Microbiological quality of honey from the Pampas Region (Argentina) throughout the extraction process

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Garro" "autores" => array:3 [ 0 => array:2 [ "nombre" => "Antonieta" "apellidos" => "Rodríguez de Olmos" ] 1 => array:2 [ "nombre" => "Maria Alejandra" "apellidos" => "Correa Deza" ] 2 => array:2 [ "nombre" => "Marisa S." "apellidos" => "Garro" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754116300967?idApp=UINPBA00004N" "url" => "/03257541/0000004900000001/v1_201704040030/S0325754116300967/v1_201704040030/en/main.assets" ] "itemAnterior" => array:19 [ "pii" => "S0325754116300955" "issn" => "03257541" "doi" => "10.1016/j.ram.2016.10.002" "estado" => "S300" "fechaPublicacion" => "2017-01-01" "aid" => "142" "copyright" => "Asociación Argentina de Microbiología" "documento" => "article" "crossmark" => 1 "licencia" => "http://creativecommons.org/licenses/by-nc-nd/4.0/" "subdocumento" => "fla" "cita" => "Rev Argent Microbiol. 2017;49:50-4" "abierto" => array:3 [ "ES" => true "ES2" => true "LATM" => true ] "gratuito" => true "lecturas" => array:2 [ "total" => 1142 "formatos" => array:3 [ "EPUB" => 48 "HTML" => 646 "PDF" => 448 ] ] "en" => array:13 [ "idiomaDefecto" => true "cabecera" => "Brief report" "titulo" => "First survey on antibiotic resistance markers in Enterobacteriaceae in Cochabamba, Bolivia" "tienePdf" => "en" "tieneTextoCompleto" => "en" "tieneResumen" => array:2 [ 0 => "en" 1 => "es" ] "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "50" "paginaFinal" => "54" ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Primer relevamiento de marcadores de resistencia a antibióticos en Enterobacteriaceae en Cochabamba, Bolivia" ] ] "contieneResumen" => array:2 [ "en" => true "es" => true ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1248 "Ancho" => 1475 "Tamanyo" => 88942 ] ] "descripcion" => array:1 [ "en" => "Antimicrobial susceptibility profiles. CTX, cefotaxime; CAZ: ceftazidime, FOX: cefoxitin, FEP: cefepime, NAL: nalidixic acid, CIP: ciprofloxacin, LEV: levofloxacin, KAN: kanamycin, GEN: gentamicin, AMI: amikacin." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Paola M. Saba Villarroel, Gabriel O. Gutkind, José A. Di Conza, Marcela A. Radice" "autores" => array:4 [ 0 => array:2 [ "nombre" => "Paola M." "apellidos" => "Saba Villarroel" ] 1 => array:2 [ "nombre" => "Gabriel O." "apellidos" => "Gutkind" ] 2 => array:2 [ "nombre" => "José A." "apellidos" => "Di Conza" ] 3 => array:2 [ "nombre" => "Marcela A." "apellidos" => "Radice" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754116300955?idApp=UINPBA00004N" "url" => "/03257541/0000004900000001/v1_201704040030/S0325754116300955/v1_201704040030/en/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "Original article" "titulo" => "Microbiological quality of honey from the Pampas Region (Argentina) throughout the extraction process" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "55" "paginaFinal" => "61" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Leticia A. Fernández, Carolina Ghilardi, Betiana Hoffmann, Carlos Busso, Liliana M. Gallez" "autores" => array:5 [ 0 => array:3 [ "nombre" => "Leticia A." "apellidos" => "Fernández" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] ] ] 1 => array:3 [ "nombre" => "Carolina" "apellidos" => "Ghilardi" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 2 => array:3 [ "nombre" => "Betiana" "apellidos" => "Hoffmann" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 3 => array:3 [ "nombre" => "Carlos" "apellidos" => "Busso" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] ] ] 4 => array:4 [ "nombre" => "Liliana M." "apellidos" => "Gallez" "email" => array:1 [ 0 => "labea@uns.edu.ar" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "Laboratorio de Estudios Apícolas (LabEA-CIC), Departamento de Agronomía, Universidad Nacional del Sur, San Andrés 800, 8000 Bahía Blanca, Provincia de Buenos Aires, Argentina" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Laboratorio de Ecología, Departamento de Agronomía, Universidad Nacional del Sur, San Andrés 800, 8000 Bahía Blanca, Provincia de Buenos Aires, Argentina" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Consejo Nacional de Investigaciones Científicas y Técnicas de la República Argentina (CONICET), Buenos Aires, Argentina" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Calidad microbiológica de la miel en la Región Pampeana (Argentina) a lo largo del proceso de extracción" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1248 "Ancho" => 1375 "Tamanyo" => 63756 ] ] "descripcion" => array:1 [ "en" => "Indoor air quality expressed by the number of molds and yeast (MY) and culturable heterotrophic mesophilic bacteria (CHMB) counts which were determined by the culture settling plate in two areas of honey houses during 2014 and 2015. Bars indicate standard deviation (SD)." ] ] ] "textoCompleto" => "IntroductionA honey house is a room or place within a building used for extracting, processing and/or handling honey. It is the center of activities for beekeepers. It represents an important portion of their investment, and may contribute greatly to the overall efficiency of their entire operation<a class="elsevierStyleCrossRef" href="#bib0215">6</a>. Due to the importance of Argentina's honey exports, SENASA<a class="elsevierStyleCrossRef" href="#bib0350">33</a> passed resolution 870/2006, which deals with the hygienic and sanitary aspects of honey houses. Thus, commercial honeys are ruled by the Mercado Común del Sur (MERCOSUR) legislation and the Código Alimentario Argentino (CAA)<a class="elsevierStyleCrossRef" href="#bib0200">3</a>. The maximum level allowed by this legislation for molds and yeasts (MY) with trading purposes is 100CFU/g of honey. Likewise, the legislation does not allow the presence of Salmonella and Shigella bacteria or of total coliforms in honeys.Although honey has high osmolarity, low water activity and nutrients, it holds microorganisms which could be present in pollen, dust, air, soil, phyllosphere and nectar<a class="elsevierStyleCrossRefs" href="#bib0240">11,27,35</a>. It is well known that microbial contamination may be originated from food handlers, equipment and cross-contamination during harvest<a class="elsevierStyleCrossRef" href="#bib0190">1</a>, and processing in honey houses<a class="elsevierStyleCrossRefs" href="#bib0310">25,35</a>. Consequently, appropriate standards of hygiene must be applied<a class="elsevierStyleCrossRefs" href="#bib0210">5,37</a> in all operations involving honey handling.The microorganisms of concern in honey are some fungi and spore-forming bacteria such as Bacillus cereus and Clostridium spp. which under certain conditions might cause illness in humans<a class="elsevierStyleCrossRef" href="#bib0360">35</a>. Some of the most recognized potential sources of Clostridium botulinum spores are the soil, dust, honey and medicinal herbs<a class="elsevierStyleCrossRef" href="#bib0240">11</a>. Sagua et al.<a class="elsevierStyleCrossRef" href="#bib0340">31</a> observed that 456 cases of infant botulism in Argentina were reported between 1982 and 2007, suggesting that some of these cases may be explained by the presence of C. botulinum spores in honey. Martins et al.<a class="elsevierStyleCrossRef" href="#bib0280">19</a> found a low contamination percentage with Bacillus cereus and fungi in honeys from Portugal. Nevertheless, they suggested that these potentially pathogenic species could be harmful to predisposed patients. Pirttijarvi et al.<a class="elsevierStyleCrossRef" href="#bib0330">29</a> reported that the potential toxigenic effects of Bacillus were achieved with 10<a class="elsevierStyleCrossRef" href="#bib0205">4</a> spores per g of honey.Argentina is one of the major honey exporters to countries like the United States; Germany and Japan. There are currently about 25000 beekeepers working with three million hives in Argentina. This is the country with the largest number of hives in the Southern Hemisphere<a class="elsevierStyleCrossRef" href="#bib0225">8</a>. Several works have been published about the microbiological characteristics of honeys ready to be sold in the retail market<a class="elsevierStyleCrossRefs" href="#bib0250">13,14,16,17</a>. However, little scientific research on the microbiological quality of honey obtained at different processing points in honey houses has been published. In Argentina, Mouteira et al.<a class="elsevierStyleCrossRefs" href="#bib0285">20–23</a>, Basso et al.<a class="elsevierStyleCrossRef" href="#bib0195">2</a> and Malacalza et al.<a class="elsevierStyleCrossRef" href="#bib0275">18</a> have studied possible sources of microbiological, physical and chemical contamination as well as the effect of beekeeping equipment on honey production within the honey houses.In 2009<a class="elsevierStyleCrossRef" href="#bib0235">10</a>, we started an evaluation of the sanitary risks during honey processing within the honey houses. Mold and yeast, total coliform number as well as the presence of Salmonella spp. were determined in 50 samples<a class="elsevierStyleCrossRef" href="#bib0235">10</a>. In this work, we assessed the microbiological quality of honey obtained from different processing points, and the environmental quality within honey houses, to enlarge and complete that research. Mold and yeast, culturable heterotrophic mesophilic bacteria, spore-forming bacteria and sulfite-reducing clostridia numbers, and the presence of Shigella spp., Salmonella spp. and fecal coliform were determined in 163 samples of honey obtained from eight honey houses in the southeastern Pampas Region, Argentina.Materials and methodsSampling sitesEight honey houses were sampled in the southeast of the Pampas Region, Argentina. This is the same region of the honey house sampled in 2009 by Gallez and Fernández<a class="elsevierStyleCrossRef" href="#bib0235">10</a>.Honey was sampled at different points in each of the honey houses. The first point was at the super storage place, where supers are filled with the honeycombs. The second one was at the uncapping machine, which in all cases had thermostatically controlled heated blades. The next point was at the honey-beeswax separator, allowing to recover honey from the cappings. Different uncapping systems, with and without heating the cappings, were sampled. The fourth point was at the honey extractor which extracts the honey from the combs by centrifugal force. The fifth point was at the honey sump, which is a tank or chamber into which the honey drains. In the Pampas Region, it is usually below ground level, and it is not water jacketed. The last sampled point was at the 300kg honey drums.Honey samplesOne hundred and sixty three honey samples were collected during February and March 2014 and 2015 from eight honey houses. All samples were aseptically collected in sterile 100ml vials and were grouped according to their origin. These samples were stored at room temperature and were processed within two months from collection<a class="elsevierStyleCrossRef" href="#bib0335">30</a>.Microbial countsMicrobial analyses were carried out in all of the samples in triplicate.Mold and yeast (MY) determination was carried out by plating appropriate dilutions of the honey samples. For this