Polish Norm PN-89/Z-04111/02 and PN-89/Z-04111/03 (
\\n\\n
More than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\\n\\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\\n\\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\\n\\nAdditionally, each book published by IntechOpen contains original content and research findings.
\\n\\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Simba Information has released its Open Access Book Publishing 2020 - 2024 report and has again identified IntechOpen as the world’s largest Open Access book publisher by title count.
\n\nSimba Information is a leading provider for market intelligence and forecasts in the media and publishing industry. The report, published every year, provides an overview and financial outlook for the global professional e-book publishing market.
\n\nIntechOpen, De Gruyter, and Frontiers are the largest OA book publishers by title count, with IntechOpen coming in at first place with 5,101 OA books published, a good 1,782 titles ahead of the nearest competitor.
\n\nSince the first Open Access Book Publishing report published in 2016, IntechOpen has held the top stop each year.
\n\n\n\nMore than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\n\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\n\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\n\nAdditionally, each book published by IntechOpen contains original content and research findings.
\n\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\n\n\n\n
\n'}],latestNews:[{slug:"stanford-university-identifies-top-2-scientists-over-1-000-are-intechopen-authors-and-editors-20210122",title:"Stanford University Identifies Top 2% Scientists, Over 1,000 are IntechOpen Authors and Editors"},{slug:"intechopen-authors-included-in-the-highly-cited-researchers-list-for-2020-20210121",title:"IntechOpen Authors Included in the Highly Cited Researchers List for 2020"},{slug:"intechopen-maintains-position-as-the-world-s-largest-oa-book-publisher-20201218",title:"IntechOpen Maintains Position as the World’s Largest OA Book Publisher"},{slug:"all-intechopen-books-available-on-perlego-20201215",title:"All IntechOpen Books Available on Perlego"},{slug:"oiv-awards-recognizes-intechopen-s-editors-20201127",title:"OIV Awards Recognizes IntechOpen's Editors"},{slug:"intechopen-joins-crossref-s-initiative-for-open-abstracts-i4oa-to-boost-the-discovery-of-research-20201005",title:"IntechOpen joins Crossref's Initiative for Open Abstracts (I4OA) to Boost the Discovery of Research"},{slug:"intechopen-hits-milestone-5-000-open-access-books-published-20200908",title:"IntechOpen hits milestone: 5,000 Open Access books published!"},{slug:"intechopen-books-hosted-on-the-mathworks-book-program-20200819",title:"IntechOpen Books Hosted on the MathWorks Book Program"}]},book:{item:{type:"book",id:"450",leadTitle:null,fullTitle:"Biofuel's Engineering Process Technology",title:"Biofuel's Engineering Process Technology",subtitle:null,reviewType:"peer-reviewed",abstract:"This book aspires to be a comprehensive summary of current biofuels issues and thereby contribute to the understanding of this important topic. Readers will find themes including biofuels development efforts, their implications for the food industry, current and future biofuels crops, the successful Brazilian ethanol program, insights of the first, second, third and fourth biofuel generations, advanced biofuel production techniques, related waste treatment, emissions and environmental impacts, water consumption, produced allergens and toxins. 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Intensive poultry production, implying large densities of animals in small areas, is a significant source of air pollution which may constitute a considerable health hazard to the birds, farmers and those living in the proximity of the farm (Lonc & Plewa, 2009). On the other hand, the spread of bioaerosols on the outside of animal housing may result in local or even more extensive environmental pollution (Bakutis et al., 2004).
\n\t\t\tUnder commercial production the airborne particles will contain a mixture of biological material from a range of sources. The chickens produce large amounts of dust as a result of epithelial desquamation, as well as from feed, manure, faeces and litter (Matković et al., 2009). This dust consists of a variety of airborne particles of biological origin, i.e. bacteria, fungi, endotoxins (lipopolysaccharide, LPS) of Gram-negative bacteria, 1.3-beta-glucan of fungi, fungal spores and mycelium fragments. Hence, a more descriptive term for these airborne particles is bioaerosol in which the microorganisms can occur either as liquid droplets or as dry particles [Dutkiewicz, 1987; Matković et al., 2009; Nevalainen, 2007]. In specific conditions, bioaerosols may show pathogenic, toxic or allergy-causing effects. The particles in a bioaerosol are generally 0.3 to 100 µm in diameter; however, the respirable size fraction of 1 to 10 µm is of primary concern. Bioaerosols, ranging in size from 1.0 to 5.0 µm, generally remain in the air, whereas larger particles are deposited on surfaces (Srikanth et al., 2008).
\n\t\t\tBioaerosol may contain representatives of Gram-positive bacteria: Corynebacterium, Staphyloccocus, Streptococcus, Micrococcus, Pantoea and Sarcina (Siemiński, 2001). Their presence in large numbers may present a significant immunological challenge to the human respiratory system. In dust are suspended also endotoxins (lipopolysaccharide complex - LPS) associated with the outer membrane of Gram-negative pathogens, such as Escherichia coli, Salmonella, Shigella, Pseudomonas, Neisseria and Haemophilus influenzae. LPS is composed of two major parts, the hydrophobic lipid A and the hydrophilic polysaccharide part (commonly called the "O" region). Most biological effects of LPS are due to the lipid A part, however O-region plays an important role in effective colonisation of host tissues. Inhalation of organic dust contaminated by endotoxins may cause chronic bronchitis and inflammatory reaction in the lungs (Bakutis et al., 2004, Schierl et al., 2007, Pomorska et al., 2009).
\n\t\t\tAs with bacteria, the fungi present in the poultry dust bioaerosols may be derived from soil, dust feed and litter, but to a lesser extent from the birds themselves. Fungi are ubiquitous in all atmospheres. In general, both outdoor and indoor atmospheres are dominated by representatives of the genera Cladosporium, Penicillium, Aspergillus, Alternaria and by yeasts and Mycelia sterilia.Cladosporium is nearly always the dominant fungus in outdoor as well as indoor atmospheres. The abundance of the other fungi varies with the season and place. In relation to outdoor environments, indoor atmospheres typically display lower diversity (Araujo & Cabral, 2010). Long-term or repeated exposure to high concentrations of airborne fungal spores is recognised as contributing to the decline in lung function and allergic diseases such as asthma and allergic alveolitis known as farmer’s lung disease (Crook et al., 2008).
\n\t\t\tLiterature data usually pertain to the air biopollutant concentration inside the poultry houses. Much less is known about the relationships between the indoor and outdoor biological pollution, as well as about the spreading of indoor bioaerosols in the surroundings of the farms.
\n\t\t\tThe aim of the study was to assess the influence of microbiological air contamination in the intensive poultry breeding, both inside and outside farms. The comparative quantity and quality analysis concerns bacteria as well as fungi isolated from the air samples taken during two seasons.
\n\t\tSeasonal sampling was conducted in the summer of 2009 and spring of 2010 in two (I and II) poultry houses on family farms located near Wrocław in Lower Silesia, Poland (Fig. 1.)
\n\t\t\tBoth farms were accommodated to 18 000 and 23 000 broilers, with the density of 16-17 chicken per square meter. The broilers were kept on the rye straw deep litter in buildings equipped with mechanical ventilation (inlet and outlet ventilators), heating with a central thermogen and artificial lighting with regularly distributed bulbs.
