article information

Zahedan Journal of Research in Medical Sciences: Vol.16, issue 11; 15-19
published online: January 22, 2014
article type: Research Article
received: October 7, 2013
accepted: December 21, 2013

Isolation of Aspergillus species from Nasal Cavity and Bedroom of Healthy Volunteers and Patients with Allergic Rhinitis in Mashhad, Iran

authors:

avatar Samaneh Eidi 1 , * , avatar Abdolmajid Fata 2 , avatar Reza Farid-Hosseini 3 , avatar S. Amir Kamali 1 , avatar Zahra Hajari 1 , avatar Ali Naseri 2 , avatar Mehdi Bakhshaee 4

Department of Pathobiology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran
Department of Medical Mycology and Parasitology, Mashhad University of Medical Sciences, Mashhad, Iran
Bu-Ali Immunology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
Department of Otorhinolaryngology, Head and Neck Surgery, Mashad University of Medical Sciences, Mashhad, Iran

how to cite: Eidi S, Fata A, Farid-Hosseini R, Kamali S A, Hajari Z, et al. Isolation of Aspergillus species from Nasal Cavity and Bedroom of Healthy Volunteers and Patients with Allergic Rhinitis in Mashhad, Iran. Zahedan J Res Med Sci. 2014;16(11): 15-19. 

Abstract

Background:

The purpose of this study was to investigate the presence, frequency and comparison of Aspergillus spp. in nasal cavity and bedroom of healthy volunteers and patients with allergic rhinitis.

Materials and Methods:

In this cross-sectional study, a group of patients with allergic rhinitis (N=50) were selected based on positive skin prick test. Healthy volunteers were chosen to be in the comparison group by matching in age, gender, and no history of respiratory system disease. Samples from nasal cavity and different parts of bedroom were collected and cultured. Cultured Aspergillus spp. was identified by standard mycological techniques.

Results:

The most common species isolated from all samples of healthy volunteers was A. flavus (88%), followed by A. niger (76%) and A. fumigatus (74%). A. flavus (56%) was the predominant species isolated from all samples of patients, followed by A. niger (34%) and A. fumigatus (6%).

Conclusion:

A. flavus was the most prevalent species of Aspergillus both healthy volunteers and patients. The presence of Aspergillus in homes does not necessarily imply a cause and effect relationship with illness, but we speculate that A. flavus may be a major source of aeroallergens along with A. niger and A. fumigatus; and should alert physicians and healthcare professionals to do more vigorous environmental testing.

Introduction

Fungi are common in both outdoor and indoor environments as spores, mycelial fragmentation or dissociated intracellular and extracellular components. They are usually saprophytic and harmless but under extra ordinary conditions such as lung diseases or weakened immune systems, they can cause infections indifferent spectrum of illness includes allergic reactions, lung infections, and infections in other organs [1].

It has been reported that the increasing incidence of allergic diseases, such as asthma, rhinitis and atopy, is caused by molds in the indoor environment [2]. Therefore, indoor air quality has become an important health concern. Considering the fact that an allergic reaction may occur with exposure to minute concentration of an allergen [3], indoor molds could create a health risk for atopic individuals occupying such a building.

More than 80 genera of fungi have been associated with symptoms of respiratory tract allergies [4]. Aspergillus can be a part of indoor mycoflora. Several species of Aspergillus have been shown to be allergenic, including A. fumigatus, A. niger, A. flavus, and A. oryzae [5]. In susceptible individuals or those exposed to extremely high inocula, invasive aspergillosis may follow Aspergillus exposure. It has been demonstrated previously that individuals can and do become sensitized to Aspergillus allergens [6]. The aim of this study was to investigate the presence, frequency and comparison of Aspergillus spp. in nasal cavity and bedroom of healthy volunteers and patients with allergic rhinitis.

