Saudi Journal of Otorhinolaryngology Head and Neck Surgery

ORIGINAL ARTICLE
Year
: 2022  |  Volume : 24  |  Issue : 3  |  Page : 93--98

Types of allergens among patients undergoing skin allergy testing in the south region of Saudi Arabia


Nasir A Magboul1, Salmah M Alharbi1, Abdulazeiz Al-Qahtani2, Albaraa Najmi1, Mohammed A Al Hamoud1,  
1 Department of ORL-HNS, Asir Central Hospital, Abha, Saudi Arabia
2 Department of ORL-HNS, Armed Forces Hospitals Southern Region, Khamis Mushat, Saudi Arabia

Correspondence Address:
Dr. Nasir A Magboul
Department of ORL-HNS, Asir Central Hospital, AL-Rabwah Street, Abha 62312
Saudi Arabia

Abstract

Background: Allergy skin testing can help identify the specific causative allergens to confirm the diagnosis and design treatment for Allergic rhinitis. Objective: The study aimed to assess the types of allergens among participants who underwent Skin Allergy Test in the Southern Region of Saudi Arabia. Methods: This retrospective review of hospital records examined the results of the skin prick test from January 2018 to October 2020. Participants who underwent the same panel of allergens were included. Results: Forty-two participants were included. Only one participant (2.4%) showed no response toward any allergen, while the remainder (97.6%) exhibited a positive reaction toward at least one allergen. The highest rates of sensitization were to pollens (83.3%), followed by house dust mites (14.3%), and animal epithelia (28.6%). The most frequent pollens were Bermuda grass (64.3%), followed by Ryegrass (26.2%) and Russian thistle (21.4%). Positive reactions to Dermatophagoides pteronyssinus and Dermatophagoides farinae were observed in 14.3% and 9.5% of participants, respectively. The rates of sensitization to Epithelia of the cats were higher than that to Epithelia of dogs (26.2% vs. 14.3%, respectively). No significant association was detected between the type of aeroallergen and the age or gender of the participants. Conclusions: The most prevalent aeroallergens in the Southern region of Saudi Arabia are pollens, followed by house dust mites and animal epithelia. Sensitization to more than one allergen was common. The use of preventive measures is warranted to reduce sensitization to allergens.



How to cite this article:
Magboul NA, Alharbi SM, Al-Qahtani A, Najmi A, Al Hamoud MA. Types of allergens among patients undergoing skin allergy testing in the south region of Saudi Arabia.Saudi J Otorhinolaryngol Head Neck Surg 2022;24:93-98


How to cite this URL:
Magboul NA, Alharbi SM, Al-Qahtani A, Najmi A, Al Hamoud MA. Types of allergens among patients undergoing skin allergy testing in the south region of Saudi Arabia. Saudi J Otorhinolaryngol Head Neck Surg [serial online] 2022 [cited 2022 Nov 29 ];24:93-98
Available from: https://www.sjohns.org/text.asp?2022/24/3/93/356930


Full Text



 Introduction



Allergy is defined as a hypersensitive reaction by the immune system of the body that is induced by an unknown substance. There are four types of hypersensitivity reactions, and allergy is known as Type I (immediate) reaction. Allergy manifests with a wide range of presentations including allergic rhinitis, conjunctivitis, eczema, and bronchial asthma. The allergic reaction is mediated through the production of immunoglobulin E (IgE) by basophils and mast cells.[1]

Allergic diseases are highly prevalent worldwide, representing serious health problems due to their negative impact on the quality of life besides the burden, they impose on the health-care costs and the reduced work performance.[2],[3]

In most cases, allergens are proteins or glycoproteins with a molecular weight ranging from 5000 to 100,000 Daltons. In some cases, polysaccharides and other low-molecular-weight substances may be allergenic. The well-known indoor allergens include house dust mites, pets, cockroaches, and rodents. Outdoor allergens include pollens and molds.[4] The response to allergens differs according to the route of exposure and the size of the allergens. Inhaled allergens cause a respiratory reaction, whereas ingested or injected exposures cause gastrointestinal, cutaneous, or anaphylactic reactions. Allergens with a size ranging between 20 and 60 μm in diameter are easily carried by the wind and cause nasal and ocular symptoms (allergic rhinoconjunctivitis). Particles measuring 7 μm can deposit in the airways and cause respiratory symptoms.[5]