\n\t\t\tAir samples were taken using a MAS-100 air sampler (Merck KgaA, Darmstadt, Germany) which is representative of the new generation impactor samplers and is frequently used for indoor and outdoor sampling. These instruments are based on the principles described by Andersen and aspirate air through a perforated plate, which results in impaction of particles from an airstream onto the surface of agar medium. The speed of air flow through the sampler was about 11 m/s, air volumes were 5-200 litres (depending on the expected contamination level) and the sampling rate was 100 l/min. Indoor and outdoor samples were collected in the poultry biozone during the fattening period. The biopollutants were determined on the basis of airborne bacteria and fungi. The samples for each group of bacteria and fungi were taken at the central point of poultry houses 1.3 m from the ground level. The emission level outside the farming objects was determined similarly, i.e. 1.3 m with sampling points situated 10 m, 50 m and 100 m away from the farming buildings. At the same time both humidity and temperature were measured with a termohigrometer (Label).
\n\t\t\tMicrobiological studies of the air samples were used to determine the number of mesophilic bacteria, Enterobacteriaceae representatives, mannitol+ staphylococci,\n\t\t\t\tSalmonella sp. and mould fungi. The mesophilic bacteria were isolated with the use of TSA agar (BioMérieux).
\n\t\t\t\n\t\t\t\tEnterobacteriaceae families were determined with the use of VRB medium (BioMérieux). The estimation of Salmonella sp. was done on SS agar (BioMérieux). Mannitol salt agar
\n\t\t\tPoultry houses I and II; the sampling sites outside the poultry house at the distance of 10 m, 50 m and 100 m from the farming object respectively, as well as at the center of building.
(BioMérieux) plates were inoculated for culturing and counting staphylococci. Mould fungi were determined with the use of Sabouraud (Merck) medium. Colonies were counted after 48 h of incubation at 370C for bacteria and after 5 days at 260C for moulds and subsequently the colony-forming units (CFU) were determined. Quantitative results were expressed in CFU/m3, i.e. colony forming units in 1 m3 of the examined air and the total microbial count was corrected using the conversion formula devised by Feller:
\n\t\t\twhere:
\n\t\t\tN = 400 (number of holes in perforated lid of the sampler)
\n\t\t\tr - number of CFU counted on Petri dish
\n\t\t\tPr - statistically corrected total count of bacteria/moulds in tested air volume
\n\t\t\tBacterial species were identified on the basis of gram staining, microscopic morphology, oxidase and coagulase activity, catalase test results and metabolic properties according to standard procedures described in Bergey’s Manual of Determinative Bacteriology (2001). The following commercial systems were used: API 20E (BioMérieux, France) for enteric gram-negative organisms; API 20 NE (BioMérieux) for fastidious and nonfermenting gram-negative organisms; API Staph (BioMérieux) for gram-positive staphylococci, API 20C AUX (BioMérieux) for identification of yeasts, Slidex - Strepto Kit (BioMérieux) for the identification of Lancefield A,B,C,D,F et G group antigens of streptococci and Slidex Staph Plus (BioMérieux) to detect clumping factor, protein A and group-specific antigen bound to the S. aureus. Moulds colonies were identified on the basis of colour, texture, topography of the culture surface, smell of the colony, colour of the reverse of the colony and the presence of the diffuse pigment. Microscopic features of the fungal colonies, i.e. the presence of macroconidia and microconidia, their shape and appearance were identified later. Fungal species of the genera Aspergillus and Penicilium were identified with the use of the keys by Raper and Fennell as well as Raper et. al., while the Fusarium species were identified using the key by Kwaśna (1991). Other species were identified based on the “Atlas of Clinical Fungi”(2010).
\n\t\tThe studies were carried out in the summer of 2009 and in the spring of 2010, when the temperature of atmospheric air ranged between 15.20C and + 24.50C; the inside temperature in the poultry houses varied from 220C to 270C. Indoor relative air humidity was about 70-85 %, outdoor ca. 38-82%.
\n\t\t\tFor both poultry houses, the indoor concentration of bacteria and moulds were always higher compared with the outdoor concentration at distance 10 m, 50 m and 100 m from the poultry houses. The number of microorganisms (as CFU/m3) in the atmospheric air of both poultry houses ranged between 4 x 101– 7.2 x 103 for mesophilic bacteria, 0– 1.3 x 104 for staphylococci, 0 - 7 x 101 for coli group bacteria, and 2 x 101 – 1.3 x 104 for fungi (Fig. 2-5). Salmonella sp. were not found. On the other hand, the number of microorganisms inside both poultry houses was higher than in the surrounding area and ranged between 1.3 x 105– 5.2 x 105 for mesophilic bacteria, 1.4 x 105 – 2.6 x 105 for staphylococci, 2.0 x 102- 1.5 x 104 for coli group bacteria and 3.6 x 104 – 1,1 x 105 for fungi. Salmonella sp. similar like outdoor were not found.
\n\t\t\tOutside poultry house I mesophilic bacteria were the most numerous organisms in the spring and summer and formed about 55% of the local microbial community. Less numerous staphylococci and moulds constituted about 17% and 27.5%, respectively. The concentration of Enterobacteriaceae was fractional (0.5%). In contrast, outside poultry house II the most numerous group of bacteria were staphylococci (62%). Mesophilic bacteria and moulds constituted about 25% and 13% of the microbial community. However, air inside both poultry houses was characterized by a relatively small number of Enterobacteriaceae. On the other hand, mesophilic bacteria were dominant and formed about 44% (poultry house I) and 56.5% (poultry house II) of the local microbial community, whereas staphylococci constituted 40% and 27% and moulds 16% and 7% for poultry house I and II. Salmonella sp. was not detected in neither poultry houses.
\n\t\t\tNumber of microorganisms in the poultry house I in summer.
Number of microorganisms in the poultry house I in spring.
Number of microorganisms in the poultry house II in summer.
Number of microorganisms in the poultry house II in spring.
The level of outdoor air contamination was evaluated in the accordance with the Polish Norm (Table 1). Contaminations by mesophilic bacteria and moulds in areas surrounding poultry house I in the summer was the highest in sampling point I 10. In relation to the Polish Norms this site was heavily polluted. On the other hand, the number of staphylococci at all sampling sites in both poultry houses (except sampling points I 50 and II 100 in the spring) indicated a high contamination. In contrast, the air in the surrounding areas could be classified as medium-contaminated at all sites around the poultry houses II in the summer and in sampling point II 50 in the spring, with mesophilic bacteria. The evaluation based on the Polish Norm revealed that none of the researched measuring sites around the poultry house II was significantly contaminated by fungal microflora.
\n\t\t\t\n\t\t\t\t\t\t\tPolish Norm\n\t\t\t\t\t\t | \n\t\t\t\t\t\tMesophilic bacteria | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tStaphylococi\n\t\t\t\t\t\t | \n\t\t\t\t\t\tFungi | \n\t\t\t\t\t
not pollution * | \n\t\t\t\t\t\t< 1x103\n\t\t\t\t\t\t | \n\t\t\t\t\t\t0 | \n\t\t\t\t\t\t3x103-5x103\n\t\t\t\t\t\t | \n\t\t\t\t\t
medium pollution ** | \n\t\t\t\t\t\t1x103- 3x103\n\t\t\t\t\t\t | \n\t\t\t\t\t\t<25 | \n\t\t\t\t\t\t5x103-1x104\n\t\t\t\t\t\t | \n\t\t\t\t\t
heavily pollution *** | \n\t\t\t\t\t\t"/3x103\n\t\t\t\t\t\t | \n\t\t\t\t\t\t"/25 | \n\t\t\t\t\t\t"/ 1x104\n\t\t\t\t\t\t | \n\t\t\t\t\t
Polish Norm PN-89/Z-04111/02 and PN-89/Z-04111/03 (
Fifteen species of bacteria detected in the indoor air represented 10 genera Staphylococcus (S. aureus, S. xylosus, S. saprophitycus), Micrococcus (M. sedentarius, M. luteus), Enterococcus, Streptococcus (S. mitis), Corynebacterium (C. xerosis), Pseudomonas (P. aeruginosa, P. fluorescens), Citrobacter (C. farmerii), Escherichia (E. coli), Enterobacter (E. sakazakii, E. agglomerans) and Proteus (P. mirabilis) –\n\t\t\t\tTable. 2. Quality outdoor set consisted of 19 species representing 10 bacteria genera: Staphylococcus (S. sciuri, S. epidermidis, S. cohnii subsp., S. lentus,S. xylosus), Micrococcus (M. lylae, M. halobius, M. luteus), Streptococcus (S. mitis), Bacillus ( B. mycoides, Bacillus sp.), Pseudomonas (P. aeruginosa, P. chlororaphis), Xantomonas (X. maltophila), Shigella (S. boydii), Providencia sp., Citrobacter (C. farmeri), Enterobacter (E. agglomerans) and Proteus (P. mirabilis). For the most part, the identified bacterial species were nonpathogenic or potentially pathogenic species, with the exception of P. aeruginosa, S. aureus, Shigella sp., E. coli, P. mirabilis which are regarded as primarily pathogenic.
