|Year : 2017 | Volume
| Issue : 2 | Page : 98-103
Prevalence of sensitization to mould and yeast allergens in Egyptian patients with respiratory allergy
Nabil E Khatab1, Atef A Ibrahim1, Maged M Refaat2, Mohamed N Farres2, Ali E Ali1, Medhat M Elamawy1
1 Department of Internal Medicine, Benha Faculty of Medicine, Benha University Hospitals, Benha, Egypt
2 Department of Internal Medicine, Allergy and Clinical Immunology Unit, Faculty of Medicine, Ain Shams University Hospitals, Cairo, Egypt
|Date of Submission||23-Jul-2017|
|Date of Acceptance||07-Aug-2017|
|Date of Web Publication||20-Nov-2017|
Medhat M Elamawy
Department of Internal Medicine, Faculty of Medicine, Benha University Hospitals, Benha, 13518
Source of Support: None, Conflict of Interest: None
Background Burden of fungal allergic diseases to humans is broad and still needs much clarification on the prevalence of its related disease. Asthma-related deaths, hospital admissions, respiratory symptoms, and pulmonary functions can be adversely affected by high fungal spore concentrations in outdoor air.
Aim The aim of this study was to evaluate the prevalence of sensitization to various species of mould and yeast allergens among other common aeroallergens in Egyptian patients with respiratory allergy diseases.
Patients and methods Totally, 200 patients with allergic bronchial asthma and/or allergic rhinitis were selected from those followed up at the Allergy and Clinical Immunology Clinic at Ain Shams University Hospitals. For each patient, detailed allergic history and clinical examination were carried out. Asthma control level and severity of allergic rhinitis were classified according to 2015 Global Initiative of Asthma report and Allergic Rhinitis and its Impact on Asthma 2008, respectively. Complete blood count and Spirometry were done. In addition, skin prick test to 10 mould allergens, besides other six common aeroallergens and positive and negative controls, were carried out. Statistical package for the social sciences was used.
Results The results revealed that 74% had positive results to at least one allergen extract. Out of skin prick test-positive participants, 41.9% showed positivity toward fungal allergen. Alternaria alternate and Penicillium spp. mixture each represented 32.2% of positive fungal sensitivity patients. Moreover, 38.9% of poorly controlled asthmatic patient’s category was fungal sensitized, whereas the percentage in well-controlled patients was 30.8% and it was a significant finding as P value was 0.02.
Conclusion Fungal sensitivity is clearly correlated with respiratory allergic disease and its severity.
Keywords: allergic rhinitis, bronchial asthma, Egyptian patients, fungal respiratory allergy, respiratory allergic diseases, sensitization
|How to cite this article:|
Khatab NE, Ibrahim AA, Refaat MM, Farres MN, Ali AE, Elamawy MM. Prevalence of sensitization to mould and yeast allergens in Egyptian patients with respiratory allergy. Benha Med J 2017;34:98-103
|How to cite this URL:|
Khatab NE, Ibrahim AA, Refaat MM, Farres MN, Ali AE, Elamawy MM. Prevalence of sensitization to mould and yeast allergens in Egyptian patients with respiratory allergy. Benha Med J [serial online] 2017 [cited 2018 Aug 18];34:98-103. Available from: http://www.bmfj.eg.net/text.asp?2017/34/2/98/218826
| Introduction|| |
Although allergic diseases are increasing dramatically worldwide, only few studies evaluated asthma prevalence in Egypt; the prevalence ranged from 4.8  to 9.1% . The role of fungi in allergic respiratory symptoms is well established and has been described since the early 1700s ,. Fungal allergic diseases in humans are broad and need more clarifications about definitions and diagnostic criteria ,. Fungal exposure is associated with the development of asthma and rhinitis as well as epidemics of asthma exacerbations . Asthma-related deaths, hospital admissions, respiratory symptoms and peak expiratory flow rates can be adversely affected by high fungal spore concentrations in outdoor air .
| Patients and methods|| |
This cross-sectional study was conducted at the Allergy Outpatient Clinic of Ain Shams University Hospital from February 2015 to June 2016 and included 200 patients who were diagnosed with allergic bronchial asthma and/or allergic rhinitis. An informed consent was taken from all studied participants after ensuring the data confidentiality. The study was approved by the Institutional Ethics Committee of the Faculty of Medicine, Benha University and Ain Shams University Hospital.