To confirm the sensitization to a certain allergen in a patient with allergic manifestations, skin prick tests are used.[6] The skin prick test is a safe diagnostic procedure that can be performed in infants as well as elderly people.[7] The test shows a high sensitivity to aeroallergens, particularly the pollens and house dust mites.[8]

The determination of the patterns of allergen sensitization in a certain geographic region is crucial for allergic disease management.[9] This is particularly important in regions where aeroallergen monitoring systems are not yet well established, such as the gulf region.[10] Therefore, the present study aimed to assess the most common allergen types among patients who underwent allergy skin tests in the Southern Region of Saudi Arabia.

 Methods



Ethical considerations

The study protocol was approved by the Ethics Committee of the Armed Forces Hospital, Southern Region, Saudi Arabia. Confidentiality of the participants' data was maintained by keeping the data collection sheets anonymous after giving a code number to each subject.

Study design, setting, and date

This retrospective, hospital files-based study was conducted at the Armed Forces Hospital, Southern Region, Saudi Arabia between January, 2018 and October 2020.

Procedure

The hospital records of all participants who underwent a skin allergy test during the period from January 2018 to October 2020 were revised. All participants of both sexes, regardless of their age, were included in the study. The same panel of allergens was used in all subjects.

A data collection sheet was employed to record the extracted data, which included the subject's age, gender, response to control, and response to the tested allergens.

Data analysis

The data were extracted, revised, coded, and processed using the statistical software IBM SPSS, version 22 (SPSS, Inc. Chicago, IL, USA). All statistical analyses were performed using two-tailed tests. Descriptive analysis based on frequency and percentage was done for all variables including participants' demographic data and reactions to different sensitizers. Crosstabulation was used to show the distribution of participants' reactions to different allergens by their age and gender. The significance of the association was assessed using Pearson's Chi-square test for independence of observations. A value of P < 0.05 was considered statistically significant.

 Results



A total of 42 participants in the Southern region of Saudi Arabia underwent skin allergy tests during the period from January 2018 to October 2020. Participants' ages ranged from 6 to 74 years, with a mean age of 28.1 ± 13.9 years. The most frequent age group was 20–29 years (31%), followed by the age group <20 years (26.2%). Males (52.4%) outnumbered females (47.6%). As for the positive control results, only 11.9% of participants showed no reaction [Table 1].{Table 1}

[Figure 1] demonstrates the response to allergens among the studied patients. Only one patient (2.4%) showed no allergic reaction toward any of the used allergens, while the remainder (97.6%) exhibited a positive reaction toward at least one of the tested allergens. In more detail, 83.3% of the patients showed a positive reaction toward one or more types of pollens, 14.3% had a positive reaction toward one of the mites, and 28.6% toward the cat and/or dog epithelia.{Figure 1}

[Table 2] shows the frequency of positive reactions to different allergens among the studied patients. Seven (16.7%) patients showed negative reactions to all pollens sensitizers. Positive reactions to pollens allergens were exhibited by 22 (52.4%) patients for one allergen only, by nine (21.4%) patients to two pollens, by two (4.8%) to three pollens, and one (2.4%) patient each to four and five pollens. As for mites' allergens, 36 (85.7%) patients showed negative reactions to both types, while 3 (4.8%) showed a positive reaction to one of them and 4 patients (9.5%) showed positive reactions to both types. As for the epithelia of animals, 30 patients (71.4%) showed negative reactions to both animal epithelia, 7 (16.7%) showed a positive reaction toward one of them, and 5 (11.9%) showed positive reactions to both cat and dog epithelia. In total, only one patient (2.4%) showed negative reactions to all allergens while 30 (71.4%) showed a positive reaction to one allergen only, 10 patients (23.8%) showed positive reactions to two allergens, and one patient (2.4%) showed positive reactions to pollens, animal epithelia, and mites.{Table 2}

[Table 3] outlines the different types of allergens that were detected among the patients who underwent the skin allergy test. As for molds, Alternaria sensitizer was used, and all patients showed negative results. Considering pollens, the most frequent sensitizer that showed a positive reaction was Cynodon dactylon (Bermuda grass, 64.3%), followed by Lolium perenne (ryegrass, 26.2%), Salsola kali (Russian thistle, 21.4%), Plantago lanceolata (plantain, 7.1%), then Olea europaea (olive) and Phleum pratense (timothy) (4.8% for each). The least pollen sensitizer to show a positive reaction was Artemisis Vulgaris (mugwort, 2.4%). Regarding mites, 14.3% of the patients showed a positive reaction to Dermatophagoides pteronyssinus and 9.5% showed a positive reaction to Dermatophagoides farinae. Considering animal epithelia, 26.2% of the patients showed positive reactions to the epithelia of cats while 14.3% showed positive reactions to the epithelia of dogs.{Table 3}

[Table 4] depicts the relationship of the patients' positive reactions to allergens with age and gender. As for pollens, the highest positive reactions were reported among patients aged 30–39 years (100%), followed by patients aged <20 years. Furthermore, 90.9% of males showed positive reactions to pollens compared to 75% of females. As for mites, 37.5% of patients aged 40 years or more had positive reactions versus none of those aged <20 years. Furthermore, 20% of females showed a positive reaction to mites in comparison to 9.1% of males. Considering epithelia of animals, a positive reaction was reported among 40% of patients aged 30–39 years versus 12.5% of those aged above 40 years. Furthermore, 36.4% of males had positive reactions to animals' epithelia compared to 20% of females. All these relations were statistically insignificant (P > 0.05).{Table 4}

 Discussion



Allergic diseases are frequently encountered medical problems. Allergy testing can help the clinician determine if a patient's complaint is caused by an allergy and identify the specific causative allergens, which is of paramount importance in confirming the diagnosis and designing treatment.[6],[9] The current study aimed to assess the types of allergens among the patients who underwent skin allergy testing in the Southern Region of Saudi Arabia [Table 5].{Table 5}

The results of the present study showed that only one patient (2.4%) had no allergic reaction toward any of the used allergens, while the remainder (97.6%) exhibited a positive reaction toward at least one of the tested allergens. In more detail, 83.3% of the patients showed a positive reaction toward one or more types of pollens, 14.3% had a positive reaction towards one of the house dust mites, and 28.6% toward the cat and/or dog epithelia.

These findings agree with the results of earlier studies in Saudi Arabia and other countries, which reported pollens as the most prevalent outdoor allergens and house dust mites as the most detected indoor allergen. The prevalence rates and the types of detected allergic pollens varied according to the geographic location, which may be related to differences in the nature of plants, climate, and lifestyle.

In Saudi Arabia, the patterns of skin sensitization were assessed in several regions, but no such study was conducted in the Southern region. Almogren[11] reported on the results of the skin prick test of 139 patients in Riyadh. He found that 75.5% reacted to one or more allergens, with the most prevalent allergens in children being pollens (56%), followed by the house dust mites (43.9%), and cat epithelia (43.9%). In adults, the most common allergens were house dust mites (71.8%), pollens (26.5%–59.3%), and cat epithelia (31.2%). AlKhater[12] studied skin sensitization profiles of 100 Saudi asthmatic children in Al-Khobar, Saudi Arabia. The study reported the most common indoor allergens to be the house dust mites (54%), cat fur (53%), and the German cockroach (26%). The most prevalent outdoor allergens included pollens as well as molds, such as Alternaria and Aspergillus species (21% each).

To compare the most common the most common allergen in different regions in Saudi Arabia including our study:[13]

In other gulf countries, comparable results were also noted. A study in the United Arab Emirates[14] included 180 children with allergies among whom the most common allergens were house dust mites (38.3 and 37.2%) and Cat dander (17.2%). Zahraldin et al.[10] studied the pattern of aeroallergen hypersensitivity in 473 children in Qatar. They found that the most common aeroallergen was house dust mites (38.1%), followed by the cat (22.6%), A. Alternata (18.8%), the American cockroach (18.4%), and the dog (14.0%).

In the United States, the third National Health and Nutrition Examination Survey (NHANES III)[15] tested ten allergens in the population from 1988 to 1994. The highest prevalence rates were for house dust mites (27.5%), pollens (26.9%), cockroaches (26.1%), and cat epithelia (17.0%). The lowest rate was for peanuts (8.6%). In the Philippines, Sabit et al.[16] used 15 different pollen types for conducting skin allergy tests among 541 healthy volunteers. They reported that 49% were positive for both pollens and house dust mites, 14% for pollens only, and 37% for house dust mites.

Pollen is a fine powder-like substance that is released by weeds, grass, and trees and becomes dispersed mainly by wind.[17] The present study revealed the most common detected allergenic pollens to be Bermuda grass (64.3%), ryegrass (26.2%), Russian thistle (21.4%), and plantain (7.1%) as well as olive and timothy (4.8% for each). The tested pollens and the rates of positive reactions varied widely across the studies. In Riyadh, Saudi Arabia, the most prevalent in children were those of Russian thistle (56%) and date palm (46.3%), while the most common in adults were Bermuda grass (59.3%) and Ragweed (26.5%).[11] In Al-Khobar, Saudi Arabia, the most common in children included Russian thistle (48%), Timothy grass (23%), Chenopodium album (23%), and Prosopis glandulosa (19%).[12] In the United States,[15] the most common pollens were Perennial rye (26.9%), Ragweed (26.2), and Bermuda grass (18.1%). The lowest rate was for peanuts (8.6%).

House dust mites are considered the most common indoor allergen all over the world. Two mites are tested, namely the D. pteronyssinus and the D. farinae. We found that only 14.3% of participants showed a positive reaction (4.8% to one mite and 9.5% to both types). In Riyadh, Saudi Arabia, D. petronyssinus and D. farinae accounted for 21.7% and 19.5% of reactions in adults, whereas the rates were 38.9% and 11.1%, respectively, in children.[11] In the United Arab Emirates, D. farinae and D. petronyssinus accounted for 38.3% and 37.2% of the positive reactions, respectively. The sensitization rates in Al-Khobar, Saudi Arabia were 48% for D. farinae and 45% for D. pteronyssinus.[12] In Qatar, positive reactions were detected mostly for D. petronyssinus (38.1%) and less for D. farinae (29.0%).[10] In Northern Europe, a study estimated that 10% of participants were sensitized to storage mites.[18] Research showed that reducing the exposure to mite allergens through health education of parents and mattress encasement caused a decrease in sensitization to mites in toddlers and preschool children.[19],[20]

In the current study, about one-quarter (28.6%) of the patients showed a positive reaction toward animals' epithelia (16.7% to one animal and 11.9% to both). Animals produce allergens in forms unique to each species. Cat allergens are found mainly in cat saliva, sebaceous glands in the skin, and the urine of male cats. Cat allergens can remain inside houses up to 4–6 months after the removal of the source.[21] Dog allergens are present in dander, saliva, urine, and serum. All dog breeds produce allergenic proteins, even short-haired dogs.[22] A pan-European study revealed that 26% and 27% of adults were sensitized to cats and dogs, respectively.[23]

The results of the present study showed a lack of statistically significant association between the positive reaction to one of the tested allergens categories and either age or gender.

However, other studies have reported the presence of significant associations. The NHANES III[15] revealed a significant association of positive reaction to dust mites, cat, and most tested pollens with the second and third decades of life. Sabit et al.[16] stated that the rates of sensitization increased in the third and fourth decades of life and declined thereafter. Age differences in the rates of sensitization were also detected by longitudinal studies. In Denmark, repeated-specific IgE assessments from 1985 to 2011 revealed increased sensitization to aeroallergens in participants who were followed from the age of 1–26 years.[24] An Italian longitudinal study found that sensitization to common allergens increased with age in participants under 40 years old.[25] A multi-center study in Europe and Australia concluded that the sensitization to cat and house dust mites decreased after the age of 20 years.[26]

Differences in the prevalent types of aeroallergens were also reported among the age groups. Almogren[11] in Riyadh found that the sensitization to house dust mite and Aspergillus was more prevalent in adults while Russian thistle and date palm sensitization was more frequent among children. Zahraldin et al.[10] reported that house dust mites tended to be the most common allergen for all age groups, but the sensitization rate was highest among children beneath 5 years. Rates of cat and dog allergens were higher in children older than 10 years, while rates of Alternaria were higher in children aged 6–14 years compared to those younger than 5 years.

As regards the associations of sensitization with gender, NHANES III[15] showed a significant association with the male gender. This also was demonstrated by a later study in 2014.[27] They explained the gender difference by the higher levels of serum IgE in male participants at any age.[28] Similarly, a longitudinal study in Finland[29] found that sensitization was more common in men than in women. However, Sabit et al.[16] found that females show higher sensitizations than males in age groups above 9 years old.

The nondetection of significant associations in the present study between the types of allergens and the age or gender of the participants may be attributed to the relatively small sample size as well as differences in the inclusion criteria of the studies. Some studies included both normal and allergic participants, while others focused only on the skin prick test results of a group of allergic patients such as asthmatics.

The present study was limited by the relatively low number of included patients. In addition, the nature of these studies renders the generalization of the results nonfeasible as aeroallergens show wide geographical variations. However, the value of the results lies in the determination of the most prevalent aeroallergens in the Southern region of Saudi Arabia to aid the implementation of preventive measures that may reduce the exposure to the allergens and reduce the sensitization of the patients. This can improve the clinical condition and the quality of life of those patients.

 Conclusions



The most prevalent aeroallergens in the Southern region of Saudi Arabia are the pollens, followed by house dust mites, and animal epithelia. Sensitization to more than one allergen was common. The use of preventive measures is warranted to reduce the sensitization to allergens.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Hosoki K, Boldogh I, Sur S. Innate responses to pollen allergens. Curr Opin Allergy Clin Immunol 2015;15:79-88.
2Pawankar R. Allergic diseases and asthma: A global public health concern and a call to action. World Allergy Organ J 2014;7:12.
3Zuberbier T, Lötvall J, Simoens S, Subramanian SV, Church MK. Economic burden of inadequate management of allergic diseases in the European Union: A GA (2) LEN review. Allergy 2014;69:1275-9.
4Gautier C, Charpin D. Environmental triggers and avoidance in the management of asthma. J Asthma Allergy 2017;10:47-56.
5Platts-Mills TA, Heymann PW, Longbottom JL, Wilkins SR. Airborne allergens associated with asthma: Particle sizes carrying dust mite and rat allergens measured with a cascade impactor. J Allergy Clin Immunol 1986;77:850-7.
6Heinzerling L, Mari A, Bergmann KC, Bresciani M, Burbach G, Darsow U, et al. The skin prick test – European standards. Clin Transl Allergy 2013;3:3.
7Liccardi G, D'Amato G, Canonica GW, Salzillo A, Piccolo A, Passalacqua G. Systemic reactions from skin testing: Literature review. J Investig Allergol Clin Immunol 2006;16:75-8.
8Antunes J, Borrego L, Romeira A, Pinto P. Skin prick tests and allergy diagnosis. Allergol Immunopathol (Madr) 2009;37:155-64.
9Scott M, Roberts G, Kurukulaaratchy RJ, Matthews S, Nove A, Arshad SH. Multifaceted allergen avoidance during infancy reduces asthma during childhood with the effect persisting until age 18 years. Thorax 2012;67:1046-51.
10Zahraldin K, Chandra P, Tuffaha A, Ehlayel M. Sensitization to common allergens among children with asthma and allergic rhinitis in Qatar. J Asthma Allergy 2021;14:287-92.
11Almogren A. Airway allergy and skin reactivity to aeroallergens in Riyadh. Saudi Med J 2009;30:392-6.
