Research article Topical Sections

Assessment of occupational exposure to azole resistant fungi in 10 Portuguese bakeries

  • Received: 02 October 2017 Accepted: 05 December 2017 Published: 14 December 2017
  • Occupational exposure to bioaerosols resulting from handling of flour dust and raw materials in bakeries is associated with health problems. The emergence of azole-resistant fungal species in the environment is thought to be related with the use of azole fungicides in cereal crops and prevention of postharvest spoilage. As raw materials used in bakeries are commonly exposed to azoles, we investigated the mycobiota and azole-resistant fungi prevalence in this occupational environment. Ten Portuguese bakeries were assessed through electrostatic dust cloth (EDC, n = 27), settled dust (n = 7), and raw material (n = 26) samples. Samples were inoculated in malt extract agar (2%) (MEA) with chloramphenicol (0.05 g/L) and in dichloran glycerol (DG18), and onto Saboraud screening media supplemented with 4 mg/L itraconazole, 1 mg/L voriconazole, or 0.5 mg/L posaconazole, and incubated for 3–5 days at 27 °C. Except for one out of the ten analyzed bakeries, Cladosporium sp., Penicillium sp., and Aspergillus sp. were the most prevalent fungi identified. Aspergillus sp. and Mucorales order were identified in raw materials with both media, whereas Penicillium sp. was identified in DG18 only. Azole-resistant species were identified in the environment (EDC) and, to a lower extent, in raw materials, including Aspergillus sp. and Mucorales. The presence of azole-resistant fungal species in bakeries represents an occupational risk for workers. This study proposes complementary sampling methods for the evaluation of occupational exposure to mycobiota, and highlights the importance of studying the prevalence of azole-resistant strains in specific occupational environments.

    Citation: Liliana Aranha Caetano, Tiago Faria, Ana Crespo Batista, Susana Viegas, Carla Viegas. Assessment of occupational exposure to azole resistant fungi in 10 Portuguese bakeries[J]. AIMS Microbiology, 2017, 3(4): 960-975. doi: 10.3934/microbiol.2017.4.960

    Related Papers:

  • Occupational exposure to bioaerosols resulting from handling of flour dust and raw materials in bakeries is associated with health problems. The emergence of azole-resistant fungal species in the environment is thought to be related with the use of azole fungicides in cereal crops and prevention of postharvest spoilage. As raw materials used in bakeries are commonly exposed to azoles, we investigated the mycobiota and azole-resistant fungi prevalence in this occupational environment. Ten Portuguese bakeries were assessed through electrostatic dust cloth (EDC, n = 27), settled dust (n = 7), and raw material (n = 26) samples. Samples were inoculated in malt extract agar (2%) (MEA) with chloramphenicol (0.05 g/L) and in dichloran glycerol (DG18), and onto Saboraud screening media supplemented with 4 mg/L itraconazole, 1 mg/L voriconazole, or 0.5 mg/L posaconazole, and incubated for 3–5 days at 27 °C. Except for one out of the ten analyzed bakeries, Cladosporium sp., Penicillium sp., and Aspergillus sp. were the most prevalent fungi identified. Aspergillus sp. and Mucorales order were identified in raw materials with both media, whereas Penicillium sp. was identified in DG18 only. Azole-resistant species were identified in the environment (EDC) and, to a lower extent, in raw materials, including Aspergillus sp. and Mucorales. The presence of azole-resistant fungal species in bakeries represents an occupational risk for workers. This study proposes complementary sampling methods for the evaluation of occupational exposure to mycobiota, and highlights the importance of studying the prevalence of azole-resistant strains in specific occupational environments.