Allergic bronchial asthma and allergic rhinitis patients were diagnosed according to the 2015 Global Initiative of Asthma (GINA) report, and Allergic Rhinitis and its Impact on Asthma (ARIA) guidelines 2008, respectively. Both male and female patients were included in the study; patients with various body weights and various age groups were included. In allergic bronchial asthma, all levels of control were selected, whereas in allergic rhinitis all grades of severity were included in the study.
The study excluded the following patients: immunocompromised patients; patients on antihistaminic therapy and other drugs that affect skin prick test (SPT) reproducibility; pregnant women; patients with chronic respiratory tract infections; and those who have chronic obstructive airway disease.
For each patient, detailed allergic history, including mould exposure, and dampness in home and workplace were obtained. Chest, skin, and ear, nose and throat (ENT) examination was performed.
Assessment of asthma control level was carried out based on the questionnaire established by 2015 GINA report. The severity of allergic rhinitis was classified as ‘mild’ and ‘moderate to severe’ according to ARIA 2008.
For each patient, the following were carried out: complete blood count; spirometry for measurement of forced expiratory volume in first second (FEV1), FEV1/forced vital capacity, and bronchodilator reversibility; and SPT to mould allergens besides other common aeroallergens using commercial standardized extracts. This was carried out at the Pulmonary Functions Laboratory Unit at Ain Shams University Hospital.
Skin test procedure
Briefly, the skin of the anterior surface of the right forearm was cleaned, sterilized, and one drop of each allergen extract was carefully applied ∼3 cm apart. The epidermis was pricked carefully with a lancet through each allergen extract drop, without causing bleeding. After 20 min, the mean wheal diameter was measured through summation of the largest diameter to the diameter perpendicular to it, and dividing the result by two. Histamine (0.1%) in HCL-buffered saline and physiologic saline was used as positive and negative controls, respectively.
The SPT was considered valid if the difference in mean wheal diameter between the positive and negative controls was at least 1 mm. A mean wheal diameter of at least 3 mm greater than the negative control was considered positive . All extracts for skin testing were supplied in early 2015 by Stallergenes (Antony, Hauts-de-Seine, France). The test was conducted to all selected patients. While performing the tests, the used allergen extracts were frequently checked for expiratory date and included the following ten fungal standardized extracts: Alternaria alternate; Chaetomium globosum; Helminthosporium halodesll; Pullularia pullulans (dimorphic fungi); Aspergillus spp. mixture (Aspergillus fumigatus, Aspergillus nidulans, Aspergillus niger); Cladosporium spp. mixture (Cladosporium cladosporioides, Cladosporium herbarum); Penicillium spp. mixture (Penicillium digitatum, Penicillium expansum, Penicillium notatum); Mucor racemosus (dimorphic fungi); Rhizopus nigricans; and Merulius lacrymans and other six aeroallergen extracts, including Betulaceae spp. tree mixtures, Chenopodiaceae spp. weed mixtures, Grasses mixture, Dermatophagoides pteronyssinus, Dermatophagoides farina, and Cat epithelium.
The collected data were tabulated and analyzed using statistical package for the social sciences version 20 software (SPSS; SPSS Inc., Chicago, Illinois, USA). Categorical data were presented as number and percentages, whereas quantitative data were expressed as mean±SD. Fisher’s exact test and χ2-test were used to compare different groups. The accepted level of significance in this work was stated at 0.05, and hence P value less than 0.001 was considered highly significant, P value less than 0.05 was considered significant, and P value greater than 0.05 was considered nonsignificant.
| Results|| |
The distribution of the studied 200 patients as regards various age groups and sex is shown in [Table 1] and [Table 2], and types of respiratory allergic diseases in studied population are presented in [Table 3]. The categorization of allergic rhinitis patients and allergic rhinitis patients with allergic bronchial asthma according to severity degree is shown in [Table 4], whereas control state of allergic bronchial asthma patients and combined allergic rhinitis with allergic asthma is shown in [Table 5].
|Table 1 Distribution of studied patients as regards various age groups (n=200)|
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|Table 2 Distribution of sexes and their ages in studied population (n=200)|
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|Table 3 Types of respiratory allergy and their prevalence in the studied population (n=200)|
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|Table 4 Categorization of allergic rhinitis patients and allergic rhinitis with allergic bronchial asthma according to severity of rhinitis (n=120)|
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|Table 5 Patient’s categorization based on the degree of asthma control (n=106)|
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The results of SPT of the studied patients revealed that 74% (148 patients) had positive results to at least one allergen extract and only 26% (52 patients) had negative SPT ([Figure 1]). Out of 148 patients who showed positivity to at least one allergen extract, 62 (41.9%) patients showed positivity toward fungal allergen ([Table 6] and [Table 7]).
|Figure 1 Results of skin prick test in studied patients (n=200 patients)|
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|Table 7 Results of skin prick tests in various age groups of studied patients (n=200 patients)|
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The results showed that each A. alternate and Penicillium spp. mixture represented 32.2% of positive fungal sensitivity patients ([Table 8]). Dust mite extracts’ sensitivity with its two species D. farina and D. pteronyssinus represents the highest prevalence of allergen extracts’ positive sensitivity whatever their predominant atopic symptoms ([Figure 2]).
|Table 8 Results of skin prick test to common fungal allergens in studied population (n=62)|
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In patients with combined allergic rhinitis and allergic bronchial asthma, the results showed that Pullularia pulluans and M. lacrymans represent the highest prevalence after dust mites’ sensitivities, and these results were significant as P values of P. pulluans and M. lacrymans represent 0.006 and 0.002, respectively ([Table 9]).
|Table 9 Results of skin prick test to common allergens in studied patients as regards predominant atopic symptoms|
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Moreover, when studying the relation of the level of asthma control and the number of positive fungal sensitivity, the results showed that five patients out of 26 patients (19.2%) in well-controlled patient’s category were sensitized to only one of the studied fungal extracts, whereas no patients out of 18 patients in poorly controlled patient’s category were sensitized to any one of studied fungal extracts and two patients out of 18 (11.1%) patients in poorly controlled patient’s category were sensitized to three of the studied fungal extracts ([Table 10]).
| Discussion|| |
This cross-sectional study included various age groups from 6 to 70 years. The selected age range was similar to that in many studies that reported the prevalence of fungal allergen sensitivities in respiratory allergic patients ,. The results showed that SPT was positive in at least one of the studied extracts in 148 (74%) patients. In studies conducted in many parts of world, positive skin reaction to at least one allergen was observed in 55–97% of the respiratory allergic patients . However, in our study the percentage of positive SPT could be higher due to two reasons: first, in the present study SPTs were used to elicit allergen extract positivity instead of intradermal tests that were used in some studies. Intradermal skin tests, although are more sensitive, are less specific compared with SPT. However, some reports demonstrated a higher prevalence of Aspergillus spp. sensitization in asthma with an intradermal test compared with an SPT (28.7 vs. 24.8%) . The second reason is related to our selected age range that was wider than that selected in these studies .
In our studied patients, 41.9% of the patients were sensitized to at least one of the studied fungal species allergens. Many studies were conducted on the prevalence of fungal sensitization; in Iran, a study showed that 23.7% of the patients were sensitive to at least one of the studied fungal species allergens . Moreover, similar studies were conducted in Singapore  and Malaysia . In a large European study on prevalence of fungal sensitivity (Alternaria spp. and Cladosporium spp.) in respiratory allergic patients, positive fungal prevalence ranged from 3% in Portugal to 20% in Spain .
This different prevalence elicited by the SPT can be due to the number of allergen extracts used, climate changes, humidity, and age of studied patients. One of the highest prevalence was reported by Sathavahana Chowdary et al. , who performed skin tests (68.4% were intradermal that obtain high yield reproducibility) on 290 individuals. Among the individuals who were sensitive to allergens, sensitivity to fungi was 44%. Still the biggest study of fungal sensitization in bronchial asthma patients is the study by O’Driscoll et al. . They found that overall 66% of their patients were sensitized to one or more fungi based on SPT or specific serum immunoglobulin E or both; the majority (76%) of those with fungal sensitization were also sensitized to nonfungal allergen such house dust mites; however, the spectrum of patients they worked on had severe asthma .
On the basis of our results and above-mentioned studies of various prevalence results on fungal sensitivities in respiratory allergic patients, we still confirm that aerobiological studies and environmental factors play a role in that fungal prevalence variation.
In the present study, percentage of fungal sensitivity in the age group 6–14 years was higher than the percentage of fungal sensitivity in the other age groups, and these results were similar to other studies .
In spite of the importance to study fungal respiratory allergic diseases, yet limited studies in Egypt were done. In the study by Ashour et al. , a total of 56 patients with bilateral nasal polyposis were enrolled and SPT was performed with 37 different allergen extracts for both inhaled extract including A. alternate and ingested allergens. A total of 41 (73.2%) patients showed positive results to SPT; of them, positive results for ‘Moulds’ was seen in 14 (34.2%) patients . Moreover, in Sharkeya, Egypt, Azab et al.  indeed confirmed the significant relation between sputum colonization with Alternaria spp. and bronchial asthma and the significant relation between colonization and sensitization to Alternaria spp.