\n\t\t\tIn this work we detected 30 species (16 in poultry houses and 23 in surrounding areas) representing 16 fungal genera: Aspergillus (A. flavus –\n\t\t\t\tFig. 6), A. niger, A terreus, A. nidulans, A. parasiticus, A. glaucus, A. clavatus -\n\t\t\t\tFig. 7), Penicillium –\n\t\t\t\tFig. 10\n\t\t\t\t(P. chrysogenum, P. solitum, P. sticticus), Cladosporium (C. cladosporoides –\n\t\t\t\tFig. 8), Alternaria (A. alternata – Fig. 9, A. tennuissima), Scopulariopsis (S. brevicaulis, S. acremonium), Fusarium\n\t\t\t\t– Fig. 11\n\t\t\t\t(F. oxysporum, F. graminearum), Mucor (M. mucedo) Drechslera (D. graminae, Drechslera sp.), Verticillium sp., Mycelia sterilia, Ulocladium sp., Trichoderma (T. viridae), Scedosporium sp., Candida (C. albicans, C. inconspicua, C. lambica), Rhodotorula ( R. rubrum), Cryptococcus (C. laurentii) –\n\t\t\t\tTable 3. The majority of these species are known as the potential respiratory allergens. The most common airborne moulds, both indoors and outdoors, were Penicilium sp., Aspergillus sp., Cladosporium sp., Alternaria sp., and Fusarium sp. The yeast were sometimes the dominant fungus in the indoor air comparison with the outdoor air, where this group of fungi occur very sporadically.
\n\t\t\tAmong fungi identified from the farm I, there distinctly dominated the species belonged to genera Candida spp. which constituted on average, over 69% in summer and 82.5% in spring. In comparison with the predominated yeast inside poultry houses I, in outdoor air the most frequent species were moulds A. flavus (80% in sampling point I 50.36% in I 10 and 52.5% in I 100) and F. oxysporum (26.9%, 13.5%, 16.2% in sampling point I 10, I 50, I 100, respectively). On the other hand, in the air surroundings poultry house II dominated species were A. clavatus (about 16%) and A. alternata (38.4%) in spring and C. cladosporoides (in summer) which constituted 68.5%. Whereas, A. clavatus (54.5%) and A. flavus (27.3%) were dominated species inside poultry house II.
\n\t\t\tConidiophores of A. flavus and A. clavatus, oryg.
Conidiophores of C. cladosporoides and poroconidia of A. alternata, oryg.
Conidiophores of Penicilium sp. and macroconidia of Fusarium sp., oryg.
Genus | \n\t\t\t\t\t\tSpecies | \n\t\t\t\t\t\tSampling site | \n\t\t\t\t\t|||||||
\n\t\t\t\t\t\t\tFarm I\n\t\t\t\t\t\t | \n\t\t\t\t\t\tI 10 | \n\t\t\t\t\t\tI 50 | \n\t\t\t\t\t\tI 100 | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tFarm II\n\t\t\t\t\t\t | \n\t\t\t\t\t\tII 10 | \n\t\t\t\t\t\tII 50 | \n\t\t\t\t\t\tII 100 | \n\t\t\t\t\t||
\n\t\t\t\t\t\t\tStaphylococcus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsciuri\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\taureus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t|
\n\t\t\t\t\t\t\tepidermidis\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tcohnii subsp.2\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tlentus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\txylosus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tsaprophitycus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tMicrococcus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsedentarius\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tlylae\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t | |
\n\t\t\t\t\t\t\thalobius\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tluteus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tEnterococcus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsp.\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tStreptococcus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tmitis\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tBacillus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tmycoides\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t |
\n\t\t\t\t\t\t\tsp.\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tCorynebacterium\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\txerosis\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tPsedomonas\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\taeruginosa\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tfluorescens\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tchlororaphis\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tXantomonas\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tmaltophila\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tShigella\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tboydii\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tProvidencia\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsp.\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tCitrobacter\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tfarmerii\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tEscherichia\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tcoli\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tEnterobacter\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsakazakii\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tagglomerans\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tProteus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tmirabilis\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
Bacterial species isolated from the poultry houses I and II and from surroundings area during spring 2009 and summer 2010.
Genus | \n\t\t\t\t\t\tSpecies | \n\t\t\t\t\t\tSampling site | \n\t\t\t\t\t|||||||
\n\t\t\t\t\t\t\tFarm I\n\t\t\t\t\t\t | \n\t\t\t\t\t\tI 10 | \n\t\t\t\t\t\tI 50 | \n\t\t\t\t\t\tI 100 | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tFarm II\n\t\t\t\t\t\t | \n\t\t\t\t\t\tII 10 | \n\t\t\t\t\t\tII 50 | \n\t\t\t\t\t\tII 100 | \n\t\t\t\t\t||
\n\t\t\t\t\t\t\tAspergillus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tflavus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tniger\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tterreus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tglaucus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tnidulans\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tparasiticus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tclavatus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t|
\n\t\t\t\t\t\t\tPenicilium\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsolitum\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tsticticus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tchrysogenum\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tFusarium\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\toxysporum\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tgraminearum\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tAlternaria\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\talternata\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t
\n\t\t\t\t\t\t\ttennuissima\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tUlocladium\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsp.\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tTrichoderma\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tviridae\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tVerticilium\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsp.\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tDrechslera\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsp.\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tgramineae\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tScopulariopsis\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tbrevicaulis\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tacremonium\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tCladosporium\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tcladosporoides\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t
\n\t\t\t\t\t\t\tMucor\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tmucedo\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t |
\n\t\t\t\t\t\t\tScedosporium\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tsp.\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t
Mycelia | \n\t\t\t\t\t\tsterilia | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t |
\n\t\t\t\t\t\t\tRhodotorula\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\trubrum\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tCandida\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\talbicans\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
\n\t\t\t\t\t\t\tinconspicua\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tlambica\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t | |
\n\t\t\t\t\t\t\tCryptococcus\n\t\t\t\t\t\t | \n\t\t\t\t\t\t\n\t\t\t\t\t\t\tlaurentii\n\t\t\t\t\t\t | \n\t\t\t\t\t\t+ | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t\t | + | \n\t\t\t\t\t\t\n\t\t\t\t\t\t | \n\t\t\t\t\t\t | \n\t\t\t\t\t |
Fungal species isolated from the poultry houses I and II and from surroundings area during study period (spring 2009 and summer 2010).