    加载中
    [1] Blancocarmona JG, Picón SJ, Sotillos MG (1991) Occupational asthma in bakeries caused by sensitivity to alpha-amylase. Allergy 46: 274–276. doi: 10.1111/j.1398-9995.1991.tb00585.x
    [2] Burdorf A, Lillienberg L, Brisman J (1994) Characterization of exposure to inhalable flour dust in Swedish bakeries. Ann Occup Hyg 38: 67–78.
    [3] Lilienberg L, Brisman J (1996) Peak exposure concentrations of dust in bakeries, In: Proceeding of the 2nd International Symposium on Modern Principles of Air Monitoring, Feb 5–8, 1996, Salen, Sweden: 47.
    [4] Sander I, Flagge A, Mergret R, et al. (2001) Identification of wheat flout allergens by means of 2-dimensional immunoblotting. Allergy Clin Immunol 107: 907–913. doi: 10.1067/mai.2001.113761
    [5] Bush RK, Portnoy JM, Saxon A, et al. (2006) The medical effects of mold exposure. J Allergy Clin Immunol 117: 326–333. doi: 10.1016/j.jaci.2005.12.001
    [6] Salcedo G, Quirce S, Diaz-Perales A (2011) Wheat allergens associated with baker's asthma. J Invest Allergy Clin 21: 81–92.
    [7] Cullinan P, Cook A, Nieuwenhuijsen MJ, et al. (2001) Allergen and dust exposure as determinants of work-related symptoms and sensitization in a cohort of flour-exposed workers; a case-control analysis. Ann Occup Hyg 45: 97–103. doi: 10.1016/S0003-4878(00)00028-4
    [8] Brandl H (2011) Bioaerosols in indoor environment-A review with special reference to residential and occupational locations. Open Environ Biol Monit J 4: 83–96. doi: 10.2174/1875040001104010083
    [9] Sahlberg B, Gunnbjörnsdottir M, Soon A, et al. (2013) Airborne molds and bacteria, microbial volatile organic compounds (MVOC), plasticizers and formaldehyde in dwellings in three North European cities in relation to sick building syndrome (SBS). Sci Total Environ 444: 433–440. doi: 10.1016/j.scitotenv.2012.10.114
    [10] Viegas C, Carolino E, Sabino R, et al. (2013) Fungal contamination in swine: A potential occupational health threat. J Toxicol Env Heal A 76: 272–280. doi: 10.1080/15287394.2013.757205
    [11] Viegas C, Faria T, dos Santos M, et al. (2015) Fungal burden in waste industry: an occupational risk to be solved. Environ Monit Assess 187: 199. doi: 10.1007/s10661-015-4412-y
    [12] Viegas S, Veiga L, Almeida A, et al. (2015) Occupational exposure to Aflatoxin B1 in a Portuguese poultry slaughterhouse. Ann Occup Hyg 60: 176–183.
    [13] Viegas C, Faria T, Meneses M, et al. (2016) Analysis of surfaces for characterization of fungal burden-Does it matter? Int J Occup Med Environ Health 29: 623–632. doi: 10.13075/ijomeh.1896.00562
    [14] Viegas S, Caetano L, Korkalainen M, et al. (2017) Cytotoxic and inflammatory potential of air samples from occupational settings with exposure to organic dust. Toxics 5: 8. doi: 10.3390/toxics5010008
    [15] Viegas S, Faria T, Viegas C (2017) Bakers exposure to flour dust-a exploratory study in a Portuguese Bakery. International Symposium on Occupational Safety and Hygiene SHO 2017.
    [16] Stobnicka A, Górny RL (2015) Exposure to flour dust in the occupational environment. Int J Occup Saf Ergon 21: 241–249. doi: 10.1080/10803548.2015.1081764
    [17] Tsapko V, Chudnovets A, Sterenbogen M, et al. (2011) Exposure to bioaerosols in the selected agricultural facilities of the Ukraine and Poland-A review. Ann Agr Env Med 18: 19–27.
    [18] Tiikkainen U, Louhelainen K, Nordman H (1996) The Nordic expert group for criteria documentation of health risks from chemicals 120. Flour Dust. Arbete Hälsa 27.
    [19] Mohammadien HA, Hussein MT, El-Sokkary RT (2013) Effects of exposure to flour dust on respiratory symptoms and pulmonary function of mill workers. Egypt J Chest Dis Tuberc 62: 745–753. doi: 10.1016/j.ejcdt.2013.09.007