Results

Out of all healthy volunteers enrolled, 15 (30%) were females and 35 (70%) males. The age range of them was 15 to 67 years (median 30). Out of all patients enrolled 30 (60%) were females and 20 (40%) were males. Their age range varied from 18 to 61 years (median 27). A total of 500 plates were collected from both groups, of which 100 were nasal cavity samples and 400 were bedroom samples. In the control group, colonization with the genus Aspergillus was obtained in 32 (64%) out of the 50 nasal cavity samples, 45 (90%) bedroom air samples, 28 (56%) pillow samples, 26 (52%) dust of the bed samples, 38 (76%) dust on the shelf samples all out of 50 bedrooms. The most common species isolated from all samples of healthy volunteers was A. flavus (88%), followed by A. niger (76%) and A. fumigatus (74%). In the patients group, colonization with the genus Aspergillus was obtained in 17 (34%) out of the 50 nasal cavity samples, 17 (34%) bedroom air samples, 9 (18%) pillow samples, 12 (24%) dust of the bed samples, 7 (14%) dust on the shelf samples all out of 50 bedrooms. The most common species isolated from all samples of patients was A. flavus (56%), followed by A. niger (34%) and A. fumigatus (6%).

Figures 1 and 2 show the frequency of Aspergillus spp. isolated from nasal cavity and different parts of bedroom in control and patient groups, respectively. In table 1, we present the distribution of Aspergillus spp. isolated from nasal cavity and different parts of bedroom in control and patient groups. The most commonly isolated species in nasal cavity of control group was A. fumigatus (32%), followed by A. flavus (24%) and A. niger (10%). A. flavus had the highest rate in the bedroom air and pillow samples (58% and 42%, respectively), followed by A. niger (46% and 12%, respectively) and A. fumigatus (24% and 2%, respectively). A. fumigatus (42%) was the predominant species in dust on the shelf samples, followed by A. niger (30%), and A. flavus (10%); whereas A. flavus was the most abundant species in dust of the bed (32%), followed by A. fumigatus (28%) and A. niger (12%).

The most commonly isolated species in nasal cavity of patients group was A. flavus (26%), followed by A. niger (6%) and A. fumigatus (2%). A. flavus had the highest rate in the bedroom air, pillow and dust of the bed samples (22%, 8% and 16%, respectively), followed by A. niger (10%, 6% and 8%, respectively), and A. fumigatus (2%, 4% and 0%, respectively). In dust on the shelf, A. niger (8%) was the predominant species, followed by A. flavus (6%). Overall, there were significant differences in frequency of isolation of A. flavus and A. niger in all samples of healthy volunteers, compared with all samples of patients (p=0.001). Frequency of A. niger isolates from bedroom air and dust on the shelf samples had significant correlation in healthy volunteers, compared with patients (p=0.001). Furthermore, there was significant difference in frequency of A. flavus isolates from bedroom air and pillow samples between healthy volunteers and patients (p=0.001). Also, frequency of A. fumigatus isolates from nasal cavity and bedroom air samples had significant correlation in healthy volunteers, compared with patients (p=0.001).

Frequency of Aspergillus spp. isolated from nasal cavity and different parts of bedroom in healthy volunteers
Frequency of Aspergillus spp. isolated from nasal cavity and different parts of bedroom in healthy volunteers
Figure 1.

Frequency of Aspergillus spp. isolated from nasal cavity and different parts of bedroom in healthy volunteers

Frequency of Aspergillus spp. isolated from nasal cavity and different parts of bedroom in patients with allergic rhinitis
Frequency of Aspergillus spp. isolated from nasal cavity and different parts of bedroom in patients with allergic rhinitis
Figure 2.

Frequency of Aspergillus spp. isolated from nasal cavity and different parts of bedroom in patients with allergic rhinitis

Table1.

Distribution of Aspergillus spp. isolated from nasal cavity and different parts of bedroom in control and patient groups

Nasal cavity N (%)Bedroom air N (%)Pillow N (%)Dust of the bed N (%)Dust of the shelf N (%)
ControlPatientControlPatientControlPatientControlPatientControlPatient
A. flavus 12 (24)13 (26)29 (58)11 (22)21 (42)4 (8)16 (32)8 (16)5 (10)2 (6)
A. fumigatus 16 (32)1 (2)12 (24)1 (2)1 (2)2 (4)14 (28)0 (0)21 (42)0 (0)
A. niger 5 (10)2 (6)23 (46)5 (10)6 (12)2 (6)6 (12)4 (8)15 (30)4 (8)
Total number of isolates 321664172883612416

Discussion

In our study, 100% and 70% bedrooms of healthy volunteers and allergic rhinitis patients showed the presence of Aspergillus, respectively. Moreover, the Aspergillus spp. is isolated from 64% and 34% nasal cavity samples of healthy volunteers and allergic rhinitis patients, respectively.