12AlKhater SA. Sensitization to common aeroallergens in asthmatic children in the eastern region of Saudi Arabia. Saudi J Med Med Sci 2017;5:136-41.
13Marglani O. Common allergens noticed in patients with allergic rhinitis and asthma at a tertiary care centre in western Saudi Arabia. Saudi J Otorhinolaryngol Head Neck Surg 2016;18:37.
14Sharif H, Salih E, Awad H, Albarazi R. Common aeroallergens among children with allergies in the United Arab Emirates. Indian J Allergy Asthma Immunol 2018;32:4-9.
15Arbes SJ Jr., Gergen PJ, Elliott L, Zeldin DC. Prevalences of positive skin test responses to 10 common allergens in the US population: Results from the third National Health and Nutrition Examination Survey. J Allergy Clin Immunol 2005;116:377-83.
16Sabit M, Wong C, Andaya A, Ramos JD. Pollen allergen skin test and specific IgE reactivity among Filipinos: A community-based study. Allergy Asthma Clin Immunol 2020;16:74.
17Mansouritorghabeh H, Jabbari-Azad F, Sankian M, Varasteh A, Farid-Hosseini R. The most common allergenic tree pollen grains in the Middle East: A narrative review. Iran J Med Sci 2019;44:87-98.
18Jõgi NO, Kleppe Olsen R, Svanes C, Gislason D, Gislason T, Schlünssen V, et al. Prevalence of allergic sensitization to storage mites in Northern Europe. Clin Exp Allergy 2020;50:372-82.
19Tsitoura S, Nestoridou K, Botis P, Karmaus W, Botezan C, Bojarskas J, et al. Randomized trial to prevent sensitization to mite allergens in toddlers and preschoolers by allergen reduction and education: One-year results. Arch Pediatr Adolesc Med 2002;156:1021-7.
20Portnoy J, Miller JD, Williams PB, Chew GL, Miller JD, Zaitoun F, et al. Environmental assessment and exposure control of dust mites: A practice parameter. Ann Allergy Asthma Immunol 2013;111:465-507.
21Sparkes AH. Human allergy to cats: A review for veterinarians on prevalence, causes, symptoms and control. J Feline Med Surg 2022;24:31-42.
22Wintersand A, Asplund K, Binnmyr J, Holmgren E, Nilsson OB, Gafvelin G, et al. Allergens in dog extracts: Implication for diagnosis and treatment. Allergy 2019;74:1472-9.
23Heinzerling LM, Burbach GJ, Edenharter G, Bachert C, Bindslev-Jensen C, Bonini S, et al. GA (2) LEN skin test study I: GA (2) LEN harmonization of skin prick testing: Novel sensitization patterns for inhalant allergens in Europe. Allergy 2009;64:1498-506.
24Nissen SP, Kjaer HF, Høst A, Nielsen J, Halken S. The natural course of sensitization and allergic diseases from childhood to adulthood. Pediatr Allergy Immunol 2013;24:549-55.
25Dottorini ML, Bruni B, Peccini F, Bottini P, Pini L, Donato F, et al. Skin prick-test reactivity to aeroallergens and allergic symptoms in an urban population of central Italy: A longitudinal study. Clin Exp Allergy 2007;37:188-96.
26Amaral AF, Newson RB, Abramson MJ, Antó JM, Bono R, Corsico AG, et al. Changes in IgE sensitization and total IgE levels over 20 years of follow-up. J Allergy Clin Immunol 2016;137:1788-95.e9.
27Salo PM, Arbes SJ Jr., Jaramillo R, Calatroni A, Weir CH, Sever ML, et al. Prevalence of allergic sensitization in the United States: Results from the National Health and Nutrition Examination Survey (NHANES) 2005-2006. J Allergy Clin Immunol 2014;134:350-9.
28Barbee RA, Halonen M, Lebowitz M, Burrows B. Distribution of IgE in a community population sample: Correlations with age, sex, and allergen skin test reactivity. J Allergy Clin Immunol 1981;68:106-11.
29Haarala AK, Sinikumpu SP, Vaaramo E, Jokelainen J, Timonen M, Auvinen J, et al. Incidence and remission of aeroallergen sensitization in adults in Northern Finland: 15 years longitudinal study. Sci Rep 2021;11:4249.