The literature data usually show the air biopollutant concentration inside the poultry houses. According to many studies (Agranovski et al., 2007, Radon et al., 2002, Vučemilo et al., 2006, 2007) the number of bacteria in poultry houses ranged from 103 to 1010 CFU/m3, and the concentrations of fungi was from 2.5 x 101 to 4.9 x 106 CFU/m3. Much less is known about the relationships between the indoor and the outdoor biological pollution. In comparison with the rate of microorganisms contamination in the poultry houses, the concentration of bacterial and fungi in the air in surrounding areas was considerable lower and did not exceed the values found inside farms. Airborne bacterial and fungi levels measured in poultry houses I and II were always higher than in adjacent areas. Therefore we can suggested that the source of microorganisms are probably the farm objects. Baykov & Stoyanov 1999 also reported higher bacterial levels inside broiler farms than in nearby areas and the average values were similar to our results, i.e. value of mean of 16020 CFU/m3 for farmhouses and range of2060 CFU/m3to 386 CFU/m3 for immediate areas (10 m and 100 m from farm object, respectively). Very high concentration of microorganisms may reflect on insufficient ventilation in relation to the number of animals kept in poultry houses.
\n\t\t\tThe presence of bacteria and fungi in poultry air is a natural phenomenon. Their primary source are the animals themselves, feed and litter. Microorganisms are a constituent of solid and liquid bioaerosols. This mostly refers to saprophytes, however pathogenic microorganisms were also found in the poultry houses air. Aerial count of pathogenic bacteria and fungi depends on the health condition of animals kept in the poultry houses. In addition, microorganisms count inside poultry farms air and monitoring of its emission from this building to the adjacent environment are important parameters for the assessment of the influence of poultry houses on the environmental pollution (Matković et al., 2006). In the present study, microbiological air contamination were determined at three sites at a distance of 10 m, 50 m and 100 m from the poultry houses. The results of total microorganisms count measurements outside the both poultry houses showed it to be lower than the total bacterial and moulds count inside the poultry houses. Number of microorganisms increase at 10 m distance from the poultry houses and gradually decreased to reach the lowest value at a distance of 100 m.
\n\t\t\tAnalyzing the results of the microbiological research about air pollution, it should be remembered that the results are temporary values, occurring at the moment the measurement. In connection with the physico-chemical properties of the air, the degree of contamination of the air can change diametrically within a few minutes (Donderski et al., 2005). Weather condition have a enormous influence on the count of microorganisms in the air. Temperature rise accompanied by rain scarcity can lead to a sudden increase in the concentration of microorganisms in the air. Consequently in summer with the weather conditions most friendly for the spread and development of numerous microorganisms, mesophilic bacteria, staphylococci, gram-negative bacteria and fungi were the more abundant in the air around the poultry houses than in early spring, where the temperature and humidity were lower.
\n\t\t\tStaphylococci seem to be a useful indicator bacteria (Schulz et al., 2004). Although this group of bacteria do not produce spores, they have the ability to survive in the air for a long time, which means spreading infections through the air. In the poultry houses I and II and outdoor air we observed very high numbers of potentially pathogenic staphylococci, what is really negative phenomenon. In our study the predominant species were coagulase negative. S. aureus and S. saprophitycus are pathogens for humans and the other species isolated in our studies may act as opportunistic pathogens in humans and animals. Karwowska 2005 also described the very high number of staphylococci in the air farming.
\n\t\t\tMoulds and yeast can live practically anywhere and have particularly favorable conditions inside the poultry houses. Among fungi recovered from the farm I, the species belonged to genera Candida spp. were dominated. This is a large group of potentially pathogenic species. They are usually an etiological factor in mycoses and less frequently, in mycoallergies. As they can produce toxins (e.g. candotoxins), the species can cause mycotoxycoses and increase microorganism sensitivity to some bacterial infections (Ejdys et al., 2009). On the other hand, in outdoor air the most frequent species were moulds Aspergillus flavus and Fusarium oxysporum. Amongst the several secondary metabolites produced by A. flavus are aflatoxins, the most toxic and potent carcinogenic natural compounds ever characterized. Whereas, the F. oxysporum is potentially producers of zearalenone, scirpentriol, NT-2 toxin, nivalenol, acetoxyscirpenediol, acetyl T-2toxin and others dangerous toxins (
In the air surroundings poultry house II dominated species were Aspergillus clavatus, Alternaria alternata, Cladosporium cladosporoides. Whereas, A. clavatus and A. flavus were the most frequent species inside poultry house II. We should emphasized that A. alternata is one of the most common fungi associated with asthma. Not only the presence of asthma but also persistence and severity asthma have been strongly associated with sensitization and exposure to A. alternata (Salo et al., 2006). On the other hand, the presence of opportunistic pathogens from the genus Aspergillus poses a risk of invasive aspergillosis in farm workers and those living in the proximity of the farms. According to the data obtained by other authors (Soliman et al., 2009) fungi e.g. Candida albicans, Aspergillus niger, A. nidulans, Penicilium sp. and Mucor sp. were prevalent in broiler farms in Egypt. However, Romanowska-Słomka and Mirosławski 2009 described the occurrence of the moulds and yeast Aspergillus sp., Penicillium sp., Candida sp. and Cryptococcus sp. in poultry houses. Other investigators (Agranovski et al. 2007) isolated and identified many fungal strain, including genera: Cladosporium, Aspergillus, Penicillium, Scopulariopsis, Fusarium, Epicoccum, Mucor, Trichophyton, Alternaria, Ulocladium, Basidiospores, Acremonium, Aureobasidium, Drechslera, Pithomyces, Chrysosporium, Geomyces and Rhizomucor from farming areas. The presence of such fungi in farmhouses was proved by the results of this study.
\n\t\t\tThe highest total Enterobacteriacea counts were found in indoor air and in areas nearby poultry houses I and II. In this present studies both in farms and surroundings areas Escherichia coli, Proteus mirabilis, Shigella boydii, Citrobacter farmerii, Enterobacter agglomerans, E. sakazakii, Klebsiella pneumoniae, Providencia sp. were identified. Different results was observed by Vučemilo et. al who found four dominating species of the Enterobacteriaceae family: E. coli, Pantoea sp., Serratia plymuthica and Serratia marcescens. According to Lues et. al 2007\n\t\t\t\tE. coli and the other members of the coliforms bacteria could be a good indicators of air contamination.
\n\t\tThe farming buildings are emitters of the considerable amounts of microbiological contaminants into the atmospheric air. This high emission of potentially pathogenic microorganisms via aerosols from animal housing facilities to the outdoor environment may constitute a considerable risk to human health and environmental pollution.
\n\t\t\tSo far, in literature there are no reliable data about relationships between the indoor and the outdoor biological pollution. This study contributes to the understanding of the level concentration of bioaerosol and its composition with regard to the different distance from farms. The quantity and quality of microbial analysis shows both different bacteria genera and fungi in indoor and outdoor microbiological contamination. Comparing our own results with available literature data on the indoor and outdoor air biopollutant concentration in the poultry houses enables to understand the distribution process.