Fungal allergenicity and its role in the pathogenesis of rhinitis are increasingly investigated these days and several allergenic fungi including Aspergillus have been determined [9]. On the other hand, people spend 90% of their time indoors, 50-70% at home, and 30% in the bedroom, almost one third of their life; therefore, indoor air quality has become an important health concern [10]. Many studies have shown that indoor Aspergillus is an important human health risk for those who are susceptible to infection or allergy [5, 6, 11].

Study of Bahkali and Parves revealed that the highest number of fungal colonies were found in the living room followed by bedrooms, and Aspergillus was the predominant genus in house-dusts which corresponds with the results of this study [1]. Su et al. and Sharma et al. noted that Aspergillus had the highest concentration in homes of asthmatic and nonasthmatic children in southern Taiwan and northern India, respectively [12, 13]. Ara et al. showed that the fungal flora in bedrooms was characterized by a high detection rate of xerophilic fungi, such as Aspergillus and Eurotium [2]. Cetinkaya et al. and Hedayati et al. reported that Aspergillus was the second most abundant genus isolated from asthmatic patients’ houses and healthy subjects, respectively [4, 10]. Gomez de Ana et al. in Spain exerted that the genus Aspergillus was isolated in approximately 70% (winter) and 89% (summer) of homes of patients allergic to fungi [14].

In contrast, Arabi-Mianroodi et al. isolated Aspergillus only from 8% nasal cavity of healthy individuals [15]. In the present study, the most common species isolated from all samples of healthy volunteers and patients was A. flavus, followed by A. niger and A. fumigatus. A. fumigatus was the predominant species isolated from nasal cavity of control group; whereas, in the patient group, A. flavus was the most abundant species. In both control and patient groups, A. flavus had the highest rate in the bedroom air, pillow and dust of the bed samples; whereas, A. niger was the most commonly isolated species from dust on the shelf.

Similar to our findings, Hedayati et al. in north of Iran reported that the most common species of Aspergillus was A. flavus both in the indoor and outdoor air of asthmatic patients’ houses [10]. In contrast, Sharma et al. in India

and Li et al. in Taiwan noted that A. flavus and A. niger were the predominant species in indoor and outdoor air of asthmatic and control children [13, 16]. Gomez de Ana et al. in Spain showed that A. niger was predominantly detected from the indoor air of the homes of patients allergic to fungi [14]. Sakai et al. in Japan reported that the major Aspergillus spp. was A. restrictus in indoor and outdoor air of dwellings [17].

Concerning the fungal isolation from nasal cavity, Kordbacheh et al. isolated A. flavus and A. fumigatus from the patients with nasal polyposis [18]. Likewise, Darwazeh et al. reported that the predominant species isolated from Saudi healthy subjects was A. flavus followed by A. niger and A. fumigates [19]. Sellart-Altisent et al. in Spain revealed that A. flavus was the most common species isolated from nasal cavity of allergic and healthy subjects [20].

Unlike the findings obtained from the present study, Woodcock et al. in the UK reported that A. fumigatus was the commonest species isolated from pillows and vacuum dust [21].

The studies performed in different countries provide variable results of total fungal concentration and distribution of fungal species because it basically depends on media and sampling method used, season of the year, geographical location, and living conditions as well as fungal growth substrates in different countries [22].

Several recent epidemiologic studies reported positive associations between home dampness and respiratory morbidity of the occupants. These studies also indicated that dampness and fungal problems are present in 20% to 50% of modern homes. Fungi are regarded as one of the causal factors in the relationship between home dampness and respiratory symptoms, and homes classified as damp tend to have higher levels of fungi than those not so classified. In addition, poorly maintained heating, ventilation, and air-conditioning (HVAC) systems have been recognized as sources of microorganisms, including fungi [23]. Moreover, most fungi, including Aspergillus genus, produce highly allergic proteins or glycoproteins that could cause hypersensitivity diseases in susceptible subjects. There is also evidence suggesting that sensitization and exposure to fungi will increase the chances of asthma attack and some fungi are also clearly associated with symptoms of asthma [12]. Aspergillus spp. has been known to be one of the most prevalent airborne fungi in indoor environment. Exposure to Aspergillus has been reported to cause several types of human health problems, primarily irritations, infections, allergies, and toxic effects, and it has been suggested that toxigenic Aspergillus are the cause of additional adverse health effects [5, 6, 11]. Several species of Aspergillus have been shown to be allergenic, including A. fumigatus, A. niger, A. flavus, A. restrictus, and A. oryzae. Over 20 allergens have been characterized in A. fumigatus, two from A. flavus (Asp fl 13 and Asp fl 18), and four from the closely related A. oryzae (Asp o 13, Asp o 21, Asp o lactase, and Asp o lipase) [24, 25]. Microbial volatile organic compounds (MVOC) are low-molecular-weight alcohols, aldehydes, ketones, aromatic compounds, amines, terpenes, chlorinated hydrocarbons, and sulfuric compounds that are produced by either primary or secondary metabolic pathways employing aerobic or anaerobic metabolism [10]. Aspergillus versicolor is a strong producer of these compounds. Some other species of Aspergillus including A. fumigatus, A. sydowii, A. flavus and A. niger are MVOC producers too [26]. These species are common Aspergillus species that are grown indoors. Some individuals, such as patients with allergic rhinitis, can sense and respond to lower concentrations of MVOC than others.