procedure, a 10g sample was homogenized in 90ml of 0.85% w/v NaCl (initial suspension) for 15min at 180rpm at room temperature. Decimal serial dilutions were plated onto fungi and yeast agar supplemented with chloramphenicol (Britania, Argentina) to inhibit bacteria. MY were counted after three – five days from plate incubation at 22–24°C.For assessment of culturable heterotrophic mesophilic bacteria (CHMB), decimal serial dilutions from the initial suspension that was previously described, were plated onto nutrient agar (Britania, Argentina). Plates were counted 72h after the incubation at 30°C.Total coliforms: aliquots of 1ml of the initial suspension were added to empty plastic Petri dishes. Violet Red Bile Lactose (VRBL, Merck) medium was poured over them. The plates were incubated at 35–37°C for three days.Results from all determinations were expressed as colony forming units (CFU)/g of honey.Complementary microbiological determinationsThe following microbial analyses were carried out in the samples coming from the honey drums.Evaluation of Bacillus spp.: the second dilution was heat activated at 70/80°C for 10min, and cooled immediately in iced water for another 10min. Aerobic spore-forming bacteria were plated on nutrient agar (Britania, Argentina). Plates were incubated three days at 35°C.Search for fecal coliforms: one ml of the initial suspension (10:90) for basic microbiological determinations was added to test tubes with brilliant green bile broth (2%) with Durham tubes inverted inside and were incubated at 37°C for two days. Positive samples (growth and gas production) in this medium were selected to streak in Mac Conkey solid medium. Suspicious colonies were isolated and placed in new tubes containing brilliant green bile broth (2%) and inverted Durham tubes and were incubated at 44°C for two days. Positive samples in this medium were reported as containing thermotolerant coliforms in 0.1g of honey. To confirm the presence of Escherichia coli, the positive tubes were tested by growth in EMB agar (Britania). Typical colony growth on EMB agar was confirmed by traditional assays including indole, methyl red, VP and citrate. Results expressed as presence or absence of E. coli.Isolation of spores of sulfite-reducing clostridia: aliquots of 25ml of the initial suspension for basic microbiological determinations were added to empty tubes which were centrifuged for 15min at 5000rpm. The pellet was thermally treated at 80°C for 5min. Then, 100μl of this suspension was spread on plates with SPS (sulfite–polymixin–sulfadiazine) agar (Bioclar, Argentina), and they were incubated anaerobically with the AnaeroPack–Anaero culture system (Mitsubishi Gas Chemical, Japan) in a vacuum desiccator at 37°C for 5 days.Isolation of Salmonella spp. and Shigella spp.: these bacteria were investigated according to a modification of the standard method suggested by the International Commission on Microbiological Specifications for Foods (ICSMF)<a class="elsevierStyleCrossRef" href="#bib0245">12</a>. For pre-enrichment, 25g of honey was added to 225ml of peptone water (Britania, Argentina) and cultures were incubated at 35°C for 24h. One ml of the pre-enrichment step was added to glass tubes containing selenite cystine broth (42°C for 24h) and another one ml to glass tubes containing tetrathionate broth (35°C for 24h). These enrichment steps were followed by the inoculation of selective solid media: EMB, salmonella shigella agar (SSA) and brilliant green agar (BGA). All media used were from Britania (Argentina). Petri dishes were incubated at 35°C for 48h and suspected colonies of Salmonella were tested in triple sugar iron (TSI, Britania) and lysine iron (LIA, Britania) agar. Colonies exhibiting typical reactions on TSI and LIA were purified and further characterized by traditional assays: urease, oxidase, phenylalanine decarboxylase, VP, indole, citrate and gelatin. Results were expressed as presence or absence of Salmonella spp.Environmental microbiological evaluationThe honey house may contain various other facilities in addition to the extracting plant, such as storage space for hive equipment and honey, workshops, office space, and possibly a packing or salesroom or both<a class="elsevierStyleCrossRef" href="#bib0215">6</a>. The research was conducted in the main extraction zone as well as in the other facilities.The culture settling plate technique, also known as sedimentation technique, was used for conducting a qualitative environmental assessment<a class="elsevierStyleCrossRef" href="#bib0345">32</a>. For this purpose, open Petri dishes filled with 20ml of a microbiological culture medium suitable for bacteria and fungi were used as the sampling surface. Fungi and yeast agar medium supplemented with chloramphenicol (Britania, Argentina) was used in order to determine the number of MY while nutrient agar medium (Britania, Argentina) was used for CHMB. Petri dishes were distributed at the processing areas previously mentioned and exposed for about one hour within the honey house. Once in the laboratory, plates were incubated at 26–28°C for 5 days for MY and 30–35°C for 3 days for CHMB. Results were expressed as CFU/min.ResultsMicrobial counts at different points of honey processing within the honey houseSimilar results were obtained for all microbiological determinations within all the studied honey houses during 2014 and 2015 (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>Eighty nine samples out of 163 had ≤10CFU per g of honey of MY, 69 samples ranged from 10 to 50CFU/g of honey, and two reached 65.5CFU/g of honey. Eighty one percent of the samples showed ≤30CFU of CHMB/g of honey, while only seven samples had between 50 and 54.25CFU/g. Total coliforms were different between the two harvesting periods. In 2014, 20 (35%) out of 57 samples had total coliforms, in which the count was less than 20CFU/g of honey. In 2015, total coliforms were not detected in samples taken from different points of the honey house.Microbiological quality of the honey from drumsThirty-six samples of honey were obtained from drums in the different honey houses. In 25 samples (69.4%), the counts of CHMB were less than ≤30CFU per g of honey. In addition, 20 samples (55.5%) showed between 10 and 50CFU of MY per g of honey (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Total coliforms were not detected in 25 samples, while colonies different from the typical morphology of coliforms were only observed in 11 samples.Fecal coliforms were not detected in samples from 2014 or 2015. All samples were contaminated with less than 50spores/g of Bacillus spp., except two from 2014 which showed between 50 and 100 spores. Typical black colonies from spores of sulfite-reducing clostridia were not detected in any sample when working under a total anaerobic atmosphere. In addition, bacteria from the genera Salmonella spp. Shigella spp. were not found in any of the honey drum samples.Microbiological quality of the honey house environmentThere were no statistical differences in MY and CHMB counts between the rooms/areas of the main extraction zone and other rooms/areas of the honey houses (<a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>DiscussionMicroorganisms in honey might come from several and different sources. Primary sources include pollen, digestive tracts of honey bees, dust, air, soil and nectar. Secondary sources are due to honey handlers and processing, and are easy to control by the application of good manufacturing practices (GMP)<a class="elsevierStyleCrossRefs" href="#bib0200">3,11,15</a>. In this work, we report the analysis of 163 honey samples which were obtained from different points of the honey processing within eight honey houses located in the southeast of the Pampas Region, Argentina. Our studies started in 2009 with 50 samples from one honey house<a class="elsevierStyleCrossRef" href="#bib0235">10</a>.We did not find any differences in microbial counts at the different points of honey processing among the eight honey houses sampled. Therefore, the results are discussed according to the six points we sampled within the honey house (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). In 2009, all samples from honeycombs and honey extractor samples showed low levels of MY (≤10CFU/g of honey). Low levels of MY and CHMB were also observed at those processing points and in the honey obtained from the uncapping machines (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Ten to 50CFU of MY/g honey were observed in four out of 30 samples in 2009<a class="elsevierStyleCrossRef" href="#bib0235">10</a> (13.3%), whereas 69 out of 163 samples were obtained with those counts in 2014/2015 (42.3%). These samples belonged to the following processing points: honeycomb uncapping, honey sump and honey drum. The higher MY counts in 2014/2015 than in 2009 might be due to higher rainfall, thus favoring microorganism development. In addition, total coliforms were present only in 11.65% of the samples in 2014, while there were no total coliforms in honey samples during 2009 and 2015. However, it is important to note that the food codes refer to honey for retail sale, at the end point of the food chain. Drums were the last sampling point in this study, previous to bottling, and total coliforms were absent in all the drum samples.Little information is available in Argentina about microbiological contamination within the honey houses. Mouteira and Basso (2014)<a class="elsevierStyleCrossRef" href="#bib0305">24</a> studied four points in a honey house of Ranchos in Buenos Aires Province. They reported counts of MY of 97CFU/g honey in honeycombs, 75CFU/g honey in honeycomb uncapping, 35CFU/g honey in honey extractor and 34.7CFU/g honey in drums. They also observed the absence of total coliforms. In another work, Mouteira et al.<a class="elsevierStyleCrossRef" href="#bib0290">21</a> compared the physicochemical and microbiological quality of honeys from two honey house buildings with different technology in Argentina. They found that although MY counts were below the maximum established limit by the CAA<a class="elsevierStyleCrossRef" href="#bib0200">3</a> (≤100CFU/g of honey), their number increased in all the studied processing points of the honey house which did not comply with GMP regulations. They also observed 19.87coliforms/g of honey in the drums in this honey house. Furthermore, Sereia et al.<a class="elsevierStyleCrossRef" href="#bib0355">34</a> compared and verified the main contamination sources and the hygienic/sanitary conditions of organic honey from Parana River islands (Brasil). These authors conclusively demonstrated that secondary sources of contamination were responsible for the reduction in the quality of organic honey.The maximum MY level allowed for trading by the MERCOSUR and CAA<a class="elsevierStyleCrossRef" href="#bib0200">3</a> legislations is 100CFU/g of honey: all drum samples showed cell counts below this stipulated value (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Likewise, the legislation neither allows the presence of Salmonella and Shigella bacteria nor of total coliforms. All the honey drum samples in our work showed these characteristics. Our results of the microbiological quality of honey at the end of the process in the honey house were similar to those reported by other authors in Argentina<a class="elsevierStyleCrossRefs" href="#bib0230">9,13,20</a>. In fact, our results are also similar to those published by other researchers who analyzed honey from different parts of the world<a class="elsevierStyleCrossRefs" href="#bib0220">7,26,36</a>.In the present study, we assessed the indoor air quality at the honey houses by the settling plate technique. It is interesting to note, that although there were no statistical differences of MY and CHMB counts between both studied areas, there was a tendency in both groups of microorganisms to be lower in the main extraction zone than in other rooms/areas. Similarly, Oliveira et al.