data: approximately 10-14% of patients suffering from pollinosis worldwide are sensitized to this allergen [38]. About 25% of patients with wormwood pollen allergy subsequently develop cross-reactive hypersensitivity to various food products, such as celery (the so-called "Celery-Mugwort-Spice" syndrome), honey, sunflower seeds, chamomile, and pistachios [23, 31].

There are between 350 and 500 species of wormwood registered in the plant kingdom [30] worldwide, with 187 species in China [24]. The botanical relationship and cross-reactivity of ragweed pollen with wormwood pollen are the cause of clinically significant reactions in other geographical regions. However, the absence of high cross-reactivity excludes the possibility of parallel therapy for mixed (wormwood + ragweed) pollinosis, as is possible with flowering (woody) or grassland hay fever.

The phylogeny of the genus Artemisia, updated through molecular marker analysis [30, 37], includes six sections: Artemisia, Abrotanum, Dracunculus, Absinthium, Seriphidium, and Tridentata. Most wormwood species belong to the first four sections and are distributed in temperate climate regions, where most patients with wormwood pollen allergy reside. Several species belonging to Seriphidium and Tridentata are found in semi-desert and steppe environments [36]. Common wormwood is the most studied species, primarily distributed in Northwestern and Central Europe. Five main species have been identified in China (A. annua, argyi, sieversiana, capillaris, lavandulifolia) as part of a national research program on pollen monitoring in the region [29]. Several species, such as A. annua, have invaded Europe and America, becoming potentially serious sources of allergy [16]. Overall, allergy to wormwood pollen is directly related to the distribution of the Artemisia species, whose pollen is a causative factor in the formation of specific sensitivity in the overwhelming majority of patients worldwide.

Molecular Characterization of Wormwood Pollen.

To date, it has been shown that Art v1 and Art v3 are the main allergenic molecules worldwide; however, a recently identified group, Art an 7, also appears to be important, although IgE levels in this group are generally much lower [19, 26]. Through sequential cloning of pollen from one species, Artemisia vulgaris, seven isoforms of Art v1 with minor changes at the C-terminus and very similar IgE reactivity have been identified [13]. Five isoforms of Art v3 have also been identified, one partial sequence through N-terminal sequencing [15], and the remaining four through gene cloning [18].

However, Art v1 of wormwood represents a specific marker of true allergy, suitable for distinguishing true sensitization to wormwood from cross-reactivity. Approximately 79-95% of patients with wormwood allergy are sensitized to Art v1, the major allergen of wormwood. Art v1 is a modular glycoprotein weighing 28 kDa, which can induce a strong T-cell response [30]. Unlike other common pollen allergens with multiple T-cell epitopes, Art v1 contains only one immunodominant T-cell epitope [20].

Wormwood is characterized by broad cross-reactivity among different species of the genus Artemisia, as well as, to a significant extent, with members of the Asteraceae (Compositae) family [17]. Cross-reactivity between wormwood and ragweed pollen has also been demonstrated [28]. However, the degree of homology and cross-reactivity in terms of IgE and induced IgG4 between Amb a 1 and Art v 1 is low, which does not allow for comprehensive allergen-specific immunotherapy (ASIT) [12].

Regional Features in Mongolia.

In Mongolia, detailed studies of pollen monitoring were conducted from 1980 to 2000 as part of joint Russian-Mongolian comprehensive biological expeditions organized by the Russian Academy of Sciences and the Academy of Sciences of Mongolia, as well as scientific research in Mongolia, Russia, and Kazakhstan. The research established that the flora of Mongolia is quite diverse and heterogeneous, which is attributed to the country's geographical position at the intersection of major floristic regions of the globe: the Siberian taiga region, which encompasses the northern taiga and mountain-steppe zones, and the Central Asian desert region, which includes steppe and desert-steppe zones.