In addition, A. flavus, and A. fumigatus are so-called high-risk microorganisms and the confirmed presence of these species will require urgent risk management decisions to be made [12].

In conclusion, A. flavus was the most prevalent species of Aspergillus both healthy volunteers and patients. The presence of Aspergillus in homes does not necessarily imply a cause and effect relationship with illness, but we speculate that A. flavus may be a major source of aeroallergens along with A. niger and A. fumigatus; and should alert physicians and healthcare professionals to do more vigorous environmental testing.

Acknowledgements

References

  • 1.

    Bahkali AH, Parvez S. Fungal flora in house dust in Riyadh, Saudi Arabia. Mycoses. 1999;42(4):339-43. [PubMed ID: 10424107].

  • 2.

    Ara K, Aihara M, Ojima M. Survey of fungal contamination in ordinary houses in Japan. Allergol Int. 2004;53(4):369-77. https://doi.org/10.1111/j.1440-1592.2004.00356.x.

  • 3.

    Salvaggio J, Aukrust L. Postgraduate course presentation: Mold-induced asthma. J Allergy Clin Immunol. 1981;68(5):327-46. https://doi.org/10.1016/0091-6749(81)90131-7.

  • 4.

    Cetinkaya Z, Fidan F, Unlu M, Hasenekoglu I, Tetik L, Demirel R. Assessment of indoor air fungi in Western-Anatolia, Turkey. Asian Pac J Allergy Immunol. 2005;23(2-3):87-92. [PubMed ID: 16252837].

  • 5.

    Hedayati MT, Pasqualotto AC, Warn PA, Bowyer P, Denning DW. Aspergillus flavus: human pathogen, allergen and mycotoxin producer. Microbiology. 2007;153(Pt 6):1677-92. [PubMed ID: 17526826]. https://doi.org/10.1099/mic.0.2007/007641-0.

  • 6.

    McGinnis MR. Pathogenesis of indoor fungal diseases. Med Mycol. 2004;42(2):107-17. [PubMed ID: 15124863].

  • 7.

    Cosentino S,, Palmas F. Occurrence of fungal spores in the respiratory tract and homes of patients with positive skin test to fungi. Aerobiologia. 1996;12(1):155-60. https://doi.org/10.1007/BF02248143.

  • 8.

    Yazicioglu M, Asan A, Ones U, Vatansever U, Sen B, Ture M, et al. Indoor airborne fungal spores and home characteristics in asthmatic children from Edirne region of Turkey. Allergol Immunopathol (Madr). 2004;32(4):197-203. https://doi.org/10.1157/13064923.

  • 9.

    Mokhtari Amirmajdi M, Mokhtari Amirmajdi NA, Eftekharzadeh Mashhadi I, Jabari Azad F, Tavakol Afshari J, Shakeri MT. Alternaria in patients with allergic rhinitis. Iran J Allergy Asthma Immunol. 2011;10(3):221-6. [PubMed ID: 21891828].

  • 10.

    Hedayati MT, Mayahi S, Denning DW. A study on Aspergillus species in houses of asthmatic patients from Sari City, Iran and a brief review of the health effects of exposure to indoor Aspergillus. Environ Monit Assess. 2010;168(1-4):481-7. [PubMed ID: 19697147]. https://doi.org/10.1007/s10661-009-1128-x.

  • 11.

    Denning DW. Invasive aspergillosis. Clin Infect Dis. 1998;26(4):781-803. quiz 804-5. [PubMed ID: 9564455].