<a class="elsevierStyleCrossRef" href="#bib0325">28</a> found that the installation of honey houses in untidy environments, and the environmental variables, could have been responsible for the presence of MY in quantities above those permitted by the standards. Furthermore, Grabowski and Klein<a class="elsevierStyleCrossRef" href="#bib0240">11</a> supported this idea explaining that like any other foodstuff, the hygienic status of honey is the result of the environmental conditions along the food chain.The “unheated” honey-wax separation process might be better to preserve the chemical quality of the honey. However and in accordance with our previous data, it implied a higher microbiological hazard than the heated process. This highlights the need to perform more studies in the honey house in this regard<a class="elsevierStyleCrossRef" href="#bib0235">10</a>. In this research, we characterized honey samples from eight honey houses; the different points of honey processing within these honey houses in the Pampas Region did not show any sanitary risks.Some simple good practices are not always applied, and their implementation could improve the microbiological quality of the honey. For instance, workers should wear clean outer clothing and adequate hair covering at all times during honey extraction and processing. Sanitary curtains and insect nets should be fitted over openings to reduce environmental contamination and to avoid bees from entering. Sumps must be adequately covered. While not in use, the equipment must be stored protecting it from dust, dirt, rodents, insects or other contamination sources. The application and/or reinforcement of proper honey handling and sanitation practices would allow to improve the microbiological quality of honeys.Ethical responsibilitiesProtection of human and animal subjectsThe authors declare that no experiments were performed on humans or animals for this study.Confidentiality of dataThe authors declare that no patient data appear in this article.Right to privacy and informed consentThe authors declare that no patient data appear in this article.FundingWe thank the Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC) Argentina, for financial support.Conflicts of interestThe authors declare that they have no conflicts of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:13 [ 0 => array:3 [ "identificador" => "xres824210" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec820702" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres824209" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec820703" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Sampling sites" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Honey samples" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Microbial counts" ] 3 => array:2 [ "identificador" => "sec0030" "titulo" => "Complementary microbiological determinations" ] 4 => array:2 [ "identificador" => "sec0035" "titulo" => "Environmental microbiological evaluation" ] ] ] 6 => array:3 [ "identificador" => "sec0040" "titulo" => "Results" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0045" "titulo" => "Microbial counts at different points of honey processing within the honey house" ] 1 => array:2 [ "identificador" => "sec0050" "titulo" => "Microbiological quality of the honey from drums" ] 2 => array:2 [ "identificador" => "sec0055" "titulo" => "Microbiological quality of the honey house environment" ] ] ] 7 => array:2 [ "identificador" => "sec0060" "titulo" => "Discussion" ] 8 => array:3 [ "identificador" => "sec0065" "titulo" => "Ethical responsibilities" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0070" "titulo" => "Protection of human and animal subjects" ] 1 => array:2 [ "identificador" => "sec0075" "titulo" => "Confidentiality of data" ] 2 => array:2 [ "identificador" => "sec0080" "titulo" => "Right to privacy and informed consent" ] ] ] 9 => array:2 [ "identificador" => "sec0085" "titulo" => "Funding" ] 10 => array:2 [ "identificador" => "sec0090" "titulo" => "Conflicts of interest" ] 11 => array:2 [ "identificador" => "xack276424" "titulo" => "Acknowledgements" ] 12 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2015-09-04" "fechaAceptado" => "2016-05-03" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec820702" "palabras" => array:3 [ 0 => "Honey" 1 => "Honey house" 2 => "Microbiological quality" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec820703" "palabras" => array:3 [ 0 => "Miel" 1 => "Sala de extracción" 2 => "Calidad microbiológica" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "The microbiological quality of honey obtained from different processing points and the environmental quality within honey houses were assessed in the Pampas Region (Argentina). Mold and yeast (MY), culturable heterotrophic mesophilic bacteria (CHMB), the number of spore-forming bacteria as well as the presence of Shigella spp., Salmonella spp. and fecal coliforms were evaluated in 163 samples. These samples were taken from eight honey houses. Results showed that 89 samples had ≤10CFU of MY/g honey, 69 ranged from 10 to 50CFU/g and two reached 65.5CFU/g. Eighty one percent of the samples showed ≤30CFU of CHMB/g honey and only seven samples had between 50 and 54.25CFU/g. Thirty six honey samples were obtained from drums: in 25 samples (69.4%) CHMB counts were less than ≤30CFU/g of honey; in 20 samples (55.5%) the values of MY were between 10 and 50CFU/g honey and total coliforms were only detected in 20 samples. Fecal coliforms, spores of clostridia as well as Salmonella spp. and Shigella spp were not detected and less than 50 spores of Bacillus spp. per g were observed in the honey from drums. Therefore, the microbiological honey quality within the honey houses did not show any sanitary risks. Our results were reported to honey house owners to help them understand the need to reinforce proper honey handling and sanitation practices." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "Este estudio evaluó la calidad microbiológica de la miel dentro de varias plantas de extracción de miel y la calidad del medio ambiente de las mismas en la Región Pampeana (Argentina). Se trabajó con 163 muestras de miel provenientes de 8 plantas de extracción. Se cuantificaron hongos y levaduras, bacterias aeróbicas mesófilas, bacterias esporuladas y esporas de clostridios. Asimismo, se determinó la presencia de Salmonella spp., Shigella spp. y coliformes fecales. Los resultados mostraron que por g de miel, 89 muestras tuvieron menos de 10UFC de hongos y levaduras, 69 tuvieron entre 10 y 50UFC y 2 alcanzaron 65,5UFC. Ochenta y uno por ciento de las muestras presentaron menos de 30UFC de bacterias aeróbicas mesófilas por g de miel mientras que solo 7 tuvieron entre 50 y 54,25UFC. Se obtuvieron 36 muestras de miel directamente de tambor: los conteos de bacterias aeróbicas mesófilas fueron≤30UFC/g de miel en 25 muestras (69,4%); los valores de hongos y levaduras estuvieron entre 10 y 50UFC en 20 muestras (55,5%) y solo se detectaron coliformes totales. No se observaron coliformes fecales, esporas de clostridios así como tampoco Salmonella spp. y Shigella spp. y se obtuvieron menos de 50 esporas de Bacillus spp./g en miel de los tambores. Se concluye que la calidad microbiológica de la miel en las plantas de extracción no presentó riesgo sanitario. Los resultados fueron entregados a los dueños de las mismas como aporte para que valoren la importancia de reforzar la aplicación de buenas prácticas de manejo y saneamiento." ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1248 "Ancho" => 1375 "Tamanyo" => 63756 ] ] "descripcion" => array:1 [ "en" => "Indoor air quality expressed by the number of molds and yeast (MY) and culturable heterotrophic mesophilic bacteria (CHMB) counts which were determined by the culture settling plate in two areas of honey houses during 2014 and 2015. Bars indicate standard deviation (SD)." ] ] 1 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">Section of the honey house \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col">Total of honey samples \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Culturable heterotrophic mesophilic bacteria</th><th class="td" title="table-head " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Yeast and Molds</th><th class="td" title="table-head " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Total coliforms</th></tr><tr title="table-row"><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Samples \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Counts \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Samples \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Counts \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Samples \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Counts \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry " rowspan="2" align="left" valign="middle">Honeycombs</td><td class="td" title="table-entry " rowspan="2" align="char" valign="middle">19</td><td class="td" title="table-entry " align="char" valign="top">17 (89.5)<a class="elsevierStyleCrossRef" href="#tblfn0005">a</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤30<a class="elsevierStyleCrossRef" href="#tblfn0010">b</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">19 (100) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">19 (100) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ND<a class="elsevierStyleCrossRef" href="#tblfn0015">c</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">2 (10.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">54.25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " rowspan="4" align="left" valign="top">Honeycomb uncapping</td><td class="td" title="table-entry " rowspan="4" align="char" valign="middle">29</td><td class="td" title="table-entry " align="char" valign="top">25 (86) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤30 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">17 (58.6) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">10–50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">25 (86) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ND \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">4 (14) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TNTC<a class="elsevierStyleCrossRef" href="#tblfn0020">d</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9 (31.0) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 (14) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">19 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 (6.9) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">65.5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 (3.4) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TNTC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " rowspan="3" align="left" valign="middle">Separation of honey from beeswax</td><td class="td" title="table-entry " rowspan="3" align="char" valign="middle">23</td><td class="td" title="table-entry " align="char" valign="top">15 (65.