One of the most significant genera in the etiology of specific sensitization in Mongolia is the genus Wormwood, Artemisia, from the Asteraceae family [14]. This genus is represented by 105 species [7], of which 10 species have been studied in detail and are widely distributed in populated areas and other anthropogenic landscapes. The genus Artemisia (Sivers' wormwood - Artemisia siversiana and large-headed wormwood - A. macrocephala) plays a leading role as a source of causative pollen allergens in the development of pollinosis in Mongolia. The concentration of wormwood pollen in soil samples varies significantly across different botanical-geographical regions of Mongolia. The highest concentration of wormwood pollen was found in samples from the Central Khalkha steppe region (31.8%), followed by the Eastern Gobi desert-steppe region (20.8%), and the desert-steppe region of the Great Lakes Basin (21.6%), the Eastern Mongolian steppe (20.8%), the Khingan mountain-steppe region (20%), and the Khangai mountain-forest-steppe region (20%). The Mongolian-Daurian mountain-forest-steppe region had a concentration of 15%, while the lowest concentration of wormwood pollen was noted in soil samples taken from the Prikhubsugul mountain-taiga region (4%) [6].

The pollen season for wormwood in Mongolia is quite prolonged, lasting from mid-July to mid-August. Wormwood begins to bloom in the first decade of July, replacing Artemisia commutate Bess., plume wormwood Artemisia scoparia Waldst et Kit., and tarragon Artemisia dracunculus L. In the second decade, Sivers' wormwood Artemisia sieversiana Willd. and large-headed wormwood bloom, followed by Mongolian wormwood, and in the third decade, cold wormwood Artemisia frigid Willd. continues to bloom. Most species of wormwood continue to bloom until the end of summer, with the blooming period ending by late August. However, cold wormwood Artemisia Willd., Siberian orache Atriplex sibirica L., and prostrate kochia Kochia prostrata (L.) Schrad. continue to bloom until early September [6].

Thus, the species diversity within the wormwood family represented in Mongolia is characterized by a wide degree of variety, which, in turn, determines a high prevalence of specific sensitization to this allergen.

Allergen-Specific Immunotherapy – The Foundation of Treatment for Sensitization to Wormwood Pollen.

In international consensus documents from the WHO (WHO Position Paper on Allergen Immunotherapy: Therapeutic Vaccines for Allergic Diseases, 1997), it is stated that allergen-specific immunotherapy (ASIT) is one of the main methods for treating IgE-mediated allergic diseases [11, 25].

ASIT not only effectively alleviates allergy symptoms but also has what is known as a "disease-modifying effect," which prevents the transformation of allergic rhinitis (AR) into bronchial asthma (BA), halting the progression of the "atopic march" and preventing the formation of sensitization to new allergens and the development of polyvalent allergies [21]. ASIT can achieve long-term remission of allergic diseases, reduce the need for basic and symptomatic medications, lessen the severity of the disease, and significantly decrease the number of exacerbations. Long-term control of disease symptoms is achieved through prolonged ASIT (from 3 to 5 years), but effects may be observed after just one course [27].

Currently, sublingual allergen-specific immunotherapy (SLIT) is widely used for treating respiratory allergies. This method of treatment has a higher safety profile compared to subcutaneous allergen-specific immunotherapy (SCIT) and does not require frequent visits to a physician, thereby improving compliance between the doctor and the patient [32].

For SLIT in cases of sensitization to wormwood pollen, standardized allergens are currently absent in the pharmaceutical market of Russia. One of the most promising preparations for SLIT aimed at developing tolerance to wormwood pollen allergens in sensitive patients is the product Antipollin, produced by Burly (Kazakhstan), registered as a dietary supplement and containing in one tablet an extract of native allergen ranging from 0.0001 to 1000 PNU (PNU, protein nitrogen unit — an international unit used to express the concentration of protein nitrogen in allergens, equal to the content of 1×10^-5 mg of protein nitrogen).

The manufacturer offers a wide range of therapeutic allergens, including a mixed allergen of wormwood, which consists of allergenic molecules from bitter wormwood, annual wormwood, tarragon, and common wormwood, which is particularly relevant given the heterogeneous composition of the family and species diversity.

Currently, a significant amount of clinical data has been accumulated, demonstrating the high efficacy and safety profile of Antipollin for conducting SLIT [2].