As regards results of SPT to fungal extracts in the studied positive fungal population in this present research, the results showed that each A. alternate and Penicillium spp. mixture represents 32.2% of positive fungal sensitivity patients, followed by Aspergillus spp. mixture, accounting for 22.6%. Ecological studies of fungal spores’ prevalence found that Aspergillus spp. and Penicillium spp. are usually considered the major indoor fungi. A. alternate also has been reported in house dust samples in the absence of environmental mould spores . Concerning fungal prevalence in Egypt, Awad et al.  conducted a study to assess cultured airborne fungal concentrations in urban and rural areas and found that Alternaria spp., Aspergillus spp., Cladosporium spp., Penicillium spp., and yeasts were the predominant genera indoors and outdoors.
Although the highest prevalence of fungal sensitivities in our research is in the category of mostly indoor fungi, these fungi could also be found in outdoor environment. Moreover, until standardized fungal allergen extracts are available, the exact prevalence of fungal species sensitivities will be difficult to confirm.
In patients with combined allergic rhinitis and allergic bronchial asthma, the results showed a significant finding as regards the sensitivities to P. pulluans, M. lacrymans, and Chenopodiaceae weed mixtures, as P value represents 0.006, 0.002, and 0.02, respectively, and these results are in agreement with another study that found the sensitivity to P. pulluans to be significantly associated with more severe asthma .
Moreover, when studying the relation of the level of asthma control and the number of positive fungal sensitivity, the results showed that five patients out of 26 (19.2%) patients in well-controlled patient’s category were sensitized to only one of the studied fungal extracts, whereas no patients out of 18 patients in poorly controlled patient’s category were sensitized to any one of the studied fungal extracts and two patients out of 18 (11.1%) patients in poorly controlled patient’s category were sensitized to three of the studied fungal extracts. With a significant P value of 0.02, it can be said that the number of fungal species extract sensitivities was related with level of asthma control.
Indeed, many studies showed the relation with fungal sensitivity and severity of asthma, as some authors related mould sensitization in patients with severe asthma and multiple hospital admissions . Moreover, multiple mould reactions were also more common in the group with multiple admissions .
Moreover, Black et al.  found that patients who had been admitted in the ICU with severe, potentially life-threatening asthma were significantly more likely to have one or more positive skin tests for fungal dry weather spores. Moreover, a large cross-sectional study found that sensitization to Alternaria spp. or Cladosporium spp. is a powerful risk factor for severe asthma in several European countries .
Therefore, on the basis of our results and other above-mentioned studies, fungal sensitization is more common in respiratory allergic disease, especially in poorly controlled asthma. This study represents one of the first reports of sensitization to mould allergens in our region over a large number of Egyptian respiratory allergic patients using large fungal extract panel.
The author conveys the deepest gratitude to all professors and staff members of the Internal Medicine Department, Faculty of Medicine, Benha University, and Allergy and Clinical Immunology unit’s staff members, Ain Shams Faculty of Medicine, for their help and encouragement, and every person who helped me in completing this work.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Khallaf N, el-Ansary S, Hassan M. Acute respiratory infections: sentinel survey in Egypt. Cairo, Egypt: National ARI Control Programme, Child Survival Project, Ministry of Health, Bab El Louk; 1993.
Mansour AE, Yasein YA, Ghandour A, Zaidan O, Abo El-Abaas MM. Prevalence of bronchial asthma and its impact on the cognitive functions and academic achievement among preparatory school children in Damietta Governorate, Egypt. J Am Sci 2014; 10:119–127.
Fang Z, Ouyang Z, Hu L, Wang X, Zheng H, Lin X. Culturable airborne fungi in outdoor environments in Beijing, China. Sci Total Environ 2005; 350:47–58.
Pomés A, Chapman MD, Wünschmann S. Indoor allergens and allergic respiratory disease. Curr Allergy Asthma Rep 2016; 43:1–10.
Agarwal R. Severe asthma with fungal sensitization. Curr Allergy Asthma Rep 2011; 11:403–413.
Agarwal R. Allergic bronchopulmonary aspergillosis Chest 2009; 135:805–826.