\n\t\tHigh amounts of biogenic amines in food are considered undesirable microcomponents from the safety perspective, due to their potentially negative effects on consumer health. According to the risk assessment of biogenic amines carried out by the European Food Safety Authority (EFSA) [1], the amine content currently found in foods could be responsible of the triggering of health disorders. Histamine is the biogenic amine most commonly associated with the onset of health complaints. In fact, the triggering of symptoms derived by an excessive consumption of this amine was described for the first time over 60 years ago. It was firstly called scombroid fish poisoning, because the symptoms appeared mainly after the consumption of fish from the Scombridae and Scomberesocidae families, which have naturally high histidine contents. However, the World Health Organisation (WHO) recommendeds using the term histamine poisoning or histamine intoxication, since other foods can also be involved [2]. Histamine intoxication occurs in the form of an outbreak, affecting those who have consumed a particular histamine-rich food. A few years ago, another histamine-related disorder began to be described, known as histamine intolerance, which arises from the failure of the diamine oxidase (DAO) enzyme to metabolise histamine in the intestines. This enzymatic deficit in a sensitive population may explain some of the uncertainties classically associated with histamine intoxication. In this chapter we review the available information on dietary histamine and its adverse effects, using a risk analysis approach, focusing specifically on the components of risk assessment and management.
\nHistamine (2-[4-imidazolyl] ethylamine) is the causative agent of both histamine intoxication and histamine intolerance. Based on its chemical structure and number of amine groups, histamine is classified as a heterocyclic diamine. Important physiological activities of histamine in the human organism include synaptic transmission, blood pressure control, allergic response and cellular growth control [1]. Histamine is also found in foods, mainly fish, fish products and fermented foodstuffs [1, 3]. The major pathway for the formation of histamine in foods is the decarboxylation of its precursor amino acid, histidine, by the action of the bacterial enzyme L-histidine decarboxylase (Figure 1). This enzyme requires pyridoxal-5′-phosphate (vitamin B6) as a cofactor, an exception being the pyruvoyl-dependent histidine decarboxylase of Gram-positive bacteria [3, 4, 5]. Other biogenic amines commonly found in foods are tyramine, putrescine and cadaverine and to a lesser extent β-phenylethylamine and tryptamine [3, 4, 6]. These amines are all synthesised by the microbial decarboxylation of their corresponding precursor amino acids [7]. Therefore, the accumulation of histamine and other biogenic amines in foods requires the concurrence of several factors: microorganisms with decarboxylase enzymes, the availability of precursor amino acids and favourable environmental conditions for the growth or activity of aminogenic microorganisms [6, 8].
\nHistamine formation by histidine decarboxylation.
Although the ability to decarboxylate certain amino acids is a strain-dependent property, several genera of both Gram-positive and Gram-negative bacteria associated with food spoilage and/or with technological applications can produce histamine (Table 1) [1, 5, 9]. Enterobacteriaceae, including mesophilic and psychrotolerant species of Morganella, Enterobacter, Hafnia, Proteus and Photobacterium, are the most prolific histamine-producing bacteria in fish [4, 7, 9, 10]. In the case of fermented foods, aside from certain strains of enterobacteria, many lactic acid bacteria are also reported as histamine-producing microorganisms [1, 9].
\nFood | \nMicroorganisms | \n
---|---|
Fish | \nMorganella morganii, Morganella psychrotolerans, Klebsiella pneumonia, Hafnia alvei, Proteus vulgaris, Proteus mirabilis, Enterobacter cloacae, Enterobacter aerogenes, Serratia fonticola, Serratia liquefaciens, Citobacter freundii, Clostridium sp, Pseudomonas fluorescens, Pseudomonas putida, Aeromonas spp., Pleisomonas shigelloides, Photobacterium phosphoreum, Photobacterium psychrotolerans | \n
Fermented food (cheese, dry-fermented meat sausage, wine) | \nLactobacillus buchneri, Oenococcus oeni, Lactobacillus hilgardii, Pediococcus parvulus, Pediococcus damnosus, Lactobacillus bavaricus, Lactobacillus brevis, Lactobacillus curvatus, Lactobacillus parabuchneri, Lactobacillus rossiae, Lactobacillus saerimneri 30a, E. aerogenes, E. cloacae, Escherichia coli, H. alvei, Klebsiella oxycata, M. morganii, S. liquefaciens, Tetragenococcus spp., Leuconostoc spp. | \n
The function of decarboxylase enzymes in bacterial metabolism is not fully understood, although it has been described as one of the primary emergency systems involved in the acid stress response [6]. Decarboxylases work in cooperation with a membrane antiporter protein, thus enabling amino acids to be transported into the cell and biogenic amines to be excreted out of the cell. Since decarboxylation consumes a proton, biogenic amine formation contributes to the regulation of intracellular pH and may also help to increase the pH of extracellular media with a low buffer capacity [5, 8]. Apart from the alkalinisation effect, amino acid decarboxylation can also induce metabolic energy generation through a proton motive force, a fundamental function for bacteria without a high capacity to generate ATP [1, 5, 6, 8].
\nIn general, food products susceptible to containing high levels of histamine are those that are microbiologically spoiled (fresh fish, meat, etc.) or fermented/cured, in which the active bacteria can present an aminogenic capacity [11, 12]. Moreover, foods rich in free histidine may be more susceptible to histamine accumulation, as is the case of scombroid fish species [7, 12]. Endogenous histamine is also found in foods that contain blood or viscera, as well as in some plant products [3, 13].
\nStorage temperature is one of the most important factors of histamine formation in food [7, 10, 14, 15]. High temperatures (around 25–30°C) have been described by many authors as optimal for most histaminogenic microorganisms, but significant histamine formation has also been reported in refrigerated foods (4–10°C), especially fish [14, 16, 17]. Only ice storage at near 0°C was found to retard histamine formation [17]. In fermentation processes, histamine and other biogenic amines formation is reduced at temperatures lower than 15°C [18]. Other factors, such as pH, formulation (e.g. salting, species, nitrites), starter cultures, technological conservation processes (pasteurisation, high hydrostatic pressures, irradiations) and packaging (vacuum, modified atmospheres), have been extensively studied as potential conditioners of microbial capacity to form histamine [6, 11, 12, 14].
\nHistamine is involved in vital physiological activities in the human body, including neurotransmission, immunomodulation, haematopoiesis, wound healing, circadian rhythms, regulation of cell proliferation, contraction of smooth muscle cells, vasodilatation, increased vascular permeability and mucous secretion, alterations in blood pressure, arrhythmias and the stimulation of gastric acid secretion [15, 19]. Its effects occur through the binding of histamine with four receptors (H1R, H2R, H3R and H4R) located in the target cells of various tissues. Plasma histamine levels between 0.3 and 1.0 ng/mL are considered normal [19].
\nIn humans, two main routes of histamine metabolism are known, involving the enzymes histamine-N-methyltransferase (HNMT) and DAO (Figure 2). The product of HNMT-catalysed histamine methylation is N-methylhistamine (MHA), which is subsequently transformed by the monoamine oxidase (MAO) to N-methylimidazole acetaldehyde. The latter is then converted to N-methylimidazoleacetic acid (MIAA) by aldehyde dehydrogenase (ALDH). HNMT, a cytosolic enzyme that metabolises histamine only in the intracellular space, is expressed in almost all tissues, although mainly in the liver and kidney [15, 20]. On the other hand, the oxidative deamination of histamine by DAO leads to imidazole acetaldehyde and then, via ALDH transformation, to imidazole acetic acid (IAA), which is combined with a ribose molecule for its excretion [15, 20]. DAO, which is found mainly in the intestines, placenta and kidneys, is a secretory protein responsible for scavenging extracellular histamine after mediator release [15, 20].
\nMetabolic pathways of histamine in the human organism.
Histamine intoxication occurs after the ingestion of foods with unusually high amounts of histamine, which overwhelm the metabolic capacity of the organism [1, 21]. Previously known as scombrotoxicosis, scombroid fish poisoning, pseudoallergic fish poisoning, histamine overdose or mahi-mahi flush [1, 15], it was initially associated with ingestion of fishes from the Scombridae and Scomberesocidae families (e.g. mackerel, tuna, albacore and bonito). The first histamine intoxication was reported in sailors some centuries ago, but it was not until 1946 that publications began to describe the relationship between histamine and intoxication symptoms [9, 22, 23]. In the 1980s, the WHO recommended using the term histamine poisoning or intoxication, as the condition could be caused by the consumption of other fish species, as well as other foods [2].