  • 12.

    Su HJ, Wu PC, Chen HL, Lee FC, Lin LL. Exposure assessment of indoor allergens, endotoxin, and airborne fungi for homes in southern Taiwan. Environ Res. 2001;85(2):135-44. [PubMed ID: 11161663]. https://doi.org/10.1006/enrs.2000.4113.

  • 13.

    Sharma R, Deval R, Priyadarshi V, Gaur SN, Singh VP, Singh AB. Indoor fungal concentration in the homes of allergic/asthmatic children in Delhi, India. Allergy Rhinol (Providence). 2011;2(1):21-32. [PubMed ID: 22852111]. https://doi.org/10.2500/ar.2011.2.0005.

  • 14.

    de Ana SG, Torres-Rodriguez JM, Ramirez EA, Garcia SM, Belmonte-Soler J. Seasonal distribution of Alternaria, Aspergillus, Cladosporium and Penicillium species isolated in homes of fungal allergic patients. J Investig Allergol Clin Immunol. 2006;16(6):357-63. [PubMed ID: 17153883].

  • 15.

    Arabi Mianroodi AA, Nasiri D, Khanjani N. The fungi flora of healthy nasal mucosa in Kerman, Iran. Iran J Otorhinolaryngol. 2011;23(63):21-8.

  • 16.

    Li CS, Hsu LY, Chou CC, Hsieh KH. Fungus allergens inside and outside the residences of atopic and control children. Arch Environ Health. 1995;50(1):38-43. [PubMed ID: 7717768]. https://doi.org/10.1080/00039896.1995.9955011.

  • 17.

    Sakai K, Tsubouchi H, Mitani K. [Airborne concentrations of fungal and indoor air pollutants in dwellings in Nagoya, Japan]. Nihon Koshu Eisei Zasshi. 2003;50(10):1017-29. [PubMed ID: 14639963].

  • 18.

    Kordbacheh P, Zaini F, Sabokbar A, Borghei H, Safara M. Fungi as causative agents of nasal polyps in Tehran, Iran. Iran J Public Health. 2006;35(1):53-7.

  • 19.

    Darwazeh AM, Al-Dosari A, Al-bagieh NH. Oral Candida and nasal Aspergillus flora in a group of Saudi healthy dentate subjects. Int Dent J. 2002;52(4):273-7. [PubMed ID: 12212815].

  • 20.

    Sellart-Altisent M, Torres-Rodriguez JM, Gomez de Ana S, Alvarado-Ramirez E. [Nasal fungal microbiota in allergic and healthy subjects] Spanish [Abstract]. Rev Iberoam Micol. 2007;24(2):125-30. [PubMed ID: 17604431].

  • 21.

    Woodcock AA, Steel N, Moore CB, Howard SJ, Custovic A, Denning DW. Fungal contamination of bedding. Allergy. 2006;61(1):140-2. [PubMed ID: 16364170]. https://doi.org/10.1111/j.1398-9995.2005.00941.x.

  • 22.

    Das S, Gupta-Bhattacharya S. Enumerating outdoor aeromycota in suburban West Bengal, India, with reference to respiratory allergy and meteorological factors. Ann Agric Environ Med. 2008;15(1):105-12. [PubMed ID: 18581987].

  • 23.

    Verhoeff AP, Burge HA. Health risk assessment of fungi in home environments. Ann Allergy Asthma Immunol. 1997;78(6):544-54. quiz 555-6. [PubMed ID: 9207717]. https://doi.org/10.1016/S1081-1206(10)63214-0.

  • 24.

    Mari A, Riccioli D. The allergome web site-a database of allergenic molecules. Aim, structure, and data of a web-based resource. J Allergy Clin Immunol Pract. 2004;113(2):S301. https://doi.org/10.1016/j.jaci.2004.01.573.

  • 25.

    Itabashi T, Hosoe T, Toyasaki N, Imai T, Adachi M, Kawai K. [Allergen activity of xerophilic fungus, Aspergillus restrictus]. Arerugi. 2007;56(2):101-8. [PubMed ID: 17347596].

  • 26.

    Gao P, Korley F, Martin J, Chen BT. Determination of unique microbial volatile organic compounds produced by five Aspergillus species commonly found in problem buildings. AIHA J (Fairfax, Va). 2002;63(2):135-40. [PubMed ID: 11975648].