    [20] Gisi U (2013) Assessment of selection and resistance risk for DMI fungicides in Aspergillus fumigatus in agriculture and medicine: a critical review. Pest Manag Sci 70: 352–364.
    [21] Vermeulen E, Maertens J, De Bel A, et al. (2015) Nationwide surveillance of azole resistance in Aspergillus diseases. Antimicrob Agents Ch 59: 4569–4576. doi: 10.1128/AAC.00233-15
    [22] Meletiadis J, Roilides E (2013) Rare invasive fungal infections: Epidemiology, diagnosis and management. Curr Fungal Infect Rep 7: 351–360. doi: 10.1007/s12281-013-0155-9
    [23] Walsh TJ, Anaissie EJ, Denning DW, et al. (2008) Treatment of aspergillosis: Clinical practice guidelines of the infectious diseases society of America. Clin Infect Dis 46: 327–360. doi: 10.1086/525258
    [24] Kontoyiannis DP (2012) Invasive mycoses: Strategies for effective management. Am J Med 125: S25–S38. doi: 10.1016/j.amjmed.2011.10.009
    [25] Howard SJ, Webster I, Moore CB, et al. (2006) Multi-azole resistance in Aspergillus fumigatus. Int J Antimicrob Agents 28: 450–453. doi: 10.1016/j.ijantimicag.2006.08.017
    [26] Lelièvre L, Groh M, Angebault C, et al. (2013) Azole resistant Aspergillus fumigatus: An emerging problem. Med Maladies Infect 43: 139–145. doi: 10.1016/j.medmal.2013.02.010
    [27] Abdolrasouli A, Rhodes J, Beale M, et al (2015) Genomic context of Azole-resistance mutations in Aspergillus fumigatus using whole-genome sequencing. Mbio 6: 1–11. doi: 10.3391/mbi.2015.6.1.01
    [28] Verweij PE, Chowdhary A, Melchers WJG, et al. (2016) Azole resistance in Aspergillus fumigatus: Can we retain the clinical use of mold-active antifungal Azoles? Clin Infect Dis 62: 362–368. doi: 10.1093/cid/civ885
    [29] Zhang J, Snelders E, Zwaan BJ, et al. (2017) A novel environmental Azole resistance mutation in Aspergillus fumigatus and a possible role of sexual reproduction in its emergence. Mbio 8: e00791-17.
    [30] Verweij PE, Snelders E, Kema GH, et al. (2009) Azole resistance in Aspergillus fumigatus: a side-effect of environmental fungicide use? Lancet Infect Dis 9: 789–795. doi: 10.1016/S1473-3099(09)70265-8
    [31] Howard SJ, Cerar D, Anderson MJ, et al. (2009) Frequency and evolution of Azole resistance in Aspergillus fumigatus associated with treatment failure. Emerg Infect Dis 15: 1068. doi: 10.3201/eid1507.090043
    [32] Mortensen KL, Mellado E, Lass-Florl C, et al. (2010) Environmental study of azole-resistant Aspergillus fumigatus and other aspergilli in Austria, Denmark, and Spain. Antimicrob Agents Ch 54: 4545–4549. doi: 10.1128/AAC.00692-10
    [33] Arendrup MC (2014) Update on antifungal resistance in Aspergillus and Candida. Clin Microbiol Infect Suppl 6: 42–48.
    [34] Kontoyiannis DP, Lionakis MS, Lewis RE, et al. (2005) Zygomycosis in a tertiary-care cancer center in the era of Aspergillus-active antifungal therapy: a case-control observational study of 27 recent cases. J Infect Dis 191: 1350–1360. doi: 10.1086/428780
    [35] Bitar D, Van Cauteren D, Lanternier F, et al. (2009) Increasing incidence of zygomycosis (mucormycosis), France, 1997–2006. Emerg Infect Dis 15: 1395–1401. doi: 10.3201/eid1509.090334
    [36] Auberger J, Lass-Florl C, Aigner M, et al. (2012) Invasive fungal breakthrough infections, fungal colonization and emergence of resistant strains in high-risk patients receiving antifungal prophylaxis with posaconazole: real-life data from a single-centre institutional retrospective observational study. J Antimicrob Chemoth 67: 2268–2273. doi: 10.1093/jac/dks189