\nThe symptomatology associated with histamine intoxication is closely related to the different physiological actions of histamine in the organism. The main symptoms are neurological, gastrointestinal, dermatological and respiratory, notably rash, erythema, sweating, nausea, vomiting, diarrhoea, a sensation of burning in the mouth, swelling of tongue and face, headache, respiratory distress, palpitations and hypotension [4, 15, 21]. Symptoms are generally mild, appearing 30 minutes after ingestion and disappearing within 24 hours [4, 10, 24]. On rare occasions, they can be more severe and require medical attention [3, 4]. The severity or type of reaction depends on the amount of histamine in the plasma. Thus, plasma concentrations higher than the normal level of 1–2 ng/mL result in an increase in gastric secretion and heart rate; 3–5 ng/mL causes headache, flushing, urticaria, pruritus and tachycardia, 6–8 ng/mL a decrease in blood pressure, 7–12 ng/mL bronchospasm and over 100 ng/mL cardiac arrest [19].
\nThe similarity between the described symptomatology and that of allergic reactions can lead to an incorrect diagnosis. Intoxication may be distinguished from a food allergy by taking into account the absence of an allergy history and its occurrence in an outbreak involving more than one patient over a short period of time after the consumption of foods with a high histamine load [9]. For a differential diagnosis, the concentration of serum tryptase measured within 1–2 hours of the onset of symptoms can also be helpful. In food allergy, the activity of serum tryptase increases, whereas in histamine intoxication it should remain within normal physiological values [15, 25]. Moreover, intoxication may be confirmed by elevated histamine levels in the suspected implicated food [1].
\nHistamine intolerance, also known as enteral histaminosis or sensitivity to food histamine, is a disorder in histamine homeostasis mainly due to reduced intestinal degradation by a deficit of DAO activity and the resulting enhanced plasma concentrations [19, 26, 27]. This disorder is not so widely known as histamine intoxication, since the first reference regarding histaminosis or histamine intolerance dates from 1988, and most of the studies have appeared during the last 15 years [28]. DAO enzyme deficiency may have a genetic aetiology. A significant relationship has been found between lower DAO activity and the presence of different single-nucleotide polymorphisms (SNPs) in the AOC1 gene located on chromosome 7 (7q36.1) that encodes this enzyme [29, 30]. The secretion of DAO may also be inhibited by certain pathologies, especially inflammatory bowel diseases, and also by the action of drugs (acetylcysteine, clavulanic acid, metoclopramide, verapamil, etc.) [15, 19]. The role of DAO inhibitor drugs may be significant, as it has been estimated they are being consumed by approximately 20% of the European population [1, 28].
\nSeveral clinical studies have linked DAO deficiency with the appearance of gastrointestinal (abdominal pain, diarrhoea and vomiting), dermatological (atopic dermatitis, eczema or chronic urticaria) and/or neurological (headaches) complaints [31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42]. Individuals with histamine intolerance due to DAO deficiency may suffer symptoms similar to those of intoxication, but they appear after a lower histamine intake. The diagnosis is based on the presentation of at least two clinical symptoms, which go into remission when a low-histamine diet is adopted (always after ruling out positive results for food allergy) [19, 42]. Individuals with histamine intolerance can also be identified by determining serum DAO activity, although evidence for the usefulness of this analysis is still scarce and inconclusive [27, 34, 36, 43, 44]. Despite the lack of well-proven data on the incidence of histamine-intolerant individuals with a DAO deficit, it has been estimated as affecting 1% of the population [19].
\nAlthough a range of plasma histamine levels have been associated with the onset of different symptoms, as described above, there is no consensus on what quantities of histamine in food are responsible for intoxication outbreaks. Dose-response data from food histamine are scant [24]. According to some studies in healthy volunteers, histamine was found to trigger intoxication symptoms at levels of 75–300 mg when administered with food (fish or non-alcoholic drinks) [1]. When histamine was administered with alcoholic beverages, levels of 0.12–4 mg in wine did not cause significant effects on healthy volunteers, whereas another trial demonstrated the onset of clinical symptoms in 12 out of 40 patients with histamine intolerance following a provocation test with 4 mg of histamine in sparkling wine [1]. Wantke et al. [45] reported the onset of symptoms after the ingestion of 50 μg of histamine in wine (125 mL) in patients with histamine intolerance. On the other hand, when 120 mg of histamine was introduced directly into the duodenum (not transported by food), symptoms appeared in patients diagnosed with chronic urticaria but not in healthy volunteers [1].
\nThe majority of histamine poisoning outbreaks described in the literature occurred after the consumption of high amounts of histamine, mainly in fish [1]. The histamine levels in the foods associated with these outbreaks vary considerably, in the vast majority of cases with values ranging from 100 to 5000 mg/kg [46, 47, 48, 49, 50, 51, 52, 53], although amounts of up to 10,000 mg/kg have also been reported [53].
\nDue to the lack of consensus to establish a threshold toxic dose for histamine intoxication, some authors have proposed some safe levels [3, 4]. Lehane and Olley [54] suggested 30 mg of histamine as a safe dose, calculated from the maximum level of 100 mg/kg of histamine in foods and based on a fish serving of 300 g and a consumer weight of 60 kg. The same authors, however, pointed out that the accuracy of their calculation was limited by an incomplete understanding of histamine intoxication. Later, Rauscher-Gabernig et al. [24] reported that dietary histamine levels in the range of 6–25 mg/meal had no adverse effects. The EFSA expert panel on biological risks proposed 50 mg/person/meal as a safe upper limit of histamine intake for healthy individuals, based on the few studies published to date [1]. This value corresponds with the 50 mg safe threshold advocated for the healthy population by the joint FAO/WHO report on health risks of histamine and other biological amines in fish and derivatives [21].
\nA safe level of histamine intake for intolerant individuals is not proposed in any of the studies on this disorder. The only recommendation available is from EFSA, which carried out a risk assessment of biogenic amine formation in fermented products and concluded that only foods with histamine levels below detectable limits can be considered safe for intolerant patients [1].
\nOne of the most important factors affecting sensitivity to dietary histamine is the different histamine-metabolising capacity of each individual. Thus, those with a lower activity of enzymes involved in histamine metabolism (DAO, HNMT, MAO) are more sensitive to suffer the effects after histamine ingestion [1]. An impaired enzymatic activity may have a genetic explanation or be caused by intestinal pathologies or the action of drugs with an inhibitory effect [15, 19, 20]. In this context, the most studied enzyme is DAO. The enhanced sensitivity of women to histamine in certain physiological states, such as in the premenstrual period, is attributed to a reduced DAO activity [55]. Conversely, an increase in DAO production of up to 500-fold has been reported during pregnancy, accompanied by a remission of certain symptoms related to histamine intolerance [56]. Therefore, from the metabolic point of view, there is inter- as well as intra-individual variation in sensitivity.
\nThe toxicity of histamine may be enhanced by dietary components, such as other biogenic amines or alcohol. Putrescine, cadaverine, tyramine and spermidine are biogenic amines usually found together with histamine in food and likewise are DAO substrates. Due to competition for intestinal mucin attachment sites and metabolisation, the ingestion of high quantities of these other amines may potentiate the adverse effects of histamine [1, 10, 15, 54]. This effect has been demonstrated in amines such as putrescine, cadaverine and tyramine, among others, in both in vitro and animal studies [1, 11]. These amines were found to exert an inhibitory effect on histamine metabolism when present at levels 4–5 times higher than that of histamine [11]. This potentiation mechanism could explain why symptoms do not appear when histamine is administered intravenously and yet are triggered when the same amounts of histamine are consumed in foods containing other amines [4].