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤30 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15 (65) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">17 (74) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ND \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">8 (34.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TNTC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8 (35) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">10–50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5 (21.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">NC<a class="elsevierStyleCrossRef" href="#tblfn0025">e</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1 (4.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " rowspan="3" align="left" valign="middle">Honey extractor</td><td class="td" title="table-entry " rowspan="3" align="char" valign="middle">38</td><td class="td" title="table-entry " align="char" valign="top">33 (86.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤30 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">25 (65.8) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">29 (76.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ND \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">3 (7.9) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TNTC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">13 (34.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">10–50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9 (23.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">19 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">2 (5.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " rowspan="3" align="left" valign="middle">Honey sump</td><td class="td" title="table-entry " rowspan="3" align="char" valign="middle">18</td><td class="td" title="table-entry " align="char" valign="top">17 (94.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤30 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">11 (61.1) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">10–50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9 (50) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ND \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">1 (5.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TNTC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7 (38.9) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5 (27.7) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">NC \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4 (22.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">6 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " rowspan="3" align="left" valign="middle">Honey drum</td><td class="td" title="table-entry " rowspan="3" align="char" valign="middle">36</td><td class="td" title="table-entry " align="char" valign="top">25 (69.4) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤30 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">20 (55.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">10–50 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">25 (69.4) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">ND \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">8 (22.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TNTC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14 (38.9) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">≤10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">11 (30.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">NC \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">3 (8.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">52 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 (5.5) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">TNTC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1385775.png" ] ] ] "notaPie" => array:5 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "The percentage of samples in relation to the total of samples at the specific processing point within the honey house is given in parenthesis." ] 1 => array:3 [ "identificador" => "tblfn0010" "etiqueta" => "b" "nota" 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We also want to thank Juan Manuel Ringhetti for the donation of many culture media and Claudio Valverde from UNQ for his valuable comments on the manuscript.Microbiological quality of honey from the Pampas Region (Argentina) throughout the extraction process" "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/03257541/0000004900000001/v1_201704040030/S0325754116300864/v1_201704040030/en/main.assets" "Apartado" => array:4 [ "identificador" => "41740" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Microbiología de alimentos" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/03257541/0000004900000001/v1_201704040030/S0325754116300864/v1_201704040030/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0325754116300864?idApp=UINPBA00004N"]

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Calidad microbiológica de la miel en la Región Pampeana (Argentina) a lo largo del proceso de extracción

Leticia A. Fernándeza,c, Carolina Ghilardia,b, Betiana Hoffmanna, Carlos Bussoa,c, Liliana M. Galleza,

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labea@uns.edu.ar

Corresponding author.

a Laboratorio de Estudios Apícolas (LabEA-CIC), Departamento de Agronomía, Universidad Nacional del Sur, San Andrés 800, 8000 Bahía Blanca, Provincia de Buenos Aires, Argentina

b Laboratorio de Ecología, Departamento de Agronomía, Universidad Nacional del Sur, San Andrés 800, 8000 Bahía Blanca, Provincia de Buenos Aires, Argentina

c Consejo Nacional de Investigaciones Científicas y Técnicas de la República Argentina (CONICET), Buenos Aires, Argentina

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        "autoresLista" => "Leticia A&#46; Fern&#225;ndez, Carolina Ghilardi, Betiana Hoffmann, Carlos Busso, Liliana M&#46; Gallez"
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            "nombre" => "Liliana M&#46;"
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            "entidad" => "Laboratorio de Estudios Ap&#237;colas &#40;LabEA-CIC&#41;&#44; Departamento de Agronom&#237;a&#44; Universidad Nacional del Sur&#44; San Andr&#233;s 800&#44; 8000 Bah&#237;a Blanca&#44; Provincia de Buenos Aires&#44; Argentina"
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        "titulo" => "Calidad microbiol&#243;gica de la miel en la Regi&#243;n Pampeana &#40;Argentina&#41; a lo largo del proceso de extracci&#243;n"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Indoor air quality expressed by the number of molds and yeast &#40;MY&#41; and culturable heterotrophic mesophilic bacteria &#40;CHMB&#41; counts which were determined by the culture settling plate in two areas of honey houses during 2014 and 2015&#46; Bars indicate standard deviation &#40;SD&#41;&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">A honey house is a room or place within a building used for extracting&#44; processing and&#47;or handling honey&#46; It is the center of activities for beekeepers&#46; It represents an important portion of their investment&#44; and may contribute greatly to the overall efficiency of their entire operation<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">6</span></a>&#46; Due to the importance of Argentina&#39;s honey exports&#44; SENASA<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">33</span></a> passed resolution 870&#47;2006&#44; which deals with the hygienic and sanitary aspects of honey houses&#46; Thus&#44; commercial honeys are ruled by the Mercado Com&#250;n del Sur &#40;MERCOSUR&#41; legislation and the C&#243;digo Alimentario Argentino &#40;CAA&#41;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">3</span></a>&#46; The maximum level allowed by this legislation for molds and yeasts &#40;MY&#41; with trading purposes is 100<span class="elsevierStyleHsp" style=""></span>CFU<span class="elsevierStyleMonospace">&#47;</span>g of honey&#46; Likewise&#44; the legislation does not allow the presence of <span class="elsevierStyleItalic">Salmonella</span> and <span class="elsevierStyleItalic">Shigella</span> bacteria or of total coliforms in honeys&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Although honey has high osmolarity&#44; low water activity and nutrients&#44; it holds microorganisms which could be present in pollen&#44; dust&#44; air&#44; soil&#44; phyllosphere and nectar<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">11&#44;27&#44;35</span></a>&#46; It is well known that microbial contamination may be originated from food handlers&#44; equipment and cross-contamination during harvest<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">1</span></a>&#44; and processing in honey houses<a class="elsevierStyleCrossRefs" href="#bib0310"><span class="elsevierStyleSup">25&#44;35</span></a>&#46; Consequently&#44; appropriate standards of hygiene must be applied<a class="elsevierStyleCrossRefs" href="#bib0210"><span class="elsevierStyleSup">5&#44;37</span></a> in all operations involving honey handling&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">The microorganisms of concern in honey are some fungi and spore-forming bacteria such as <span class="elsevierStyleItalic">Bacillus cereus</span> and <span class="elsevierStyleItalic">Clostridium</span> spp&#46; which under certain conditions might cause illness in humans<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">35</span></a>&#46; Some of the most recognized potential sources of <span class="elsevierStyleItalic">Clostridium botulinum</span> spores are the soil&#44; dust&#44; honey and medicinal herbs<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">11</span></a>&#46; Sagua et al&#46;<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">31</span></a> observed that 456 cases of infant botulism in Argentina were reported between 1982 and 2007&#44; suggesting that some of these cases may be explained by the presence of <span class="elsevierStyleItalic">C&#46; botulinum</span> spores in honey&#46; Martins et al&#46;<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">19</span></a> found a low contamination percentage with <span class="elsevierStyleItalic">Bacillus cereus</span> and fungi in honeys from Portugal&#46; Nevertheless&#44; they suggested that these potentially pathogenic species could be harmful to predisposed patients&#46; Pirttijarvi et al&#46;<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">29</span></a> reported that the potential toxigenic effects of <span class="elsevierStyleItalic">Bacillus</span> were achieved with 10<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">4</span></a> spores per g of honey&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">Argentina is one of the major honey exporters to countries like the United States&#59; Germany and Japan&#46; There