    [37] Odds FC, Brown AJ, Gow NA (2003) Antifungal agents: mechanisms of action. Trends Microbiol 11: 272–279. doi: 10.1016/S0966-842X(03)00117-3
    [38] Springer J, Goldenberger D, Schmidt F, et al. (2016) Development and application of two independent real-time PCR assays to detect clinically relevant Mucorales species. J Med Microbiol 65: 227–234. doi: 10.1099/jmm.0.000218
    [39] Perlin DS, Rautemaa-Richardson R, Alastruey-Izquierdo A (2017) The global problem of antifungal resistance: Prevalence, mechanisms, and management. Lancet Infect Dis.
    [40] Madsen AM, Matthiesen CB, Frederiksen MW, et al. (2012) Sampling, extraction and measurement of bacteria, endotoxin, fungi and inflammatory potential of settling indoor dust. J Environ Monitor 14: 3230–3239. doi: 10.1039/c2em30699a
    [41] Viegas C, Faria T, Caetano LA, et al. (2017) Fungal contamination in green coffee beans samples: a public health concern. J Toxicol Env Health A 80: 719–728. doi: 10.1080/15287394.2017.1286927
    [42] ISO (2008) Microbiology of food and animal feeding stuffs: Horizontal method for the enumeration of yeasts and moulds. Part 1: Colony count technique in products with water activity greater than 0.95.
    [43] ISO (2008) Microbiology of food and animal feeding stuffs: Horizontal method for the enumeration of yeasts and moulds. Part 2: Colony count technique in products with water activity less than or equal to 0.95.
    [44] Cozen W, Avol E, Diaz-Sanchez D, et al. (2008) Use of an electrostatic dust cloth for self-administered home allergen collection. Twin Res Hum Genet 11: 150–155. doi: 10.1375/twin.11.2.150
    [45] Viegas C, Ramalho I, Alves M, et al. (2017) Electrostatic dust cloth: A new sampling method for occupational exposure to bioaerosols. In: Arezes P, editor, International Symposium on Occupational Safety and Hygiene, Guimarães: SPOSHO, 39–41.
    [46] Kilburg-Basnyat B, Metwali N, Thorne PS (2016) Performance of electrostatic dust collectors (EDCs) for endotoxin assessment in homes: effect of mailing, placement, heating and electrostatic charge. J Occup Environ Hyg 13: 85–93. doi: 10.1080/15459624.2015.1078468
    [47] Bergwall C, Stehn B (2002) Comparison of selective mycological agar media for the isolation and enumeration of xerophilic moulds and osmotolerant yeasts in granulated white sugar. Zuckerindustrie 127: 259–264.
    [48] The European Committee on Antimicrobial Susceptibility Testing, Breakpoint tables for interpretation of MICs and zone diameters, version 7.1, 2017. Available from: http://www.eucast.org.
    [49] Hoog C, Guarro J, Gené G, et al. (2000) Atlas of clinical fungi, Centraalbureau voor Schimmelcultures, Utrecht, the Netherlands.
    [50] Degois J, Clerc F, Simon X, et al. (2017) First metagenomic survey of the microbial diversity in bioaerosols emitted in waste sorting plants. Ann Work Expo Health 61: 1076–1086. doi: 10.1093/annweh/wxx075
    [51] Lanternier F, Dannaoui E, Morizot G, et al. (2012) A global analysis of mucormycosis in France: the RetroZygo Study (2005–2007). Clin Infect Dis 54: S35–S43. doi: 10.1093/cid/cir880
    [52] Springer J, Lackner M, Ensinger C, et al. (2016) Clinical evaluation of Mucorales-specific real-time PCR assay in tissue and serum samples. J Med Microbiol 65: 1414–1421. doi: 10.1099/jmm.0.000375
    [53] Cuenca-Estrella M, Gomez-Lopez A, Mellado E, et al. (2006) Head-to-head comparison of the activities of currently available antifungal agents against 3,378 Spanish clinical isolates of yeasts and filamentous fungi. Antimicrob Agents Ch 50: 917–921. doi: 10.1128/AAC.50.3.917-921.2006