\nAlcohol and its metabolite acetaldehyde can also have a potentiating effect. Competition for the ALDH enzyme, which is involved in the metabolism of both alcohol and histamine, results in an accumulation of histamine [1, 12]. The presence of these potentiating factors can thus explain the appearance/absence of symptoms or the variable degrees of reaction among individuals who have consumed foods containing the same amount of histamine.
\nFrequent misdiagnosis and the lack of an adequate and obligatory system for reporting histamine intoxication could account for the limited statistical data on the incidence of this food-borne disease [10, 15]. A total of 386 outbreaks were reported in 2010–2015 by different EU member states according to the EFSA reports on food-borne outbreaks [57]. In 191 of the outbreaks, the food responsible was determined with strong evidence, involving more than 1000 cases of which 107 were hospitalised (Figure 3). No deaths due to histamine intoxication were reported during this period. According to these data, there is no clear declining trend in the incidence of histamine intoxication in recent years, in contrast with other types of food poisoning (Figure 3). During this period, fish and fishery products were the primary cause of histamine intoxication in the European Union (176 outbreaks), followed by “mixed foods” (six outbreaks, three of which included a dish of tuna), “cheese” (three outbreaks), “buffet meal”, “crustaceans, shellfish, mollusc and products thereof”, “dairy products other than cheese”, “vegetables and juices and other products thereof” (one outbreak each) and “other foods” (two outbreaks) [57].
\nAssessment of the incidence of histamine intoxication in EU countries during the 2010–2015 [57].
On the other hand, according to information extracted from the Rapid Alert System for Food and Feed (RASFF), there was a clear rise in notification of histamine intoxication cases linked to tuna consumption during 2014–2017, with a particularly sharp increase in 2017 [57]. In May 2017, Spain and France reported a high incidence of histamine intoxication after the consumption of yellowfin tuna from Spain. Additional cases may have arisen in other countries that imported this food product. More than 150 people in Spain and more than 40 in France were affected after consuming tuna that was allegedly treated with a vegetable extract to alter the colour and enhance display freshness [58]. The modification of colour may mask spoilage responsible for the production of histamine and other biogenic amines.
\nTo assess consumer exposure, it is necessary to have data on histamine levels in foods. The overall exposure to dietary histamine is difficult to estimate due to its multiple potential sources and variable concentration. Figure 4, which shows the distribution of histamine contents in different foods retailed in Spain, reflects this characteristic high variability, both among different food categories and within the same category.
\nHistamine distribution (mg/kg or mg/L) in different food products [3].
Fresh fish and fishery products usually do not contain histamine or only low levels [59]. As shown in Figure 4, in most of the Spanish retail fish samples reported by Bover-Cid et al. [3], histamine was absent or found in very small quantities (P95 below 5 mg/kg). These data are in agreement with the scientific report published by EFSA based on samples of non-fermented fish and fish products from different European countries, in which only 27% of a total of 6329 samples contained histamine, usually at low concentrations (median of 2.5 mg/kg) [1]. However, a lack of freshness in raw fish and/or hygienically inadequate manufacturing processes of semi-preserved or preserved fish products can lead to markedly high histamine content. An example is the 657 mg/kg of histamine recorded within the Spanish canned fish category (Figure 4) or the 8910 mg/kg in fish and fishery products in the EFSA report [1]. Notably, when freshness is lost, in addition to high amounts of histamine, other amines related to the decarboxylase activity of spoilage bacteria, such as cadaverine and putrescine, also frequently accumulate.
\nIn fresh, cooked or cured meat, as in fish, no histamine occurrence is expected as long as freshness and a proper hygienic status of the products or manufacturing processes are ensured [1, 3, 60]. In contrast, fermented foods are susceptible to accumulating large amounts of histamine [1, 3, 5, 61]. In this type of foods, the occurrence of histamine depends not only on the hygienic conditions of the raw materials and/or manufacturing processes but also on the aminogenic capacity of the bacteria responsible for the fermentation [11, 12]. As can be seen in Figure 4, the presence of histamine in Spanish retail fermented foods is frequently relatively low (85% of samples below 20 mg/kg), but in some cases its levels are notably high, as in cheese (389 mg/kg), fermented sausages (475 mg/kg) or soybean products (730 mg/kg). In fermented beverages (e.g. wine and beer), histamine contents are much lower than those reported for other fermented foods. Notably, together with histamine, tyramine is usually the most frequent and abundant amine in fermented foods, because its formation is closely related to the lactic acid bacteria responsible for the fermentation processes, and its levels can reach 600 mg/kg in cheese, 700 mg/kg in fermented sausages and 1700 mg/kg in fermented vegetables. The occurrence of putrescine and cadaverine is also quite common but at lower and more variable concentrations than tyramine.
\nAmong foods of plant origin, only some vegetables usually show significant levels of histamine, such as spinach, tomato and eggplant [13]. In these products low levels of histamine may have a physiological origin, but undesirable microbial enzymatic activity during storage can lead to the accumulation of high levels [13, 62]. Lavizzari et al. [62] reported a significant increase in histamine levels in different spinach samples stored at refrigeration temperature during 2 weeks. Histamine formation in this type of vegetables was attributed to the activity of some Gram-negative bacteria, mainly belonging to Enterobacteriaceae and Pseudomonadaceae groups, as their growth is favoured by the relatively high pH of spinach. Asparagus, pumpkin, chard and avocado rarely contain histamine and at very low levels [13]. Other types of frequently consumed foods, such as cereals, milk, yoghurt and eggs, do not show significant contents of histamine or any other biogenic amine [3].
\nIn addition to food content, another fundamental issue when assessing exposure to histamine is the actual consumption of food by the population. Food consumption data need to be as representative as possible, with sources such as the most recent national dietary surveys.
\nIn the exposure assessment performed by EFSA, the 95-percentiles of biogenic amine contents of different European foods and their consumption patterns were combined to provide exposure values in terms of mg/day as an estimation of a high exposure scenario [1]. For histamine, the highest exposure values were obtained for the category “fresh, frozen and canned fish” (8.8–41.4 mg/day) followed by “dry-fermented sausages” (6.4–37.1 mg/day), “cheese” (13–32.1 mg/day) and “fish sauces” (0.4–29.9 mg/day). Likewise, in an assessment of the dietary histamine exposure of Austrian consumers, it was concluded that tuna fish and some fermented products (cheese and sauerkraut) were the top contributors to the total histamine intake [24]. According to this study, a typical meal with fish as a main dish could contribute from 2.3 to 264 mg of histamine. Recently, Latorre-Moratalla et al. [63] carried out an assessment of Spanish consumer exposure to histamine derived from the consumption of dry-fermented sausages, concluding that in 95% of cases, it was lower than 6.8 mg/meal.
\nThe larger serving size of fish products, together with the extremely high histamine contents arising from hygienic defects in their conservation or manufacturing processes, could explain why these foods contribute more to histamine exposure than others, such as cheese or dry-fermented sausages, which a priori have higher average histamine contents. This could also explain why fish and fishery products are the predominant cause of histamine intoxication.
\nPerforming an adequate quantitative risk characterisation of histamine exposure is hampered by the lack of dose-response data. However, a qualitative approach, taking into account the limited data available, suggests that the risk of suffering histamine intoxication is relatively low, since exposure exceeds the safety limit on very few occasions.