In a study conducted by E.F. Glushkova and O.I. Sidorovich, 27 adults aged 20 to 53 with various forms of respiratory allergy participated, receiving ASIT with the Antipollin mixed wormwood preparation. The effectiveness of the therapy was assessed by the dynamics of allergic rhinoconjunctivitis (ARC) symptoms using a visual analog scale, RTSS, and the level of control over BA symptoms. The results of the study clearly demonstrated that conducting just one course of ASIT significantly reduced the severity of rhinorrhea and nasal congestion by 61.60%, eye itching by 71.43%, nasopharyngeal itching by 82.00%, and increased control over BA symptoms by 83.30% [1].

In another study involving 22 adult patients diagnosed with allergic rhinitis (AR), mild side reactions were observed at the beginning of treatment with the Antipollin "Mixed Mites" preparation. These reactions manifested as slight discomfort in the oral area, such as itching in the sublingual region and tingling of the tongue. However, these symptoms resolved spontaneously within a few minutes after allergen application and did not reappear after 3-5 days from the start of therapy. Importantly, no systemic reactions were detected. According to published results, 21 out of 22 patients (95.5%) experienced complete disappearance or significant reduction of AR symptoms, including nasal itching, rhinorrhea, and nasal congestion after the treatment course. It is also noteworthy that during SLIT, patients were able to significantly reduce their intake of previously used antihistamines and hormonal medications, even to the point of complete cessation [10].

In 2019, a clinical study was conducted at the Department of Clinical Immunology and Allergology of the Saratov State Medical University named after V.I. Razumovsky, Ministry of Health of Russia, to assess the efficacy of SLIT with the Antipollin "Mixed Wormwood" preparation in patients suffering from seasonal allergic rhinitis (SAR) and rhinoconjunctivitis. The study demonstrated the high efficacy of the Antipollin "Mixed Wormwood" preparation in inducing tolerance to the causative allergen, evidenced by a significant reduction in SAR and rhinoconjunctivitis symptoms, as well as a decrease in the volume of necessary pharmacological assistance [5].

In the study by N.S. Tataurshchikova and B. Sangidorzh, the efficacy of the combined use of SLIT with the Antipollin preparation and the immunostimulator Cycloferon was compared to monotherapy with SLIT (Antipollin) in immunocompromised patients suffering from AR. The results showed significant improvement in the condition of patients with virus-associated AR in both groups. However, in the group receiving combination therapy, there was a greater reduction in the consumption of anti-allergic medications, as well as a decrease in the frequency and severity of clinical manifestations of the disease [9]. A review publication from 2014 by the same authors provided additional data on the effectiveness of SLIT and the rationale for using Antipollin in terms of therapy rationality. Antipollin demonstrated advantages in standardization, price, and antigen dose gradient (from 0.0001 PNU at the beginning of treatment to 1000 PNU at the end) [8].

To evaluate the effectiveness of Antipollin in seasonal pollinosis, 50 patients were studied for immune status indicators (total IgE, IL-4, IL-5, sIgA1, and sIgA in oropharyngeal secretions), as well as the dynamics of clinical manifestations, since the suppression of IL-4, IL-5, and IL-13 by allergen-specific T-cells due to the induction of peripheral T-cell tolerance is one of the mechanisms of ASIT. The study achieved a good clinical effect during SLIT. In 81% of patients, a favorable influence on the course of SAR was noted, accompanied by an increase in secretory IgA levels by 10-16%, and a decrease in IL-4 levels by 5-7% and IL-5 by 7.5%. During the SLIT conducted as part of the study, no cases of systemic allergic reactions were recorded, which undoubtedly indicates the high safety profile of this preparation. Over six months of observation, total IgE levels decreased by 17.0-18.5% [4]. The conducted studies assessed not only the clinical picture of the studied diseases (AR, BA, atopic dermatitis, etc.) according to generally accepted scales and tests but also objective parameters such as IgE levels and IL in nasopharyngeal secretions, as well as the overall reduction in the frequency of anti-allergic medication use.

In 2023, a study was conducted to investigate the efficacy of SLIT in patients with SAR sensitized to weed pollen. Patients underwent a pre-seasonal course with the Antipollin "Mixed Weeds - 2" preparation (sublingual tablets containing allergens from ragweed, common wormwood, bitter wormwood, and cyclahene, with active substance concentrations ranging from 0.0001 to 1000 protein nitrogen units (PNU)). The effectiveness of the therapy was monitored by analyzing the Total Nasal Symptom Score and the daily medication intake scale. The following conclusions were drawn from the study:

  1. SLIT with the Antipollin "Mixed Weeds - 2" preparation is an effective and safe method for treating SAR.
  2. The clinical efficacy of SLIT with the Antipollin "Mixed Weeds - 2" preparation was expressed in the reduction of the severity of SAR exacerbations and a decrease in the volume of symptomatic therapy during exacerbations [3].

