Type:
Whole Allergen
Whole Allergen
Whole Allergen
Rye grass
Inhalation
Poaceae (Gramineae)
L.perenne
Lolium perenne
Perennial Rye Grass, Perennial Rye-grass, Perennial Ryegrass, Ray-grass, Annual Ryegrass
Grass pollens are the principal causes of respiratory allergic disease globally. The IgE reactivity to these allergens is manifested by about 40% of allergic patients and 20% of the general population. Perennial ryegrass (Lolium perenne) is a well-known allergenic member of the temperate grasses belonging to the tribe Poeae of the subfamily Pooideae. It is a cool-season forage, hay, lawn, and erosion-control grass, native to Europe but has now spread extensively to the temperate regions of Asia and North Africa, Northern and Southern America, Australia, and New Zealand. It is a potent seasonal grass pollen allergen in temperate regions like Australia, especially in the early summers. Molecular and biochemical characterization of ryegrass has revealed the presence of several allergen components, among which, Lol p 1 and Lol p 5 are the most dominant allergens responsible for triggering specific IgE reactions in more than 90% of sensitized individuals. It can induce allergic reactions affecting the upper and lower respiratory system like allergic rhinitis and epidemic thunderstorm asthma in sensitized individuals through inhalation. The allergen molecules of rye grass show limited cross-reactivity with Bermuda grass, Bahia grass, Timothy grass, Canary grass, Velvet grass, Maize, and Orchard.
Ryegrass (Lolium perenne) is a perennial grass growing in bunches. But it can also conduct as annual, short-lived perennial or, perennial depending on environmental conditions. The inflorescence, spikelet, and seed (floral parts) or the roots, stem, and leaves (vegetative parts) help in its identification. The hollow flowering stem of the grass is 30-100 cm in height with nodes and internodes (leaf on every node) and a reddish stem base. Initially, leaves are folded in a bud. A mature leaf blade (bright green color) is 2 to 6 mm in width and 5 to 15 cm in length. They taper sharply to a point and present a prominent longitudinal ridge along the midrib (keeled) on the upper surface. The lower surface of the leaf is smooth, glossy, and hairless while the margins are somewhat rough when touched. This perennial grass has a spike inflorescence (5-30 cm long) with 5-40 spikelets (alternately arranged) on the central axis. Each spikelet bears 3-10 small flowers (florets) and possesses awnless lemmas (1).
L. perenne (perennial ryegrass) resembles the annual grass or Italian ryegrass (L. multiflorum L.). Both these species differ in their leaves. The leaves of perennial ryegrass are narrower and folded whereas the annual grass leaves are rolled. Also, the spikelets have awnless lemma in contrast to annual ryegrass (1, 2).
The flowering period of ryegrass in Australia extends from late spring to early summer (3) and usually pollinates through the wind (4, 5). However, the pollination season differs from one region to another. In south-eastern Australia, it is usually seen between late September to December end with peak observed from mid-October till early December (6).
Ryegrass grows fast and has high nutritive value and is mainly used for fodder and as a forage grass and pasture grass (2, 7). It is also used as a feed crop for wild animals. It offers high levels of protein, and minerals, good palatability as well as easily digestible energy. Perennial ryegrass is also one of the most adaptable turf grasses (1).
The perennial rye grass differs from cultivated rye (Secale cereale; g12); rye, the foodstuff (Secale cereale; f5), and the Wild Rye grass (Elymus tricoides; g70). Perennial ryegrass (Lolium perenne) is a well-known allergenic member of the temperate grass clade (BEP) and tribe Poeae of the subfamily Pooideae (8, 9). This subfamily consists of 5 tribes with over 2000 species. The ryegrasses, within the tribe Poeae also include Kentucky blue grass (Poa pratensis), Timothy grass (Phleum pratense), Orchard grass (Dactylis glomerata), and Sweet vernal grass (Anthoxanthum odoratum) (2, 8).
Taxonomic tree of Perennial Rye Grass (10) | |
---|---|
Domain | Eukaryota |
Kingdom | Plantae |
Phylum | Spermatophyta |
Subphylum | Spermatophytina |
Class | Magnoliopsida |
Order | Poales |
Family | Poaceae |
Genus | Lolium |
Species | Lolium perenne |
The perennial ryegrass pollen (RGP) grain is spheroidal in shape with a single pore (11). The diameter of the RGP varies between 25 and 30 µm. The surface of the pollen grain is sculptured and has papillae. Each papilla has numerous protuberances (12). The cell walls of pollen grain are uniformly thick (13). The external wall (exine) is multi-layered that extends to the inner wall (intine) through microchannels (12).
The two major allergenic molecules of ryegrass include Lol p 1 and Lol p 5 (5), both produced in the cytoplasm of RGP (12). Lol p 1 moves to the mature pollen grain surface when it encounters moisture, while Lol p 5 is stored in starch granules in the mature pollen. These granules are respirable and contain allergens (4, 5, 14). Nearly 700 starch granules (0.6-2.5 µm) are contained in a single mature RGP (11, 12).
Perennial rye grass pollen (RGP) is a potent seasonal aeroallergen in the temperate zones, especially in the early summers (15, 16).
It is a major grass pollen allergen in Australia’s temperate regions like south-eastern Queensland (17, 18). In Melbourne, exposure to perennial ryegrass is the primary reason for seasonal allergic rhinitis (AR) between late spring and early summer (3). A high prevalence of sensitization to perennial RGP is reported in Melbourne, Australia, which may be attributed to co-existing Bermuda grass sensitization (19).
Most patients with seasonal allergies in the Australian sub-continental region are sensitized to perennial ryegrass (20). A study on 330 grass-pollen allergic patients (35.3–46.6 years) with AR was conducted in subtropical (Queensland) and temperate (New South Wales, Western and South Australia) regions of Australia. The skin prick test (SPT) revealed that the sensitization to perennial ryegrass pollen and Lol p 1 was highest (amongst Johnson grass, Bermuda grass, and Bahia grass) in patients from temperate regions. The IgE test for Lol p 1 was significantly higher (p≤0.001) compared to other allergens in patients from South Australia (21). Further, a retrospective study conducted in Melbourne found 100% sensitization to perennial RGP in 85 asthmatic patients reporting to the emergency departments of a hospital during the thunderstorm asthma epidemic in November 2016 (19).
A longitudinal asthma cohort study in Melbourne was carried out on 479 patients to understand the sensitization to rye grass. The patients were recruited at 7 years of age and underwent regular follow-up till the age of 50 years. Sensitization to rye grass was found to be the least in the non-asthmatic group (3%), increased in the viral-associated wheeze group (14%), and asthma (37%) groups. At 10 years of age, the prevalence in the Severe Asthma group was 45%. In the non-asthmatic group, the prevalence of rye grass sensitization increased from recruitment to 10 years of age (3% to 13%), decreased to 14 years of age (13% to 2%), and increased again to 21 years of age (2% to 12%). In the viral-associated wheeze group, there was an increase in the rate from the recruitment group to 10 years of age (14% to 22%) and from 14 to 21 years of age (23% to 35%). Sensitization prevalence to rye grass presented 2 peaks in the cohort, one from 7 to 10 years of age and the other from 14 to 21 years of age (22).
A study involving 66 children (5 months to 15 years) having Atopic Dermatitis (AD) evaluated the sensitization prevalence to perennial ryegrass, among other food and inhalant allergens, using IgE reactivity in Virginia, US. It was observed that sensitivity to perennial ryegrass first developed during the pre-school years and was seen to increase from infancy to adolescence. The sensitization prevalence was observed to be 17% in children less than 2 years of age that increased to 57% in 2-5-year-old children (23). However, a cross-sectional study in Mexico on 173 patients (2 to 64 years) with allergenic symptoms found the frequency of skin reactivity for perennial ryegrass to be 5.20% (24).
Further, a study in Korea on 2991 children and adolescents with AR found only 2.7% of individuals sensitized to perennial ryegrass (25).
The risk of rye grass pollen allergy is high during its pollination period. In Melbourne, the peak of atmospheric grass pollen count (APC) is around November end which is linked to the pollination season of perennial ryegrass (3). Also, the pollination season of perennial ryegrass coincides with the time of the year when thunderstorm asthma (TA) is most likely (4). The critical contributors to the risk of TA include a trifecta of RGP sensitization namely, serum RGP-specific IgE, seasonal allergic rhinitis (SAR), and thunderstorm exposure in the pollen season (5, 14, 19).
The International Study of Asthma and Allergies in Childhood (ISAAC) Phase Three, a cross-sectional survey, performed on 10,59,053 children [6-7 years (3,88,811 children) and 13-14 years (6,70,242 children)] in 98 countries found the average overall prevalence of rhino-conjunctivitis to be 14.6% and 8.5%, among the children aged 13-14 years and 6-7 years, respectively (26). It has been estimated that in the United States (US), around 13% to 17% of children live with ARC (27). Allergic rhino-conjunctivitis substantially affects the daily life activities of the school-going children causing disturbed sleep, limiting school, reduced school performance, and outdoor activities (27).
Perennial ryegrass is a species of the cool season since it grows well in cool, moist climates. However, it cannot tolerate harsh winters and thus behaves as a short-lived perennial in such regions. The best seasons for its growth are spring and autumn (1).
Perennial ryegrass grows favorably on fertile, well-drained soils. However, it is adapted to a wide variety of soils (1). It can thrive on waterlogged soils as well. Ryegrass can withstand long durations of flooding (15 to 25 days) at temperatures below 80°F (27°C). Both, alkaline and acidic soils are tolerated by perennial ryegrass (1). This grass species is susceptible to drought (though variations in genotypes may be evident towards drought stress responses (7).
Perennial ryegrass is found throughout the world. Yet, it is mostly seen in the temperate regions (15, 28). Originally found in Europe, it has extensively spread to the temperate regions of Asia and North Africa, Northern and Southern America, Australia, and New Zealand (1, 17).
It is abundantly found in Australia (4). At present, it is dominantly found in farms all over southern Victoria, especially in Melbourne (3). In New South Wales, perennial ryegrass is primarily used in pastures and crops as it adapts well to a wide variety of soils (6).
In North America, ryegrass is prevalent as pasture grass (4). While it is widely used as forage in the coastal Northwest, the Midwest, the irrigated intermountain valleys of the West, and the Northeast of the US. In the Pacific Northwest, perennial ryegrass is grown for hay (1).
The significant route of exposure to RGP is through inhalation (4). It can lead to the development of allergic reactions affecting the upper and lower respiratory system like allergic rhinitis and epidemic thunderstorm asthma (4, 14).
Rye grass pollen is a significant source for AR during the springtime and early summers (16). Seasonal allergic rhinitis is also observed in individuals sensitized to RGP (4).
In patients sensitized to perennial ryegrass, typical ocular and nasal signs and symptoms are seen when intact grains of RGP are deposited in the upper respiratory tract through inhalation (5). A longitudinal asthma cohort study in Melbourne was carried out on 479 patients who were recruited at 7 years of age and underwent regular follow-up till the age of 50 years. It was found that the prevalence of AR increased in 1 year from 1% to 6% in the group without asthma and from 45% to 56% in the asthmatic group, in patients sensitized to RGP. This has important clinical implications as the adolescent period seems to be a significant phase wherein the prevalence of rye grass sensitization and rhinitis increased (22).
A study evaluated patient (aged between 0 to more than 65 years) characteristics elicited during the pollination season for rye grass at New South Wales. Data from 9 inland base hospitals were collected from the past 13 years. It was observed that 53% of peak asthma count days spanned over the rye grass pollen season, establishing that the highest number of asthma cases occurred during the pollination season of rye grass. Patients more than 14 years of age signified 74% of the hospital visits on peak asthma count days during the pollen season while they accounted for 50% of the hospital visits on peak days at times other than the pollen season (6).
Thunderstorm Asthma (TA) occurs as a trifecta involving clinical AR, RGP sensitization, and outdoor exposure to RGP (5, 14, 19). TA is characterized by acute asthmatic attacks just after a thunderstorm. Clinical symptoms including breathlessness, wheezing, or cough develop suddenly in patients because of the bronchospasm (20). Also, recurrent asthmatic attacks are observed after periods of heavy rainfalls or thunderstorms. It may be due to the expulsion of huge amounts of respirable subcellular particles, containing allergens, from hydrated RGP (29).