\nAccording to the qualitative risk characterisation performed by EFSA, exposure to histamine (95-percentile value) in fermented foods does not go beyond the safe threshold of 50 mg/meal/person [1]. However, it is stressed that this upper limit may be exceeded by the consumption of more than one food item with high histamine content during the same meal. Likewise, Latorre-Moratalla et al. [63] concluded that the risk of suffering acute effects related to histamine intake after the consumption of dry-fermented sausages in Spain is very low, since the exposure levels rarely exceed the safe threshold. It should be noted that all available studies have been carried out on specific food groups and to date none have dealt with the full range of histamine-containing foods.
\nThe risk for the histamine-intolerant population is higher, because even small amounts of histamine may trigger adverse effects [1, 63]. No studies have been carried out to evaluate this risk.
\nFrom the perspective of risk management, decision-makers or the food industry should consider different actions to reduce consumer exposure to dietary histamine. For example, regulatory measures or strategies to prevent, reduce or eliminate the presence of histamine and other amines in foods could be implemented.
\nFrom a legal perspective, tolerable limits of histamine have been fixed by different countries only for fish and fishery products. The European Union through Regulation (EC) No. 2073/2005 on microbiological criteria has established that in fishery products from species with a naturally high histidine content (particularly fish from the Scombridae, Clupeidae, Engraulidae, Coryphaenidae, Pomatomidae and Scomberesocidae families), using a sampling plan of nine samples, the mean histamine value must be less than 100 mg/kg, no sample should exceed 200 mg/kg and among nine samples only two can have a histamine content between 100 and 200 mg/kg [64]. In fishery products obtained from species with a high histidine content and subjected to an enzymatic maturation treatment in brine, the maximum average value allowed is 200 mg/kg, the maximum individual value is 400 mg/kg and there can only be two samples between these two values in a sampling plan of nine samples [64, 65]. The Food and Drug Administration (FDA) of the United States, using a sampling plan of 18 samples, establishes a tolerable maximum level of 50 mg/kg of histamine for tuna and mahi-mahi or between 50 and 500 mg/kg of histamine for other fish species, with just one sample higher than these values [66]. In Canada, Switzerland and Brazil, the maximum limit allowed in fish and fishery products is 100 mg/kg and in Australia and New Zealand 200 mg/kg [7].
\nAs histamine and other biogenic amines are a food safety concern, the food industry needs to consider improving control strategies. Available knowledge about biogenic amine formation in certain foods has made it possible to design measures to prevent or at least reduce their accumulation during manufacture and storage.
\nA key strategy is to guarantee and improve the hygienic quality of raw materials and manufacturing processes. Since contaminant microorganisms are responsible for biogenic amine formation in many products, food quality and safety management based on hazard analysis and critical control points (HACCP) are essential [4, 7]. The time/temperature binomial is the most critical and determinant risk factor in biogenic amine formation in most fresh and lightly preserved meat and seafood products, as well as in raw materials (of animal and plant origin) used in the preparation of cooked, ripened or fermented products [3, 7, 11]. Predictive models of biogenic amine formation in perishable products as a function of time and temperature could be used to avoid hazardous storage conditions [11, 67]. This approach has already been implemented to reduce histamine accumulation in seafood, which is particularly associated with histamine formation by Morganella psychrotolerans and M. morganii [67]. Other factors that inhibit or reduce aminogenic activity, such as the packaging atmosphere and the addition of salt and other preservatives, should be taken into account for lightly preserved fish, meat and vegetables [6, 11].
\nIn the case of fermented foods or beverages, the hygienic quality of raw materials may be enhanced by decreasing the microbial load through pasteurisation, a common practice in the cheese-making industry [5]. However, in fermented meat products, high temperature causes detrimental changes in the raw materials, thus rendering the conventional heat treatments unsuitable. The application of high-pressure treatments to raw materials (milk and meat) could be an effective strategy to improve their hygienic status, thereby reducing the biogenic amine accumulation without significant alteration of sensory properties [11, 68].
\nTechniques that avoid biogenic amine formation should also be implemented in fermented food products. For example, the use of a suitable formulation (adjusting the type and amount of fermentable sugar, spices and preservatives) and well-established technological parameters (temperature and relative humidity) enables a quick and accurate selection of desired fermentative microbiota, which limits the action of contaminant microorganisms, including amine formation [11, 18]. Moreover, it has been widely demonstrated that the selection of microorganisms without aminogenic activity for the starter cultures constitutes an effective control measure against biogenic amine accumulation in fermented products [6, 11, 18, 61]. For cases where these strategies are not sufficiently effective, a new approach currently being explored is the application of starter cultures with amino-oxidase activity, which are able to degrade previously formed amines [11, 61].
\nA general control strategy for wine that includes many of these approaches is the so-called low-histamine technology, which is based on the guaranteed hygienic quality of the raw materials, the addition of selected starter cultures and the use of specific production techniques that inhibit histamine formation [3]. The current challenge for the food industry is to extend this technology to other biogenic amines and other products. The successful implementation of “low biogenic amine technologies” will enable food manufacturers to produce safe and high-quality amine-free food.
\nAlthough the health problems associated with histamine consumption are well known, there are some uncertainties, especially regarding the threshold level of this amine that may trigger the symptoms. Histamine concentrations reported as responsible for intoxication outbreaks are extremely variable. Thus, despite the association of adverse effects with the ingestion of high levels of histamine, lower levels can also cause symptoms in sensitive individuals with a genetic or acquired impairment in the enzymatic degradation of histamine (the histamine-intolerant population). The difficulty in establishing a specific toxic dose is also due to the presence of other biogenic amines in the implicated foods, which can potentiate the adverse effects of histamine.
\nThe few qualitative risk assessments of histamine performed to date all indicate that the current risk of suffering histamine intoxication is low. However, in the population with histamine intolerance, the risk of suffering symptoms derived from the intake of histamine would be much higher. In fact, according to the risk assessment performed by EFSA, only levels below the detectable limit can be considered as safe. Therefore, for these individuals, the main strategy to avoid histamine-related health problems is to follow a diet that excludes foods rich in this or other amines, such as putrescine and cadaverine, which can potentiate the adverse effects of histamine.
\nAccording to current EU data, the consumption of spoiled fish and fishery products is the main cause of histamine intoxication outbreaks. Although this type of food usually has a low or negligible histamine content, a lack of freshness and poor hygienic conditions may result in the accumulation of high levels and trigger an outbreak. In contrast, whereas fermented foods often have higher histamine contents than fish and fish derivatives, their serving size tends to be lower, which could explain why they are generally less implicated in the outbreaks. Nevertheless, even when the risk of intoxication is low, the accumulation of high levels of histamine in fermented foods may indicate poor hygienic quality and is an argument for extending the legislative criteria to foods other than fish.
\nThe lack of consensus on what quantities of dietary histamine produce intoxication can be explained by the coexistence of other biogenic amines in the same foods, as well as inter- and intra-individual variability in histamine metabolisation. The impaired ability to metabolise ingested histamine has led to the description of a relatively new disorder, that of histamine intolerance due to DAO deficiency.
\nA current challenge for the food industry is to offer products with minimal biogenic amine levels, and it may be recommendable to declare the presence or absence of histamine in food labelling. Private initiatives have already begun to include the message “without histamine” in products as a hallmark of quality. Such labelling could help those with histamine intolerance to make a more informed selection of suitable foods.
\nSònia Sánchez-Pérez is a recipient of a doctoral fellowship from the University of Barcelona (APIF2018).
\nThe authors declare no conflict of interest.
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