Speaking about the prospects for the development of new vaccine preparations for treating pollinosis caused by sensitization to allergenic molecules from wormwood pollen, a recently conducted study in Kazakhstan draws attention. The authors concluded that a significant drawback of current ASIT methods is the long duration of therapy and the multiple administrations of allergen vaccines. The aim of this study was to conduct a pilot study in mice using a new immunotherapy scheme with an ultra-short vaccine that includes various adjuvants to assess its effectiveness in inducing tolerance in the treatment of allergic BA, where the causative allergen is wormwood pollen. In the study, various adjuvant vaccine options containing the recombinant protein from wormwood pollen Art v 1 were evaluated, using either newer (Advax, Advax-CpG, ISA-51) or more traditional adjuvants (aluminum hydroxide, squalene water emulsion (SWE)), administered intramuscularly or subcutaneously. Vaccine forms were administered to mice previously sensitized to wormwood pollen four times at weekly intervals. Desensitization was determined by measuring the reduction of immunoglobulin E (IgE), cellular immunity, ear swelling tests, and pathological changes in the lungs of the animals after exposure to aeroallergens.

The study demonstrated that the protein composition Art v 1 with adjuvants Advax, Advax-CpG, SWE, or ISA-51 induced a significant decrease in both total and Art v 1-specific IgE, along with an increase in Art v 1-specific IgG compared to the positive control group. A shift in T-cell cytokine secretion towards Th1 (Advax-CpG, ISA-51, and Advax) or a balanced Th1/Th2 response (SWE) was observed. Protection against lung inflammatory reactions after provocation was noted with the use of ISA-51, Advax, and SWE Art v 1. Overall, the group of vaccines with the ISA-51 adjuvant induced the greatest reduction in allergic ear swelling and protection against type 2 lung inflammation and other types in treated animals. This pilot study shows promising prospects for the development of new vaccine preparations for SLIT [35].

Thus, considering the lack of alternatives for SLIT preparations for patients sensitized to wormwood pollen allergens, as well as the high safety profile of the Antipollin preparation, which is supported by the results of numerous clinical studies, the Antipollin "Mixed Wormwood" preparation can be regarded as a promising therapeutic tool for inducing tolerance in sensitive patients.

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About the authors

Bayarmаa Tuvshinbayar

Federal State Autonomous Educational Institution of Higher Education "Russian Peoples' Friendship University named after Patrice Lumumba", Moscow, Russian Federation.

Email: pugoeva.khadi@mail.ru

postgraduate student of the Department of Clinical Immunology, Allergology and Adaptology of the Federal Scientific and Medical Educational Institution of the Peoples’ Friendship University of Russia.

Anna Vladimirovna Maksimova

Federal State Autonomous Educational Institution of Higher Education "Russian Peoples' Friendship University named after Patrice Lumumba", Moscow, Russian Federation.

Email: pugoeva.khadi@mail.ru

Candidate of Medical Sciences, Associate Professor of the Department of Clinical Immunology, Allergology, Federal Medical Education and Science Institute, RUDN University

Natalia Stanislavovna Tataurschikova

Federal State Autonomous Educational Institution of Higher Education "Russian Peoples' Friendship University named after Patrice Lumumba", Moscow, Russian Federation.

Email: pugoeva.khadi@mail.ru

Doctor of Medical Sciences, Professor, Head of the Department of Clinical Immunology, Allergology and Adaptology of the Faculty of Medical Sciences and Medical Sciences of the Peoples' Friendship University of Russia.

Khyadi Pugoeva

People’s Friendship University of Russia named after Patrice Lumumba, Moscow, Russian Federation.

Author for correspondence.
Email: pugoeva.khadi@mail.ru
ORCID iD: 0009-0005-9311-6620

Attached person for the degree of Candidate of Medical Sciences at the
Department of Clinical Immunology, Allergology and Adaptology
Russian Federation

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