The risk of asthma is strongly correlated with serum RGP–specific IgE levels (5). SAR patients who are sensitized to RGP may manifest bronchoconstriction, even though they may not have an established diagnosis of asthma (4, 5). This condition is being termed Epidemic Thunderstorm Asthma (ETSA) (5).
A study on 479 patients in Melbourne, recruited at 7 years of age and regularly followed-up till the age of 50 years, observed a decline in the prevalence of eczema in a year from 21% to 8% in the viral-associated wheeze group, 45% to 18% in the asthmatic group, from 69% to 28% in severe asthma, from 14 to 21 years of age in patients sensitized to RGP. After 21 years of age, the prevalence of eczema neither increased nor decreased in any of the groups (22).
Since rye grass pollination may increase the burden of acute asthma, the residents must be warned at the earliest in case of a forecast warning for thunderstorms to prevent the risk of asthma during the ryegrass pollen season (6).
Avoidance
Individuals who are allergic to rye grass pollen can avoid its exposure by staying indoors and keeping all windows closed (14), especially in regions where perennial ryegrass is extensively found.
Perennial ryegrass has more than 17 allergens. The molecular mass of these allergens ranges from 12 to 89 kDa (12).
However, to date, only 6 allergen molecules from perennial ryegrass have been formally named and listed officially in the database of the World Health Organization/International Union of Immunological Studies (WHO/IUIS) Allergen Nomenclature Sub-Committee (30). The table below provides detailed information on the allergenic protein identified by WHO/IUIS (30):
Allergen | Biochemical Name | Molecular Weight (kDa) | Allergenicity |
---|---|---|---|
Lol p 1 | Beta-Expasin | 27 |
|
Lol p 2 | 11 | ||
Lol p 3 | 11 | ||
Lol p 4 | 57 | ||
Lol p 5 | 31 |
|
|
Lol p 11 | Ole e 1-related protein | 16 |
|
IgE: Immunoglobulin E, kDa: kilodaltons, RGP: rye grass pollen
Lol p 1 triggers SAR by getting lodged in the upper airways. On the other hand, Lol p 5 is released from the starchy granules when the RGP ruptures and thus enters the lower airways, especially after a thunderstorm, triggering asthma (5).
Cross-reactivity between the members of Pooids (example, Lolium perenne, Phleum pratense, and Poa pratensis) and Chloridoids (example, Cynodon dactylon, and Paspalum notatum) is well-known (15).
Similarity and sequence identity of nearly 90% has been observed between group I allergens of the subfamily Pooideae, including velvet grass (Hol l 1), timothy grass (Phl p 1), ryegrass (Lol p 1), and canary grass (Pha a 1), suggesting a close relationship between these grass species (9, 16, 34). IgE-binding (53%) and antigenic similarities (76%) have been noted between rye-grass pollens (Lol p 1) and orchard (Dactylis glomerata) (35). Lol p 1 from ryegrass shares allergenic epitopes found on the timothy allergen Phl p 5. (36). Cross-reactivity has also been noted between cocksfoot (Dac g I) and ryegrass (Lol p 1) and four identical epitopes have been identified between them (37).
Amino acid sequence homology of 70% is also reported between ryegrass (Lol p 1) and maize (Zea m 1) grass belonging to Panicoideae subfamily of Poaceae grasses (34).
Perennial ryegrass shows limited cross-reactivity with Bermuda grass. This is possibly due to the lack of group 5 allergen in Bermuda grass (15). However, Bermuda grass sensitized patients are often found to be sensitized to ryegrass in Melbourne (19). Lol p 1 and Lol p 2 were found to be cross-reactive with Cyn d 1 from Bermuda grass (15). Structural homology is found between Cyn d 1 and Lol p 1 (36).
Only limited IgE cross-reactivity is observed between perennial ryegrass (Lol p 1) and Bahia grass Pas n 1. However, 64% sequence identity of Pas n 1 has been observed with Lol p 1 (16, 38).
Author: Turacoz Healthcare Solutions
Reviewer: Dr. Christian Fischer
Last reviewed: January 2021