Fukutomi Y, Taniguchi M. Sensitization to fungal allergens: resolved and unresolved issues. Allergol Int 2015; 64:321–331.
O’Driscoll BR, Hopkinson LC, Denning DW. Mold sensitization is common amongst patients with severe asthma requiring multiple hospital admissions BMC Pulm Med 2005; 5:1–4.
Heinzerling 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.
Sathavahana Chowdary V, Lakshmi P, Sangram V, Rani S, Vinay Kumar EC. Role of Fungi (molds) in allergic airway disease − an analysis in a South Indian Otolaryngology Center. Indian J Allergy Asthma Immunol 2011; 25:67–78.
Shakurnia AH, Assarehzadegan MA, Amini A, Shakerinejad G. Prevalence of fungal allergens in respiratory allergic patients in Ahvaz City, Southwest Iran. Jundishapur J Microbiol 2013; 6:1–5.
Donathi S, Sivasai KSR, Lakshmi Valluri V. Prevalence of inhalant allergens in nasobronchial allergy in Hyderabad region India. Natl J Med Res 2011; 2:431–434.
Agarwal R, Gupta D. Severe asthma and fungi: current evidence. Med Mycol 2011; 49(Suppl 1):S150–S157.
Skassa-Brociek W, Manderscheid JC, Michel FB, Bousquet J. Skin tests reactivity to histamine from infancy to elderly. J Allergy Clin Immunol 1987; 80:711–717.
Kidon MI, See Y, Goh A, Chay OM, Balakrishnan A. Aeroallergen sensitization in pediatric allergic rhinitis in Singapore: is air-conditioning a factor in the tropics? Pediatr Allergy Immunol 2004; 15:340–343.
Ishlah LW, Gendeh BS. Skin prick test reactivity to common airborne pollens and molds in allergic rhinitis patients. Med J Malaysia 2005; 60:194–200.
D’amato G, Chatzigeorgiou G, Corsico R, Gioulekas D, Jäger L, Jäger S et al.
Evaluation of the prevalence of skin prick test positivity to Alternaria and Cladosporium in patients with suspected respiratory allergy. A European multicenter study promoted by the Subcommittee on Aerobiology and Environmental Aspects of Inhalant Allergens of the European Academy of Allergology and Clinical Immunology. Allergy 1997; 52:711–716.
O’Driscoll BR, Powell G, Chew F, Niven RM, Miles JF, Vyas A et al.
Comparison of skin prick tests with specific serum immunoglobulin E in the diagnosis of fungal sensitization in patients with severe asthma. Clin Exp Allergy 2009; 39:1677–1683.
Galante D, Tassinari PA, Conesa A, Trejo E, Bianco NE. Specific IgE to indoor molds in patients with respiratory allergies. J Allergy Clin Immunol 2004; 113:S144.
Ashour ZA, Rabee H, El-Melegi HA, Attia MY, Sanad H. Evaluation of skin prick test sensitivity for 37 allergen extracts in atopic patients with nasal polyposis. Egypt J Intern Med 2014; 26:80–85. [Full text]
Azab M, Boghdadi G, Gerges M, Abd-Elsalam S, Elnaggar Y. Airway colonization with Alternaria
spp. In fungi-sensitized asthma patients in Sharkeya, Egypt Egyptian. J Med Microbiol 2016; 25:103–108.
Chapman MD, Aalberse RC, Brown MJ, Platts-Mills TA. Monoclonal antibodies to the major feline allergen Fel d I. II. Single step affinity purification of Fel d I, N-terminal sequence analysis, and development of a sensitive two-site immunoassay to assess Fel d I exposure. J Immunol 1988; 140:812.
Awad AA, Shawn GG, Patrick MT, Christopher FG. Coarse and fine culturable fungal air concentrations in urban and rural homes in Egypt. Int J Environ Res Public Health 2013; 10:936–949.
Niedoszytko M, Chełmińska M, Jassem E, Czestochowska E. Association between sensitization to Aureobasidium pullulans
spp.) and severity of asthma. Ann Allergy Asthma Immunol 2007; 98:153–156.
Black PN, Udy AA, Brodie SM. Sensitivity to fungal allergens is a risk factor for life‐threatening asthma. Allergy 2000; 55:501–504.
Zureik M, Neukirch C, Leynaert B, Liard R, Bousquet J, Neukirch F. Sensitisation to airborne moulds and severity of asthma: cross sectional study from European Community respiratory health survey BMJ 2002; 325:411.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9], [Table 10]