are currently about 25<span class="elsevierStyleHsp" style=""></span>000 beekeepers working with three million hives in Argentina&#46; This is the country with the largest number of hives in the Southern Hemisphere<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">8</span></a>&#46; Several works have been published about the microbiological characteristics of honeys ready to be sold in the retail market<a class="elsevierStyleCrossRefs" href="#bib0250"><span class="elsevierStyleSup">13&#44;14&#44;16&#44;17</span></a>&#46; However&#44; little scientific research on the microbiological quality of honey obtained at different processing points in honey houses has been published&#46; In Argentina&#44; Mouteira et al&#46;<a class="elsevierStyleCrossRefs" href="#bib0285"><span class="elsevierStyleSup">20&#8211;23</span></a>&#44; Basso et al&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">2</span></a> and Malacalza et al&#46;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">18</span></a> have studied possible sources of microbiological&#44; physical and chemical contamination as well as the effect of beekeeping equipment on honey production within the honey houses&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">In 2009<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">10</span></a>&#44; we started an evaluation of the sanitary risks during honey processing within the honey houses&#46; Mold and yeast&#44; total coliform number as well as the presence of <span class="elsevierStyleItalic">Salmonella</span> spp&#46; were determined in 50 samples<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">10</span></a>&#46; In this work&#44; we assessed the microbiological quality of honey obtained from different processing points&#44; and the environmental quality within honey houses&#44; to enlarge and complete that research&#46; Mold and yeast&#44; culturable heterotrophic mesophilic bacteria&#44; spore-forming bacteria and sulfite-reducing clostridia numbers&#44; and the presence of <span class="elsevierStyleItalic">Shigella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Salmonella</span> spp&#46; and fecal coliform were determined in 163 samples of honey obtained from eight honey houses in the southeastern Pampas Region&#44; Argentina&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Sampling sites</span><p id="par0030" class="elsevierStylePara elsevierViewall">Eight honey houses were sampled in the southeast of the Pampas Region&#44; Argentina&#46; This is the same region of the honey house sampled in 2009 by Gallez and Fern&#225;ndez<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">10</span></a>&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Honey was sampled at different points in each of the honey houses&#46; The first point was at the super storage place&#44; where supers are filled with the honeycombs&#46; The second one was at the uncapping machine&#44; which in all cases had thermostatically controlled heated blades&#46; The next point was at the honey-beeswax separator&#44; allowing to recover honey from the cappings&#46; Different uncapping systems&#44; with and without heating the cappings&#44; were sampled&#46; The fourth point was at the honey extractor which extracts the honey from the combs by centrifugal force&#46; The fifth point was at the honey sump&#44; which is a tank or chamber into which the honey drains&#46; In the Pampas Region&#44; it is usually below ground level&#44; and it is not water jacketed&#46; The last sampled point was at the 300<span class="elsevierStyleHsp" style=""></span>kg honey drums&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Honey samples</span><p id="par0040" class="elsevierStylePara elsevierViewall">One hundred and sixty three honey samples were collected during February and March 2014 and 2015 from eight honey houses&#46; All samples were aseptically collected in sterile 100<span class="elsevierStyleHsp" style=""></span>ml vials and were grouped according to their origin&#46; These samples were stored at room temperature and were processed within two months from collection<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">30</span></a>&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Microbial counts</span><p id="par0045" class="elsevierStylePara elsevierViewall">Microbial analyses were carried out in all of the samples in triplicate&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Mold and yeast &#40;MY&#41; determination was carried out by plating appropriate dilutions of the honey samples&#46; For this procedure&#44; a 10<span class="elsevierStyleHsp" style=""></span>g sample was homogenized in 90<span class="elsevierStyleHsp" style=""></span>ml of 0&#46;85&#37; w&#47;v NaCl &#40;initial suspension&#41; for 15<span class="elsevierStyleHsp" style=""></span>min at 180<span class="elsevierStyleHsp" style=""></span>rpm at room temperature&#46; Decimal serial dilutions were plated onto fungi and yeast agar supplemented with chloramphenicol &#40;Britania&#44; Argentina&#41; to inhibit bacteria&#46; MY were counted after three &#8211; five days from plate incubation at 22&#8211;24<span class="elsevierStyleHsp" style=""></span>&#176;C&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">For assessment of culturable heterotrophic mesophilic bacteria &#40;CHMB&#41;&#44; decimal serial dilutions from the initial suspension that was previously described&#44; were plated onto nutrient agar &#40;Britania&#44; Argentina&#41;&#46; Plates were counted 72<span class="elsevierStyleHsp" style=""></span>h after the incubation at 30<span class="elsevierStyleHsp" style=""></span>&#176;C&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">Total coliforms&#58; aliquots of 1<span class="elsevierStyleHsp" style=""></span>ml of the initial suspension were added to empty plastic Petri dishes&#46; Violet Red Bile Lactose &#40;VRBL&#44; Merck&#41; medium was poured over them&#46; The plates were incubated at 35&#8211;37<span class="elsevierStyleHsp" style=""></span>&#176;C for three days&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Results from all determinations were expressed as colony forming units &#40;CFU&#41;&#47;g of honey&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Complementary microbiological determinations</span><p id="par0070" class="elsevierStylePara elsevierViewall">The following microbial analyses were carried out in the samples coming from the honey drums&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Evaluation of <span class="elsevierStyleItalic">Bacillus</span> spp&#46;&#58; the second dilution was heat activated at 70&#47;80<span class="elsevierStyleHsp" style=""></span>&#176;C for 10<span class="elsevierStyleHsp" style=""></span>min&#44; and cooled immediately in iced water for another 10<span class="elsevierStyleHsp" style=""></span>min&#46; Aerobic spore-forming bacteria were plated on nutrient agar &#40;Britania&#44; Argentina&#41;&#46; Plates were incubated three days at 35<span class="elsevierStyleHsp" style=""></span>&#176;C&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Search for fecal coliforms&#58; one ml of the initial suspension &#40;10&#58;90&#41; for basic microbiological determinations was added to test tubes with brilliant green bile broth &#40;2&#37;&#41; with Durham tubes inverted inside and were incubated at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for two days&#46; Positive samples &#40;growth and gas production&#41; in this medium were selected to streak in Mac Conkey solid medium&#46; Suspicious colonies were isolated and placed in new tubes containing brilliant green bile broth &#40;2&#37;&#41; and inverted Durham tubes and were incubated at 44<span class="elsevierStyleHsp" style=""></span>&#176;C for two days&#46; Positive samples in this medium were reported as containing thermotolerant coliforms in 0&#46;1<span class="elsevierStyleHsp" style=""></span>g of honey&#46; To confirm the presence of <span class="elsevierStyleItalic">Escherichia coli</span>&#44; the positive tubes were tested by growth in EMB agar &#40;Britania&#41;&#46; Typical colony growth on EMB agar was confirmed by traditional assays including indole&#44; methyl red&#44; VP and citrate&#46; Results expressed as presence or absence of <span class="elsevierStyleItalic">E&#46; coli</span>&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Isolation of spores of sulfite-reducing clostridia&#58; aliquots of 25<span class="elsevierStyleHsp" style=""></span>ml of the initial suspension for basic microbiological determinations were added to empty tubes which were centrifuged for 15<span class="elsevierStyleHsp" style=""></span>min at 5000<span class="elsevierStyleHsp" style=""></span>rpm&#46; The pellet was thermally treated at 80<span class="elsevierStyleHsp" style=""></span>&#176;C for 5<span class="elsevierStyleHsp" style=""></span>min&#46; Then&#44; 100<span class="elsevierStyleHsp" style=""></span>&#956;l of this suspension was spread on plates with SPS &#40;sulfite&#8211;polymixin&#8211;sulfadiazine&#41; agar &#40;Bioclar&#44; Argentina&#41;&#44; and they were incubated anaerobically with the AnaeroPack&#8211;Anaero culture system &#40;Mitsubishi Gas Chemical&#44; Japan&#41; in a vacuum desiccator at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for 5 days&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Isolation of <span class="elsevierStyleItalic">Salmonella</span> spp&#46; and <span class="elsevierStyleItalic">Shigella</span> spp&#46;&#58; these bacteria were investigated according to a modification of the standard method suggested by the International Commission on Microbiological Specifications for Foods &#40;ICSMF&#41;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">12</span></a>&#46; For pre-enrichment&#44; 25<span class="elsevierStyleHsp" style=""></span>g of honey was added to 225<span class="elsevierStyleHsp" style=""></span>ml of peptone water &#40;Britania&#44; Argentina&#41; and cultures were incubated at 35<span class="elsevierStyleHsp" style=""></span>&#176;C for 24<span class="elsevierStyleHsp" style=""></span>h&#46; One ml of the pre-enrichment step was added to glass tubes containing selenite cystine broth &#40;42<span class="elsevierStyleHsp" style=""></span>&#176;C for 24<span class="elsevierStyleHsp" style=""></span>h&#41; and another one ml to glass tubes containing tetrathionate broth &#40;35<span class="elsevierStyleHsp" style=""></span>&#176;C for 24<span class="elsevierStyleHsp" style=""></span>h&#41;&#46; These enrichment steps were followed by the inoculation of selective solid media&#58; EMB&#44; salmonella shigella agar &#40;SSA&#41; and brilliant green agar &#40;BGA&#41;&#46; All media used were from Britania &#40;Argentina&#41;&#46; Petri dishes were incubated at 35<span class="elsevierStyleHsp" style=""></span>&#176;C for 48<span class="elsevierStyleHsp" style=""></span>h and suspected colonies of <span class="elsevierStyleItalic">Salmonella</span> were tested in triple sugar iron &#40;TSI&#44; Britania&#41; and lysine iron &#40;LIA&#44; Britania&#41; agar&#46; Colonies exhibiting typical reactions on TSI and LIA were purified and further characterized by traditional assays&#58; urease&#44; oxidase&#44; phenylalanine decarboxylase&#44; VP&#44; indole&#44; citrate and gelatin&#46; Results were expressed as presence or absence of <span class="elsevierStyleItalic">Salmonella</span> spp&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Environmental microbiological evaluation</span><p id="par0095" class="elsevierStylePara elsevierViewall">The honey house may contain various other facilities in addition to the extracting plant&#44; such as storage space for hive equipment and honey&#44; workshops&#44; office space&#44; and possibly a packing or salesroom or both<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">6</span></a>&#46; The research was conducted in the main extraction zone as well as in the other facilities&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">The culture settling plate technique&#44; also known as sedimentation technique&#44; was used for conducting a qualitative environmental assessment<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">32</span></a>&#46; For this purpose&#44; open Petri dishes filled with 20<span class="elsevierStyleHsp" style=""></span>ml of a microbiological culture medium suitable for bacteria and fungi were used as the sampling surface&#46; Fungi and yeast agar medium supplemented with chloramphenicol &#40;Britania&#44; Argentina&#41; was used in order to determine the number of MY while nutrient agar medium &#40;Britania&#44; Argentina&#41; was used for CHMB&#46; Petri dishes were distributed at the processing areas previously mentioned and exposed for about one hour within the honey house&#46; Once in the laboratory&#44; plates were incubated at 26&#8211;28<span class="elsevierStyleHsp" style=""></span>&#176;C for 5 days for MY and 30&#8211;35<span class="elsevierStyleHsp" style=""></span>&#176;C for 3 days for CHMB&#46; Results were expressed as CFU&#47;min&#46;</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Results</span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Microbial counts at different points of honey processing within the honey house</span><p id="par0105" class="elsevierStylePara elsevierViewall">Similar results were obtained for all microbiological determinations within all the studied honey houses during 2014 and 2015 &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0110" class="elsevierStylePara elsevierViewall">Eighty nine samples out of 163 had &#8804;10<span class="elsevierStyleHsp" style=""></span>CFU per g of honey of MY&#44; 69 samples ranged from 10 to 50<span class="elsevierStyleHsp" style=""></span>CFU&#47;g of honey&#44; and two reached 65&#46;5<span class="elsevierStyleHsp" style=""></span>CFU<span class="elsevierStyleMonospace">&#47;</span>g of honey&#46; Eighty one percent of the samples showed &#8804;30<span class="elsevierStyleHsp" style=""></span>CFU of CHMB&#47;g of honey&#44; while only seven samples had between 50 and 54&#46;25<span class="elsevierStyleHsp" style=""></span>CFU<span class="elsevierStyleMonospace">&#47;</span>g&#46; Total coliforms were different between the two harvesting periods&#46; In 2014&#44; 20 &#40;35&#37;&#41; out of 57 samples had total coliforms&#44; in which the count was less than 20<span class="elsevierStyleHsp" style=""></span>CFU<span class="elsevierStyleMonospace">&#47;</span>g of honey&#46; In 2015&#44; total coliforms were not detected in samples taken from different points of the honey house&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Microbiological quality of the honey from drums</span><p id="par0115" class="elsevierStylePara elsevierViewall">Thirty-six samples of honey were obtained from drums in the different honey houses&#46; In 25 samples &#40;69&#46;4&#37;&#41;&#44; the counts of CHMB were less than &#8804;30<span class="elsevierStyleHsp" style=""></span>CFU per g of honey&#46; In addition&#44; 20 samples &#40;55&#46;5&#37;&#41; showed between 10 and 50<span class="elsevierStyleHsp" style=""></span>CFU of MY per g of honey &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Total coliforms were not detected in 25 samples&#44; while colonies different from the typical morphology of coliforms were only observed in 11 samples&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">Fecal coliforms were not detected in samples from 2014 or 2015&#46; All samples were contaminated with less than 50<span class="elsevierStyleHsp" style=""></span>spores&#47;g of <span class="elsevierStyleItalic">Bacillus</span> spp&#46;&#44; except two from 2014 which showed between 50 and 100 spores&#46; Typical black colonies from spores of sulfite-reducing clostridia were not detected in any sample when working under a total anaerobic atmosphere&#46; In addition&#44; bacteria from the genera <span class="elsevierStyleItalic">Salmonella</span> spp&#46; <span class="elsevierStyleItalic">Shigella</span> spp&#46; were not found in any of the honey drum samples&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Microbiological quality of the honey house environment</span><p id="par0125" class="elsevierStylePara elsevierViewall">There were no statistical differences in MY and CHMB counts between the rooms&#47;areas of the main extraction zone and other rooms&#47;areas of the honey houses &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0130" class="elsevierStylePara elsevierViewall">Microorganisms in honey might come from several and different sources&#46; Primary sources include pollen&#44; digestive tracts of honey bees&#44; dust&#44; air&#44; soil and nectar&#46; Secondary sources are due to honey handlers and processing&#44; and are easy to control by the application of good manufacturing practices &#40;GMP&#41;<a class="elsevierStyleCrossRefs" href="#bib0200"><span class="elsevierStyleSup">3&#44;11&#44;15</span></a>&#46; In this work&#44; we report the analysis of 163 honey samples which were obtained from different points of the honey processing within eight honey houses located in the southeast of the Pampas Region&#44; Argentina&#46; Our studies started in 2009 with 50 samples from one honey house<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">10</span></a>&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">We did not find any differences in microbial counts at the different points of honey processing among the eight honey houses sampled&#46; Therefore&#44; the results are discussed according to the six points we sampled within the honey house &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; In 2009&#44; all samples from honeycombs and honey extractor samples showed low levels of MY &#40;&#8804;10<span class="elsevierStyleHsp" style=""></span>CFU&#47;g of honey&#41;&#46; Low levels of MY and CHMB were also observed at those processing points and in the honey obtained from the uncapping machines &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Ten to 50<span class="elsevierStyleHsp" style=""></span>CFU of MY<span class="elsevierStyleMonospace">&#47;</span>g honey were observed in four out of 30 samples in 2009<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">10</span></a> &#40;13&#46;3&#37;&#41;&#44; whereas 69 out of 163 samples were obtained with those counts in 2014&#47;2015 &#40;42&#46;3&#37;&#41;&#46; These samples belonged to the following processing points&#58; honeycomb uncapping&#44; honey sump and honey drum&#46; The higher MY counts in 2014&#47;2015 than in 2009 might be due to higher rainfall&#44; thus favoring microorganism development&#46; In addition&#44; total coliforms were present only in 11&#46;65&#37; of the samples in 2014&#44; while there were no total coliforms in honey samples during 2009 and 2015&#46; However&#44; it is important to note that the food codes refer to honey for retail sale&#44; at the end point of the food chain&#46; Drums were the last sampling point in this study&#44; previous to bottling&#44; and total coliforms were absent in all the drum samples&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">Little information is available in Argentina about microbiological contamination within the honey houses&#46; Mouteira and Basso &#40;2014&#41;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">24</span></a> studied four points in a honey house of Ranchos in Buenos Aires Province&#46; They reported counts of MY of 97<span class="elsevierStyleHsp" style=""></span>CFU<span class="elsevierStyleMonospace">&#47;</span>g honey in honeycombs&#44; 75<span class="elsevierStyleHsp" style=""></span>CFU&#47;g honey in honeycomb uncapping&#44; 35<span class="elsevierStyleHsp" style=""></span>CFU&#47;g honey in honey extractor and 34&#46;7<span class="elsevierStyleHsp" style=""></span>CFU&#47;g honey in drums&#46; They also observed the absence of total coliforms&#46; In another work&#44; Mouteira et al&#46;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">21</span></a> compared the physicochemical and microbiological quality of honeys from two honey house buildings with different technology in Argentina&#46; They found that although MY counts were below the maximum established limit by the CAA<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">3</span></a> &#40;&#8804;100<span class="elsevierStyleHsp" style=""></span>CFU&#47;g of honey&#41;&#44; their number increased in all the studied processing points of the honey house which did not comply with GMP regulations&#46; They also observed 19&#46;87<span class="elsevierStyleHsp" style=""></span>coliforms&#47;g of honey in the drums in this honey house&#46; Furthermore&#44; Sereia et al&#46;<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">34</span></a> compared and verified the main contamination sources and the hygienic&#47;sanitary conditions of organic honey from Parana River islands &#40;Brasil&#41;&#46; These authors conclusively demonstrated that secondary sources of contamination were responsible for the reduction in the quality of organic honey&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">The maximum MY level allowed for trading by the MERCOSUR and CAA<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">3</span></a> legislations is 100<span class="elsevierStyleHsp" style=""></span>CFU&#47;g of honey&#58; all drum samples showed cell counts below this stipulated value &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Likewise&#44; the legislation neither allows the presence of <span class="elsevierStyleItalic">Salmonella</span> and <span class="elsevierStyleItalic">Shigella</span> bacteria nor of total coliforms&#46; All the honey drum samples in our work showed these characteristics&#46; Our results of the microbiological quality of honey at the end of the process in the honey house were similar to those reported by other authors in Argentina<a class="elsevierStyleCrossRefs" href="#bib0230"><span class="elsevierStyleSup">9&#44;13&#44;20</span></a>&#46; In fact&#44; our results are also similar to those published by other researchers who analyzed honey from different parts of the world<a class="elsevierStyleCrossRefs" href="#bib0220"><span class="elsevierStyleSup">7&#44;26&#44;36</span></a>&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">In the present study&#44; we assessed the indoor air quality at the honey houses by the settling plate technique&#46; It is interesting to note&#44; that although there were no statistical differences of MY and CHMB counts between both studied areas&#44; there was a tendency in both groups of microorganisms to be lower in the main extraction zone than in other rooms&#47;areas&#46; Similarly&#44; Oliveira et al&#46;<a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">28</span></a> found that the installation of honey houses in untidy environments&#44; and the environmental variables&#44; could have been responsible for the presence of MY in quantities above those permitted by the standards&#46; Furthermore&#44; Grabowski and Klein<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">11</span></a> supported this idea explaining that like any other foodstuff&#44; the hygienic status of honey is the result of the environmental conditions along the food chain&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">The &#8220;unheated&#8221; honey-wax separation process might be better to preserve the chemical quality of the honey&#46; However and in accordance with our previous data&#44; it implied a higher microbiological hazard than the heated process&#46; This highlights the need to perform more studies in the honey house in this regard<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">10</span></a>&#46; In this research&#44; we characterized honey samples from eight honey houses&#59; the different points of honey processing within these honey houses in the Pampas Region did not show any sanitary risks&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">Some simple good practices are not always applied&#44; and their implementation could improve the microbiological quality of the honey&#46; For instance&#44; workers should wear clean outer clothing and adequate hair covering at all times during honey extraction and processing&#46; Sanitary curtains and insect nets should be fitted over openings to reduce environmental contamination and to avoid bees from entering&#46; Sumps must be adequately covered&#46; While not in use&#44; the equipment must be stored protecting it from dust&#44; dirt&#44; rodents&#44; insects or other contamination sources&#46; The application and&#47;or reinforcement of proper honey handling and sanitation practices would allow to improve the microbiological quality of honeys&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Ethical responsibilities</span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Protection of human and animal subjects</span><p id="par0165" class="elsevierStylePara elsevierViewall">The authors declare that no experiments were performed on humans or animals for this study&#46;</p></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Confidentiality of data</span><p id="par0170" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Right to privacy and informed consent</span><p id="par0175" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span></span><span id="sec0085" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Funding</span><p id="par0180" class="elsevierStylePara elsevierViewall">We thank the Comisi&#243;n de Investigaciones Cient&#237;ficas de la Provincia de Buenos Aires &#40;CIC&#41; Argentina&#44; for financial support&#46;</p></span><span id="sec0090" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Conflicts of interest</span><p id="par0185" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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              "titulo" => "Microbial counts at different points of honey processing within the honey house"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The microbiological quality of honey obtained from different processing points and the environmental quality within honey houses were assessed in the Pampas Region &#40;Argentina&#41;&#46; Mold and yeast &#40;MY&#41;&#44; culturable heterotrophic mesophilic bacteria &#40;CHMB&#41;&#44; the number of spore-forming bacteria as well as the presence of <span class="elsevierStyleItalic">Shigella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Salmonella</span> spp&#46; and fecal coliforms were evaluated in 163 samples&#46; These samples were taken from eight honey houses&#46; Results showed that 89 samples had &#8804;10<span class="elsevierStyleHsp" style=""></span>CFU of MY<span class="elsevierStyleMonospace">&#47;</span>g honey&#44; 69 ranged from 10 to 50<span class="elsevierStyleHsp" style=""></span>CFU&#47;g and two reached 65&#46;5<span class="elsevierStyleHsp" style=""></span>CFU&#47;g&#46; Eighty one percent of the samples showed &#8804;30<span class="elsevierStyleHsp" style=""></span>CFU of CHMB<span class="elsevierStyleMonospace">&#47;</span>g honey and only seven samples had between 50 and 54&#46;25<span class="elsevierStyleHsp" style=""></span>CFU<span class="elsevierStyleMonospace">&#47;</span>g&#46; Thirty six honey samples were obtained from drums&#58; in 25 samples &#40;69&#46;4&#37;&#41; CHMB counts were less than &#8804;30<span class="elsevierStyleHsp" style=""></span>CFU&#47;g of honey&#59; in 20 samples &#40;55&#46;5&#37;&#41; the values of MY were between 10 and 50<span class="elsevierStyleHsp" style=""></span>CFU&#47;g honey and total coliforms were only detected in 20 samples&#46; Fecal coliforms&#44; spores of clostridia as well as <span class="elsevierStyleItalic">Salmonella</span> spp&#46; and <span class="elsevierStyleItalic">Shigella</span> spp were not detected and less than 50 spores of <span class="elsevierStyleItalic">Bacillus</span> spp&#46; per g were observed in the honey from drums&#46; Therefore&#44; the microbiological honey quality within the honey houses did not show any sanitary risks&#46; Our results were reported to honey house owners to help them understand the need to reinforce proper honey handling and sanitation practices&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Este estudio evalu&#243; la calidad microbiol&#243;gica de la miel dentro de varias plantas de extracci&#243;n de miel y la calidad del medio ambiente de las mismas en la Regi&#243;n Pampeana &#40;Argentina&#41;&#46; Se trabaj&#243; con 163 muestras de miel provenientes de 8 plantas de extracci&#243;n&#46; Se cuantificaron hongos y levaduras&#44; bacterias aer&#243;bicas mes&#243;filas&#44; bacterias esporuladas y esporas de clostridios&#46; Asimismo&#44; se determin&#243; la presencia de <span class="elsevierStyleItalic">Salmonella</span> spp&#46;&#44; <span class="elsevierStyleItalic">Shigella</span> spp&#46; y coliformes fecales&#46; Los resultados mostraron que por g de miel&#44; 89 muestras tuvieron menos de 10<span class="elsevierStyleHsp" style=""></span>UFC de hongos y levaduras&#44; 69 tuvieron entre 10 y 50<span class="elsevierStyleHsp" style=""></span>UFC y 2 alcanzaron 65&#44;5<span class="elsevierStyleHsp" style=""></span>UFC&#46; Ochenta y uno por ciento de las muestras presentaron menos de 30<span class="elsevierStyleHsp" style=""></span>UFC de bacterias aer&#243;bicas mes&#243;filas por g de miel mientras que solo 7 tuvieron entre 50 y 54&#44;25<span class="elsevierStyleHsp" style=""></span>UFC&#46; Se obtuvieron 36 muestras de miel directamente de tambor&#58; los conteos de bacterias aer&#243;bicas mes&#243;filas fueron<span class="elsevierStyleHsp" style=""></span>&#8804;<span class="elsevierStyleHsp" style=""></span>30<span class="elsevierStyleHsp" style=""></span>UFC&#47;g de miel en 25 muestras &#40;69&#44;4&#37;&#41;&#59; los valores de hongos y levaduras estuvieron entre 10 y 50<span class="elsevierStyleHsp" style=""></span>UFC en 20 muestras &#40;55&#44;5&#37;&#41; y solo se detectaron coliformes totales&#46; No se observaron coliformes fecales&#44; esporas de clostridios as&#237; como tampoco <span class="elsevierStyleItalic">Salmonella</span> spp&#46; y <span class="elsevierStyleItalic">Shigella</span> spp&#46; y se obtuvieron menos de 50 esporas de <span class="elsevierStyleItalic">Bacillus</span> spp&#46;&#47;g en miel de los tambores&#46; Se concluye que la calidad microbiol&#243;gica de la miel en las plantas de extracci&#243;n no present&#243; riesgo sanitario&#46; Los resultados fueron entregados a los due&#241;os de las mismas como aporte para que valoren la importancia de reforzar la aplicaci&#243;n de buenas pr&#225;cticas de manejo y saneamiento&#46;</p></span>"
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                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td-with-role" title="table-head ; entry_with_role_rowhead " align="left" valign="top" scope="col">Section of the honey house&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col">Total of honey samples&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Culturable heterotrophic mesophilic bacteria</th><th class="td" title="table-head  " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Yeast and Molds</th><th class="td" title="table-head  " colspan="2" align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Total coliforms</th></tr><tr title="table-row"><th class="td" title="table-head  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="" valign="top" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Samples&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Counts&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Samples&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Counts&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Samples&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="center" valign="top" scope="col" style="border-bottom: 2px solid black">Counts&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry  " rowspan="2" align="left" valign="middle">Honeycombs</td><td class="td" title="table-entry  " rowspan="2" align="char" valign="middle">19</td><td class="td" title="table-entry  " align="char" valign="top">17 &#40;89&#46;5&#41;<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;30<a class="elsevierStyleCrossRef" href="#tblfn0010"><span class="elsevierStyleSup">b</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">19 &#40;100&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">19 &#40;100&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">ND<a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">c</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">2 &#40;10&#46;5&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">54&#46;25&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " rowspan="4" align="left" valign="top">Honeycomb uncapping</td><td class="td" title="table-entry  " rowspan="4" align="char" valign="middle">29</td><td class="td" title="table-entry  " align="char" valign="top">25 &#40;86&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;30&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">17 &#40;58&#46;6&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">10&#8211;50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">25 &#40;86&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">ND&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">4 &#40;14&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TNTC<a class="elsevierStyleCrossRef" href="#tblfn0020"><span class="elsevierStyleSup">d</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">9 &#40;31&#46;0&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4 &#40;14&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">19&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2 &#40;6&#46;9&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">65&#46;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1 &#40;3&#46;4&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TNTC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " rowspan="3" align="left" valign="middle">Separation of honey from beeswax</td><td class="td" title="table-entry  " rowspan="3" align="char" valign="middle">23</td><td class="td" title="table-entry  " align="char" valign="top">15 &#40;65&#46;2&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;30&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">15 &#40;65&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">17 &#40;74&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">ND&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">8 &#40;34&#46;8&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TNTC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">8 &#40;35&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">10&#8211;50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5 &#40;21&#46;7&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">NC<a class="elsevierStyleCrossRef" href="#tblfn0025"><span class="elsevierStyleSup">e</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1 &#40;4&#46;3&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " rowspan="3" align="left" valign="middle">Honey extractor</td><td class="td" title="table-entry  " rowspan="3" align="char" valign="middle">38</td><td class="td" title="table-entry  " align="char" valign="top">33 &#40;86&#46;8&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;30&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">25 &#40;65&#46;8&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">29 &#40;76&#46;3&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">ND&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">3 &#40;7&#46;9&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TNTC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">13 &#40;34&#46;2&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">10&#8211;50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">9 &#40;23&#46;7&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">19&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">2 &#40;5&#46;3&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " rowspan="3" align="left" valign="middle">Honey sump</td><td class="td" title="table-entry  " rowspan="3" align="char" valign="middle">18</td><td class="td" title="table-entry  " align="char" valign="top">17 &#40;94&#46;5&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;30&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">11 &#40;61&#46;1&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">10&#8211;50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">9 &#40;50&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">ND&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">1 &#40;5&#46;5&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TNTC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">7 &#40;38&#46;9&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5 &#40;27&#46;7&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">NC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4 &#40;22&#46;2&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " rowspan="3" align="left" valign="middle">Honey drum</td><td class="td" title="table-entry  " rowspan="3" align="char" valign="middle">36</td><td class="td" title="table-entry  " align="char" valign="top">25 &#40;69&#46;4&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;30&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">20 &#40;55&#46;5&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">10&#8211;50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">25 &#40;69&#46;4&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">ND&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">8 &#40;22&#46;2&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TNTC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">14 &#40;38&#46;9&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8804;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">11 &#40;30&#46;5&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">NC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="char" valign="top">3 &#40;8&#46;3&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">52&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2 &#40;5&#46;5&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">TNTC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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              "identificador" => "tblfn0005"
              "etiqueta" => "a"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0005">The percentage of samples in relation to the total of samples at the specific processing point within the honey house is given in parenthesis&#46;</p>"
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            1 => array:3 [
              "identificador" => "tblfn0010"
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              "nota" => "<p class="elsevierStyleNotepara" id="npar0010">The results from all of the determinations in each section of the honey house were expressed as colony forming units per gram of honey &#40;CFU&#47;g&#41;&#46;</p>"
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            2 => array:3 [
              "identificador" => "tblfn0015"
              "etiqueta" => "c"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0015">ND&#44; not detected&#46;</p>"
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              "identificador" => "tblfn0025"
              "etiqueta" => "e"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0025">NC&#44; no coliform&#46;</p>"
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          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Basic microbiological determinations in 163 samples of honey obtained from different processing points in eight honey houses in 2014 and 2015</p>"
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    ]
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      "titulo" => "References"
      "seccion" => array:1 [
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          "identificador" => "bibs0005"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Effects of harvesting methods on physicochemical and microbial qualities of honey"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "G&#46;O&#46; Babarinde"
                            1 => "S&#46;A&#46; Babarinde"
                            2 => "D&#46;O&#46; Adegbola"
                            3 => "S&#46;I&#46; Ajayeoba"
                          ]
                        ]
                      ]
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                    0 => array:2 [
                      "doi" => "10.1007/s13197-011-0329-9"
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                        "tituloSerie" => "J Food Sci Technol"
                        "fecha" => "2011"
                        "volumen" => "48"
                        "paginaInicial" => "628"
                        "paginaFinal" => "634"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/23572798"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
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            1 => array:3 [
              "identificador" => "bib0195"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Evaluaci&#243;n de las condiciones higi&#233;nicas de una sala de extracci&#243;n con placas de contacto irradiadas"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:4 [
                            0 => "I&#46;M&#46; Basso"
                            1 => "M&#46;E&#46; Pawlak"
                            2 => "A&#46; Buj&#225;n"
                            3 => "M&#46;C&#46; Mouteira"
                          ]
                        ]
                      ]
                    ]
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                  "host" => array:1 [
                    0 => array:1 [
                      "LibroEditado" => array:3 [
                        "titulo" => "37&#176; Congreso de la Asoc&#46; Argentina de Producci&#243;n Animal &#8211; RAPA&#44; vol&#46; xy&#44; Suppl&#46; 1"
                        "conferencia" => "Balcarce&#44; Provincia de Buenos Aires&#44; Argentina"
                        "serieFecha" => "2014"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            2 => array:3 [
              "identificador" => "bib0200"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:1 [
                  "referenciaCompleta" => "CAA&#46; C&#243;digo Alimentario Argentino&#46; <a href="http://www.alimentosargentinos.gov.ar/contenido/marco/capitulospdf/Capitulo_X">www&#46;alimentosargentinos&#46;gov&#46;ar&#47;contenido&#47;marco&#47;capitulospdf&#47;Capitulo&#95;X</a> &#91;accessed 04&#46;08&#46;15&#93;&#46;"
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            3 => array:3 [
              "identificador" => "bib0205"
              "etiqueta" => "4"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Caracter&#237;sticas microbiol&#243;gicas de la miel revisi&#243;n bibliogr&#225;fica"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "F&#46; Coll Cardenas"
                            1 => "C&#46; Villat"
                            2 => "G&#46; Laporte"
                            3 => "M&#46; Noia"
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Article information

ISSN: 03257541
Original language: English

DOI:10.1016/j.ram.2016.05.010

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2023 May	50	9	59
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2023 March	77	6	83
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2022 December	45	12	57
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2022 October	21	13	34
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2022 June	12	14	26
2022 May	25	10	35
2022 April	28	10	38
2022 March	35	12	47
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2022 January	37	9	46
2021 December	37	7	44
2021 November	11	8	19
2021 October	29	13	42
2021 September	15	9	24
2021 August	12	5	17
2021 July	17	8	25
2021 June	25	6	31
2021 May	25	4	29
2021 April	36	18	54
2021 March	20	5	25
2021 February	12	11	23
2021 January	12	16	28
2020 December	15	9	24
2020 November	19	4	23
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2020 September	16	10	26
2020 August	18	8	26
2020 July	16	3	19
2020 June	22	12	34
2020 May	13	4	17
2020 April	18	6	24
2020 March	16	10	26
2020 February	14	9	23
2020 January	9	6	15
2019 December	20	6	26
2019 November	6	6	12
2019 October	12	7	19
2019 September	10	4	14
2019 August	8	1	9
2019 July	11	6	17
2019 June	19	4	23
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2019 March	2	2	4
2019 February	7	4	11
2019 January	9	1	10
2018 December	9	3	12
2018 November	10	6	16
2018 October	4	17	21
2018 September	18	3	21
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2018 July	11	15	26
2018 June	9	6	15
2018 May	32	3	35
2018 April	87	6	93
2018 March	4	1	5
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2018 January	7	1	8
2017 December	4	0	4
2017 November	8	5	13
2017 October	9	6	15
2017 September	4	6	10
2017 August	12	14	26
2017 July	10	6	16
2017 June	16	18	34
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