    [54] Najafzadeh MJ, Sutton DA, Keisari MS, et al. (2014) In vitro activities of eight antifungal drugs against 104 environmental and clinical isolates of Aureobasidium pullulans. Antimicrob Agents Ch 58: 5629–5631. doi: 10.1128/AAC.03095-14
    [55] Alhanout K, Brunel JM, Ranque S, et al. (2010) In vitro antifungal activity of aminosterols against moulds isolated from cystic fibrosis patients. J Antimicrob Chemoth 65: 1307–1309. doi: 10.1093/jac/dkq089
    [56] Pound MW, Townsend ML, Dimondi V, et al. (2011) Overview of treatment options for invasive fungal infections. Med Mycol 49: 561–580.
    [57] Despot DJ, Kocsubé S, Bencsik O, et al. (2017) New sterigmatocystin-producing species of Aspergillus section Versicolores from indoor air in Croatia. Mycol Prog 16: 63–72. doi: 10.1007/s11557-016-1250-4
    [58] EFSA Panel on Contaminants in the Food Chain (CONTAM) (2013) Scientific Opinion on the risk for public and animal health related to the presence of sterigmatocystin in food and feed. EFSA J 11: 3254
    [59] Ali N, Blaszkewicz M, Manirujjaman M, et al. (2014) Biomonitoring of ochratoxin A in blood plasma and exposure assessment of adult students in Bangladesh. Mol Nutr Food Res 58: 2219–2225. doi: 10.1002/mnfr.201400403
    [60] Kano R, Kohata E, Tateishi A, et al. (2014) Does farm fungicide use induce azole resistance in Aspergillus fumigatus? Med Mycol 53: 174–177.
    [61] Jeanvoine A, Rocchi S, Reboux G, et al. (2017) Azole-resistant Aspergillus fumigatus in sawmills of Eastern France. J Appl Microbiol 123: 172–184. doi: 10.1111/jam.13488
    [62] Snelders E, Huis In't Veld RA, Rijs AJ, et al. (2009) Possible environmental origin of resistance of Aspergillus fumigatus to medical triazoles. Appl Environ Microb 75: 4053–4057. doi: 10.1128/AEM.00231-09
    [63] Denning DW, Bowyer P (2013) Voriconazole resistance in Aspergillus fumigatus: Should we be concerned? Clin Infect Dis 57: 521–523. doi: 10.1093/cid/cit321
    [64] Eduard W, Halstensen A (2009) Quantitative exposure assessment of organic dust. SJWEH Supplements 7: 30–35.
    [65] Viegas C, Malta-Vacas J, Sabino R (2012) Molecular biology versus conventional methods-complementary methodologies to understand occupational exposure to fungi. International Symposium on Occupational Safety and Hygiene SHO 2012.
    [66] Viegas C, Malta-Vacas J, Sabino R, et al. (2014) Accessing indoor fungal contamination using conventional and molecular methods in Portuguese poultries. Environ Monit Assess 186: 1951–1959. doi: 10.1007/s10661-013-3509-4
    [67] Viegas C, Faria T, Caetano LA, et al. (2017) Aspergillus spp. prevalence in different Portuguese occupational environments: what is the real scenario in high load settings? J Occup Environ Hyg 14: 771–785.
    [68] Lamoth F (2016) Aspergillus fumigatus–Related species in clinical practice. Front Microbiol 7: 683.
    [69] Viegas C, Faria T, dos Santos M, et al. (2015) Fungal burden in waste industry: an occupational risk to be solved. Environ Monit Assess 187: 199. doi: 10.1007/s10661-015-4412-y
    [70] Garcia-Solache MA, Casadevall A (2010) Global warming will bring new fungal diseases for mammals. Mbio 1: e00061-10.
    [71] Vermeulen E, Maertens J, De Bel A, et al. (2015) Nationwide surveillance of azole resistance in Aspergillus diseases. Antimicrob Agents Ch 59: 4569–4576. doi: 10.1128/AAC.00233-15
    [72] Fairlamb AH, Gow NA, Matthews KR, et al. (2017) Stop neglecting fungi. Nat Microbiol 2: 17120. doi: 10.1038/nmicrobiol.2017.120
  • Reader Comments
  • © 2017 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(3571) PDF downloads(851) Cited by(16)

Article outline

Figures and Tables

Figures(2)  /  Tables(6)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog