The distribution of staphylococci in bioaerosols from red-meat abattoirs.Introduction Contamination of foodstuffs foodstuffs npl → comestibles mpl foodstuffs npl → denrées fpl alimentaires foodstuffs food npl → via the air is generally caused by viable airborne contaminants airborne contaminants, n.pl materials in the atmosphere that can affect the health of persons in the same or a nearby environment. Also referred to as air pollution. originating from biological sources (bioaerosols) (Lutgring, Linton, Zimmerman, Peugh, & Heber, 1997; Whyte, Collins, McGill, Monahan, & O'Mahony, 2001). Bioaerosols can be liquid or solid, or can be carried on another particle or suspended in a liquid droplet droplet very small drop of fluid. droplet nuclei the finite particles of matter which are transmitted from animal to animal. , and may comprise bacterial spores, cells, fungi, fungal spores, antigens, viruses, plant pollens, toxins, fecal material, or a combination of these (Cundith, Kerth, Jones, McCaskey, & Kuhlers, 2002; Rad-more, 1986; Whyte et al., 2001). When all these substances are distributed in the air, they can serve as a feasible route for food contamination and can ultimately affect the health of both food handlers and consumers (Lutgring et al., 1997). Information on the bioaerosol contamination of food-processing plants is, however, very limited, mainly because of lack of proper equipment, lack of expertise to perform bioaerosol surveys, fear of how the outcomes of such studies will affect various companies, or some combination of these factors. As a result, knowledge of the contribution of the airborne micro-biota to the contamination of food products remains limited. Although indoor air environments are considered to be protective, they become contaminated contaminated, v 1. made radioactive by the addition of small quantities of radioactive material. 2. made contaminated by adding infective or radiographic materials. 3. an infective surface or object. with various particles that can be hazardous when concentrations exceed recommended maximum limits: 1,000 CFUs/[m.sup.3] for total number of bioaerosol particles, a limit set by the National Institute of Occupational Safety and Health The National Institute for Occupational Safety and Health (NIOSH) is the federal agency responsible for conducting research and making recommendations for the prevention of work-related injury and illness. and the American Conference of Governmental Industrial Hygienists ACGIH® advances worker protection by providing timely, objective, scientific information to occupational and environmental health professionals. History The independent National Conference of Governmental Industrial Hygienists (NCGIH) convened on June 27, 1938, in Washington, D. (ACGIH ACGIH American Conference of Governmental Industrial Hygienists, Inc. ), with the culturable count for total bacteria not to exceed 500 CFUs/[m.sup.3] (Cox & Wathes, 1995; Jensen & Schafer, 1998; Kalogerakis et al., 2005). A number of authors have recognized poor ventilation systems as possible reservoirs that may distribute bioaerosols in meat-processing plants (Cundith et al., 2002; Whyte et al., 2001). In addition, employees may distribute contaminants through clothes, skin, hair, respiratory tract respiratory tract n. The air passages from the nose to the pulmonary alveoli, including the pharynx, larynx, trachea, and bronchi. Respiratory tract (coughing and sneezing To verbally tell somebody about a new and interesting Web site. See viral marketing. ), fecal matter, and poor hygiene (Chambers, 2001; Cundith et al., 2002; Lutgring et al., 1997). Food handlers are the primary sources of indoor bioaerosols in the food industry, according to according to prep. 1. As stated or indicated by; on the authority of: according to historians. 2. In keeping with: according to instructions. 3. Nel and co-authors (Nel, Lues lues /lu·es/ (loo´ez) syphilis.luet´ic lu·es n. pl. lues Syphilis. lu·et , Buys, & Venter venter /ven·ter/ (ven´ter) pl. ven´tres [L.] 1. a fleshy contractile part of a muscle. 2. abdomen. 3. a hollowed part or cavity. ven·ter n. , 2004). Furthermore, airborne microorganisms may be of human origin from purulent pu·ru·lent adj. Containing, discharging, or causing the production of pus. Purulent Consisting of or containing pus Mentioned in: Lacrimal Duct Obstruction purulent containing or forming pus. discharges of an infected finger or eye; from abscesses, facial eruptions, or nasopharyngeal nasopharyngeal pertaining to the nasal and pharyngeal cavities. nasopharyngeal meatus see nasopharyngeal meatus. nasopharyngeal spasm see reverse sneeze. secretions; or from normal skin (Zadoks et al., 2002). Other sources that are indirectly related to bioaerosols are contaminants from waste handling and disposal, fungal or microbial microbial pertaining to or emanating from a microbe. microbial digestion the breakdown of organic material, especially feedstuffs, by microbial organisms. growth niches in the building, and unsanitary un·san·i·tar·y adj. Not sanitary. practices, including improper maintenance and poor operating and sanitation. In addition, seasonal and weather-related factors such as geographical location are also known to influence bioaerosols within food-processing environments such as abattoirs (Chang, Chung, Huang, & Su, 2001; Cundith et al., 2002; Lutgring et al., 1997; Pastuszka, Kyaw Thaw Paw, Lis, Wlazlo, & Ulfig, 2000; Ren & Frank, 1992). Some of the pathogenic bacteria Pathogenic bacteria Bacteria that produce illness. Mentioned in: Gastroenteritis most predominantly found in indoor bioaerosols are members of the Staphylococcus staphylococcus (stăf'ələkŏk`əs), any of the pathogenic bacteria, parasitic to humans, that belong to the genus Staphylococcus. The spherical bacterial cells (cocci) typically occur in irregular clusters [Gr. genus because of their ubiquitous nature (Wieser & Busse, 2000). This genus occurs naturally on the skin, as well as on the skin glands and mucous membranes Mucous membranes The inner tissue that covers or lines body cavities or canals open to the outside, such as nose and mouth. These membranes secrete mucus and absorb water and salts. Mentioned in: Leprosy, Pulmonary Fibrosis, Topical Anesthesia of warm-blooded animals (Nagase et al., 2002a; Nagase et al., 2002b; Wieser & Busse, 2000). Staphylococcus aureus Staphylococcus au·re·us n. A bacterium that causes furunculosis, pyemia, osteomyelitis, suppuration of wounds, and food poisoning. Staphylococcus aureus Staphylococcus pyogenes bacteria constitute about 10 percent of the nasal cavity nasal cavity n. The cavity on either side of the nasal septum, extending from the nares to the pharynx, and lying between the floor of the cranium and the roof of the mouth. nasal cavity, n See cavity, nasal. bacteria of healthy humans and occur at levels between 0.01 and 0.1 CFUs/[m.sup.3] in the environment (Sheretz, Bassetti, & Bassetti-Wyss, 2001). Because of their ubiquitous occurrence in nature, staphylococci staph·y·lo·coc·cus n. pl. staph·y·lo·coc·ci A spherical gram-positive parasitic bacterium of the genus Staphylococcus, usually occurring in grapelike clusters and causing boils, septicemia, and other infections. have been isolated from fresh water, meat, milk, cheese, soil, seawater seawater Water that makes up the oceans and seas. Seawater is a complex mixture of 96.5% water, 2.5% salts, and small amounts of other substances. Much of the world's magnesium is recovered from seawater, as are large quantities of bromine. , dust, and the air (Nel, Lues, Buys, & Venter, 2003; Wieser & Busse, 2000). Although extensive literature exists on the quality and safety of meat, milk, cheese and water, little information, as mentioned before, is available on the microbiological aspects of indoor air associated with red-meat abattoirs (Pastuszka et al., 2000). The majority of the larger red-meat abattoirs have deboning rooms for the removal of retail cuts from the carcasses. During this stage the product undergoes extensive handling and exposure to surfaces and utensils (Nel et al., 2003). As a result, deboning rooms are prone to several factors that can contribute to the distribution of airborne staphylococci. These include 1) conveyer systems and cutting tables; 2) movement and actions of food handlers, especially through breathing, speaking, sneezing, or coughing; 3) water drains and splashing caused during high-pressure water washing of the floor; 4) the ventilation system; and 5) workers' hands or gloves (Ren & Frank, 1992). The aim of the study reported here was to quantify the airborne staphylococci and total viable counts in the deboning rooms of selected South African red-meat abattoirs of various sizes and throughput rates. The staphylococci species found in the air are described in general and S. aureus The aureus (pl. aurei) was a gold coin of ancient Rome valued at 25 silver denarii. The aureus was regularly issued from the 1st century BC to the beginning of the 4th century AD, when it was replaced by the solidus. coagulase coagulase /co·ag·u·lase/ (-las) an antigenic substance of bacterial origin, produced by staphylococci, which may be causally related to thrombus formation. co·ag·u·lase n. types in particular were assessed in order to shed light on the airborne distribution of these microorganisms. The authors make suggestions about the role of the air environment as a vector of staphylococci contamination. Materials and Methods Sampling Site Bioaerosol samples were collected from four differently graded South African red-meat abattoirs (A, B, C, and D) in the Free State Province according to the old South African System (Van Zyl van Zyl is an Afrikaans surname, and may refer to:
Sampling Procedure During each sampling interval, samples were aseptically collected once an hour from various locations in the deboning room for a period of five hours. They were collected an hour after the beginning of the working shift, and sampling time was based on the busy hours of the morning, when only beef is processed. The majority of the abattoirs continue to process other meat species after the first six hours of the day Samples were collected with a single-stage microbial air sampler (SAS (1) (SAS Institute Inc., Cary, NC, www.sas.com) A software company that specializes in data warehousing and decision support software based on the SAS System. Founded in 1976, SAS is one of the world's largest privately held software companies. See SAS System. Super 90) (Chang et al., 2001; Clark, Rylander, & Larson, 1983; Cornier, Tremblay, Miriaux, Brochu, & Lovoie, 1990; Donham, Haglind, Perterson, Rylander, & Belin, 1989; Donham, Popendorf, Palmgren, & Larson, 1986; Haglind & Rylander, 1987; Heedrich, Brouwer, Biersteker, & Boleij, 1991; Thorne, Kiekhaefer, Whitten, & Donham, 1992). The air sampler was precalibrated at 28.3 liters per minute (L/min), and all removable components were pre-autoclaved and subsequently disinfected Disinfected Decreased the number of microorganisms on or in an object. Mentioned in: Isolation with 70 percent ethanol between sampling runs. The air sampler collects airborne microbes directly onto 55-mm rapid organism detection and counting (RODAC RODAC Replicate Organism Detection and Counting RODAC Regional Ocean Dumping Advisory Committee RODAC Reorganization Objectives Army Division, Army, & Corps ) plates through impaction (Theron, 2003). The collected samples were stored at low temperature during transportation to the laboratory. Sample Treatment For enumeration 1. (mathematics) enumeration - A bijection with the natural numbers; a counted set. Compare well-ordered. 2. (programming) enumeration - enumerated type. of total viable counts (TVCs), plate count agar Plate count agar (PCA) is a microbiological growth medium commonly used to assess or to monitor total bacterial growth of a sample. It is straw yellow in colour, and tends to be used to give an overall estimation of the bacterial growth contained on a sample, although such (PCA (tool, programming) PCA - A dynamic analyser from DEC giving information on run-time performance and code use. , Anatech, South Africa South Africa, Afrikaans Suid-Afrika, officially Republic of South Africa, republic (2005 est. pop. 44,344,000), 471,442 sq mi (1,221,037 sq km), S Africa. ) plates were incubated at 25[degrees]C for 72 hours (Vanderzant & Spittstoesser, 1992), while Baird-Parker agar (BPA BPA British Paediatric Association. , Anatech, South Africa) plates were incubated at 35[degrees]C for 48 hours for enumeration of presumptive pre·sump·tive adj. 1. Providing a reasonable basis for belief or acceptance. 2. Founded on probability or presumption. pre·sump Staphylococcus spp. (Nikanen & Aalto, 1978). Typical S. aureus colonies were confirmed with the rapid latex agglutination test latex agglutination test n. A passive agglutination test in which antigen is adsorbed onto latex particles. latex agglutination test (Slidex Staph staph n. Staphylococcus. staph adj. Plus Test Kit, Bio Merieux, South Africa) (Griethuysen, Bes, Etienne, & Kluytmans, 2001). Staphylococcal staphylococcal pertaining to Staphylococcus spp. staphylococcal clumping test used as a means of measuring the quantity of fibrinogen-split products in a sample of blood. Species Identification Staphylococcus spp. that the rapid latex agglutination test found not to be S. aureus were plated on blood agar blood agar n. A nutrient culture medium that is enriched with whole blood and used for the growth of certain strains of bacteria. and incubated for 18 to 24 hours at 35[degrees]C. These Staphylococcus species were identified with the API-Staph system (several S. aureus samples were also identified for further confirmation) (Nagase et al., 2002a; Nagase et al., 2002b) and APILAB software in accordance with the manufacturer's procedure (Bio Merieux, South Africa). Staphylococcus aureus Coagulase Typing Coagulase typing was carried out according to the manufacturer's procedure (Ushioda et al., 1981) with a coagulase typing kit (Denka Seiken, Japan). Neutral rabbit antisera specific for eight coagulase types (I to VIII) were used (Shimizu et al., 2000; Ushioda et al., 1981). Negative controls of S. epidermidis and positive controls of S. aureus were used. Aliquots (0.1 mL) of antisera as well as normal rabbit serum (as a control) were added to 0.1 mL of supernatant supernatant /su·per·na·tant/ (-na´tant) the liquid lying above a layer of precipitated insoluble material. supernatant the liquid lying above a layer of precipitated insoluble material. obtained from a 12-hour culture of each test isolate and incubated at 35[degrees]C for 1 hour. Aliquots (0.2 mL) of rabbit plasma were added, and inhibition of coagulase after further incubation at 35[degrees]C for at least 1 hour indicated the coagulase type. Strains whose coagulase activity was not neutralized by the set of antisera were designated as nontypable, as were strains that reacted to more than two specific sera (Shimizu et al., 2000). [FIGURE 1 OMITTED] Statistical Analysis Statistical analyses, including Pearson's correlation, were performed with Excel 2000 and Sigma Plot SPSS A statistical package from SPSS, Inc., Chicago (www.spss.com) that runs on PCs, most mainframes and minis and is used extensively in marketing research. It provides over 50 statistical processes, including regression analysis, correlation and analysis of variance. for Windows XP The previous client version of Windows. XP was a major upgrade to the client version of Windows 2000 with numerous changes to the user interface. XP improved support for gaming, digital photography, instant messaging, wireless networking and sharing connections to the Internet. , version 8.0. Probability values of p [less than or equal to] .05 were considered significant. All analyses were done in duplicate. Results and Discussion Distribution and Patterns of Microbiota Microbiota (human) Microbial flora harbored by normal, healthy individuals. A number of microorganisms have become adapted to a particular site or ecologic niche in or on their host. The distribution of the airborne total viable counts (TVCs) in the deboning rooms of various red-meat abattoirs is shown in Figure 1. TVCs in Abattoir A were relatively similar throughout the study period, with the exception of high counts (1.2 x [10.sup.3] CFUs/[m.sup.3]) recorded during the third hour of Week 4. The lowest TVCs (1.5 x [10.sup.1] CFUs/[m.sup.3]) in Abattoir A were recorded during Week 1 at the fourth hour. Total viable counts were notably the highest in Abattoir B during the second hour of Week 1 (12.0 x [10.sup.3] CFUs/[m.sup.3]). The counts in the remaining abattoirs, C and D, were relatively similar. In general, the airborne TVCs appeared relatively similar throughout the sampling intervals of months and days, with only a few exceptions. These counts were distributed between the values of [10.sup.1] and [10.sup.3] CFUs/[m.sup.3], similar to the counts ranging from 1.2 x [10.sup.2] to 1.1 x [10.sup.3] CFUs/[m.sup.3] recorded indoors in a study by Fabian, Miller, Reponen, and Hernandez (2005). Apart from minor fluctuations among the sampling intervals of hours and weeks, no definite pattern could be observed that could suggest a time during the day or over a month, when notable increases or decreases occurred in the TVC TVC Traditional Values Coalition TVC Televisió de Catalunya (Catalan Public Broadcasting Company, Catalonia, Spain) TVC Television Commercial TVC Thrust Vector Control TVC Texas Veterans Commission TVC Total Variable Cost bioaerosol composition that could be related to a particular activity during the deboning process. The distribution and patterns of the airborne staphylococci counts in the deboning rooms of various red-meat abattoirs are shown in Figure 2. Compared with the TVC bioaerosols (Figure 1), the staphylococci distribution showed notably fewer fluctuations among all abattoirs and sampling intervals, and definite patterns related to sampling intervals could not be observed. The staphylococci counts in Abattoir A were relatively low, and in Abattoir B the highest counts (6.0 x [10.sup.4] CFUs/[m.sup.3]) were recorded during Week 2 at the second hour (Figure 2). The remaining abattoirs had a different pattern than Abattoir B, showing similar distribution of counts throughout the sampling period, with the exception of Abattoir A, which recorded low counts (Figure 2). To shed light on the overall performance of the abattoirs, the authors calculated the mean distribution of total viable counts and staphylococcal counts among the abattoirs. The counts in Abattoir A were the lowest for both TVC and staphylococci: 1.3 x [10.sup.2] CFUs/[m.sup.3] (standard deviation In statistics, the average amount a number varies from the average number in a series of numbers. (statistics) standard deviation - (SD) A measure of the range of values in a set of numbers. [SD]: 137.7) and 8.0 CFUs/[m.sup.3] (SD: 6.54), respectively A correlation value of r = -.313 was recorded for TVC and staphylococci in Abattoir A. Abattoir B, with a correlation of r = -.358 and average values for TVC and staphylococci of 1.0 x [10.sup.3] CFUs/[m.sup.3] (SD 992.1) and 1.6 x [10.sup.2] CFUs/[m.sup.3] (SD 140.6), respectively, had the highest recorded values of the four abattoirs. Abattoir C had average counts of 3.0 x [10.sup.2] CFUs/[m.sup.3] (SD 249.4) and 3.0 x [10.sup.1] CFUs/[m.sup.3] (SD 19.9) for TVC and staphylococci, respectively, whereas Abattoir D had average counts of 3.1 x [10.sup.2] CFUs/[m.sup.3] (SD 253.9) for TVC and 2.4 x [10.sup.1] CFUs/[m.sup.3] (SD 10.9) for staphylococci. Correlations between TVC and staphylococci for abattoirs C and D were r = .941 and r = -.795, respectively showing a positive and a negative correlation Noun 1. negative correlation - a correlation in which large values of one variable are associated with small values of the other; the correlation coefficient is between 0 and -1 indirect correlation , while in the first two abattoirs, correlations between the studied microorganisms were negative or poor. Apart from correlation observed between microorganisms, the F-test was used to assess if there were any significant differences among the abattoirs. Abattoirs A and B, A and D, B and C, and B and D differed significantly (p = 2.2 x [10.sup.-6], .043, 6.9 x [10.sup.-4], and 9.3 x [10.sup.-4], respectively) with respect to microbial distribution. In the remaining abattoirs, A and C (p = .055) and C and D (p = .911), distribution of TVC and staphylococci did not differ significantly compared with the other abattoir combinations. In general, the counts found in the various abattoirs did not exceed the guideline suggested by Jensen and Schafer (1998) for ubiquitous bacterial aerosols. The relatively low numbers recorded in this study do not, however, necessarily indicate a clean and healthy environment, as counts of less than 1.0 x [10.sup.2] CFUs/[m.sup.3] have been shown to be unhealthy for immunosuppressed Immunosuppressed A state in which the immune system is suppressed by medications during the treatment of other disorders, like cancer, or following an organ transplantation. Mentioned in: Fifth Disease individuals (Jensen & Schafer, 1998). These counts may be attributed to poor personal hygiene personal hygiene person n → Körperhygiene f or lack of good processing practices in red-meat abattoirs, especially in abattoirs B and D. No significant relationship was noticed between temperature levels and microbial levels during the study. The temperature levels were 7[degrees]C-9[degrees]C in Abattoir A and 9[degrees]C-12[degrees]C in Abattoir C, and these levels were the same throughout the study period. The temperatures of the remaining abattoirs were not measured specifically, but taken with the day's temperature levels, which were 25[degrees]C-27[degrees]C for Abattoir B and 26[degrees]C-29[degrees]C for Abattoir D. Contribution of Staphylococci Bioaerosols to Contamination of Red Meat A previous study (Shale, Lues, Venter, & Buys, 2005) investigated the distribution of TVC and staphylococci in the same environment (the deboning rooms of red-meat abattoirs). Two questions arose from that study: 1) What is the contribution of staphylococci to the total microbial population of the meat in the deboning room? and 2) What is the contribution of the bioaerosols to the contamination of the meat in this area? To shed light on these questions, both descriptive and inferential in·fer·en·tial adj. 1. Of, relating to, or involving inference. 2. Derived or capable of being derived by inference. in methodologies have been applied, as they present both visual representations and statistical conclusions. The results for airborne contamination from the study reported here are therefore compared with the results for meatborne contamination reported in the previous study. Visual comparisons (by way of polar plots) were used to illustrate the extent of Staphylococcus sp. occurrence compared with the total viable counts in air and meat. The data (not shown, but see examples of polar plots in Figure 3 and Figure 4) indicated that the Staphylococcus sp. component was the most prevalent in Abattoir B and the least prevalent in Abattoir A. In the meat, the staphylococci component was largest in Abattoir D and smallest in Abattoir C. Because polar plots are only visual representations that aid the comprehension of the predominance of staphylococci in the total viable counts, they do not give a clear indication of the exact relationship between the total viable counts and the staphylococci during the sampling period of five weeks. In other words Adv. 1. in other words - otherwise stated; "in other words, we are broke" put differently , they do not indicate whether fluctuations in the staphylococci significantly influenced the total microbial composition of the air and meat. Therefore, statistical computations of such interactions are required. Statistical computation showed that only in Abattoir C was there a significant correlation (r = .959) between TVC and staphylococci, suggesting concomitant increases and decreases in the numbers of these two groups of microbiota throughout the sampling period. In the remaining abattoirs, A, B, and D, correlation values were r = .000, -.231, and -.313, respectively. Staphylococci thus proved to be a definite contributor to the total microbial contamination in both the air and meat at this abattoir. Figure 3 and Figure 4 (examples of polar plots) compare the air and meat in terms of TVC and staphylococci. Although the microorganisms are expressed per gram (meat) and per cubic meter Noun 1. cubic meter - a metric unit of volume or capacity equal to 1000 liters cubic metre, kiloliter, kilolitre metric capacity unit - a capacity unit defined in metric terms (air), the graphs give an indication of the levels of contamination in both of these environments. Compared with abattoirs A and D, abattoirs B and C had higher levels of both TVC and staphylococci in the air. It therefore appeared that the level of bioaerosol contamination in the latter two abattoirs was more substantial. It can be concluded that the air considerably influenced TVCs on the meat in Abattoir A, as there was significant correlation (r = .975) between TVC in the air and on the meat. In other words, the air considerably influenced TVC on the meat in Abattoir A. In the remaining abattoirs, B, C, and D, the correlations between the air and the meat with respect to TVC were -.413, -.463, and -.179, respectively. With respect to the impact of staphylococci bioaerosols on meat, correlation values were r = .009, .185, .133, and .754 for abattoirs A, B, C, and D, respectively. Only in Abattoir D did a strong recorded correlation imply a considerable influence of airborne staphylococci on the presence of meatborne staphylococci. [FIGURE 2 OMITTED] Although attempts have been made to apply descriptive and inferential statistics inferential statistics see inferential statistics. to assess the true impact of bioaerosols in the contamination of red meat with respect to the microbiota mentioned, the study made clear that a lot of research is needed on bioaerosols in food-processing plants. The study reported here suggests new avenues for predicting and measuring contamination of foodstuffs, particularly in red meat. Species of Staphylococci Isolated from Bioaerosols The airborne Staphylococcus species identified in the deboning rooms of the various abattoirs are given in Table 1. The species Staphylococcus capatis, generally found on the skin of humans (Euzeby, 2003), was isolated in Abattoir A (2.5 percent), Abattoir B (23 percent), and Abattoir C (35.3 percent). Staphylococcus caprae Staphylococcus caprae is a Gram positive, spherical bacteria and a member of the genus Staphylococcus. S. caprae is coagulase-negative. It was originally isolated from goats ("caprae , for which the known primary reservoir is the milk of mastitis-free goats (Alligent, Aubert, Dyke, & Solh, 2000), was isolated only in Abattoir D. Staphylococcus chromogens, which was isolated in sheep (Hogg & Lehane, 1999) was also found only in Abattoir D (Table 1). Staphylococcus conhii was isolated in all the abattoirs, although predominantly in Abattoir C (35.5 percent). This organism has been known to occur in abundance on the skin of chickens (Nagase et al., 2002a; Nagase et al., 2002b). Staphylococcus epidermidis Staphylococcus epidermidis Microbiology A coagulase-negative staphylococcus that comprises up to 80% of clinical isolates Infections by S epidermidis , which was found only in Abattoir D, is known to be found in the forehead, axillae Axilla (plural, axillae) The medical term for the armpit. Mentioned in: Hyperhidrosis , arms, and legs of humans. In addition, S. epidermidis was reported to be present in the bodies of 63.8 percent of Staphylococcus carriers in the United States United States, officially United States of America, republic (2005 est. pop. 295,734,000), 3,539,227 sq mi (9,166,598 sq km), North America. The United States is the world's third largest country in population and the fourth largest country in area. and is known as the second most common airborne bacteria in domestic environments (Nagase et al., 2002a; Nagase et al., 2002b). Staphylococcus haemolyticus Staphylococcus haemolyticus is a species of bacterium belonging to the genus Staphylococcus. It is a Gram positive coccus, coagulase negative, and catalase positive. Frequently found as a commensal organism on the skin of humans and animals, S. , which has the same primary reservoir as S. epidermidis, was found in the air of all the abattoirs with the exception of Abattoir C (Table 1); however, this species has also been isolated from dogs and other domestic animals (Lilenbaum, Veras, Blum, & Souza, 2000). [FIGURE 3 OMITTED] [FIGURE 4 OMITTED] Staphylococcus lentus, which has been reported in significant levels on the udders of goats and the skins of chickens, was isolated in Abattoir A only (8.8 percent) (Nagase et al., 2002b; Shimizu et al., 2000). Staphylococcus saprophyticus Staphylococcus saprophyticus is a coagulase-negative species of Staphylococcus bacteria (which are catalase-positive). S. saprophyticus is often implicated in urinary tract infections. S. was also isolated in Abattoir A (47 percent); it is reported to be the most often encountered agent of urinary-tract infections identified in the urine of young, sexually active females (Martineau et al., 2000). Euzeby (2003) reports that S. saprophyticus and S. lentus occur in bovine nostrils. Staphylococcus simulans isolated from Abattoir A (2.9 percent) and Abattoir C (5.9 percent), is known to be associated with human skin (Razonable, Leuullen, Patel, & Osmon, 2001). Staphylococcus warneri Staphylococcus warneri is a member of the bacterial genus Staphylococcus, consisting of Gram-positive bacteria with spherical cells appearing in clusters. It is coagulase-negative and is a common commensal organism on the skin of humans and animals. , also of human origin (Foster, 2002), was isolated only from Abattoir C. Coagulase-negative Staphylococcus xylosus Staphylococcus xylosus is a member of the genus Staphylococcus, a genus of Gram-positive bacteria that form clusters of cells. Like many other staphylococci, it is coagulase-negative and exists as a commensal on the skin of humans and animals and in the environment. was found in all the abattoirs except Abattoir C and has been reported to be associated with the teat teat (tet) nipple (1). teat n. 1. See nipple. 2. The female breast; mamma. 3. A papilla. skin of various domestic and wild animals WILD ANIMALS. Animals in a state of nature; animals ferae naturae. Vide Animals; Ferae naturae. (Shimizu et al., 2000). All other species were also isolated from meat samples in the previous study by Shale and coauthors (2005) in the same environment except S. auricularis, S. homonis, S. intermedins, and S. sciuri. Furthermore, some species such as S. caprae and S. simulans were not isolated from the meat, which suggests that there are other sources of contamination, that the microorganisms did not compete well in the meat or that they were only aerosolized Adj. 1. aerosolized - in the form of ultramicroscopic solid or liquid particles dispersed or suspended in air or gas aerosolised gaseous - existing as or having characteristics of a gas; "steam is water is the gaseous state" and never ended up on the meat in the deboning room. Occurrence of S. aureus and Its Coagulase Types in Bioaerosols Staphylococcus aureus is commonly regarded as the most pathogenic coagulase-positive species, and it is known to originate on the skin, hair, and nostrils of warm-blooded animals (Lior, Baron, & Gautier, 2003; Sheretz et al., 2001). Identification of the coagulase types of this species has helped in epidemiological investigations of food poisoning food poisoning, acute illness following the eating of foods contaminated by bacteria, bacterial toxins, natural poisons, or harmful chemical substances. It was once customary to classify all such illnesses as "ptomaine poisoning," but it was later discovered that (Shimizu et al., 2000) and has contributed significantly to the understanding of the sources, transmission, and spread of food poisoning. This species was isolated predominantly in the bioaerosols of Abattoir D (23.8 percent) followed by those of Abattoir B and Abattoir A (13 percent and 5.9 percent, respectively) as shown in Table 1. The presence of S. aureus on the bodies of humans does not alone account for its aerosolization unless the organizations are disrupted via shedding (which is common) (Sheretz et al., 2001). Furthermore, given that a common reservoir for this species is the anterior nares The Anterior Nares are the external (or "proper") portion of the nostrils (nose).[1] Common Infections (MRSA) Commonly infected by Staphylococcus aureus of humans, release of this organism into the air via sneezing is also a possibility (Sheretz et al., 2001). Table 2 shows the distribution of S. aureus coagulase types in the air of the various abattoirs. Only coagulase types I, III, VII, and VIII were isolated in the study reported here, as indicated in Table 2. Coagulase Type 1, known to be abundant in the environment, was isolated from both Abattoir B (50 percent) and Abattoir D (40 percent). This coagulase type is capable of producing hazardous enterotoxins. Staphylococcus aureus coagulase Type III, which was found only in Abattoir A, and Type VII, which was found in Abattoir B (25 percent) and Abattoir D (20 percent), have been reported to be involved in food poisoning (Shimizu et al., 2000). The primary reservoir of coagulase Type III is reported to be bovine animals (Shimizu et al., 2000; Nagase et al., 2002a); coagulase Type VII is the type most frequently encountered in staphylococcal food poisoning (contributing to 70 percent of outbreaks, followed by Type III with 12 percent). The exact reason for the dominance of coagulase Type VII is unclear (Shimizu et al., 2000). The remaining type, coagulase Type VIII, was found in the air of all the abattoirs, predominating in Abattoir D (40 percent) (Table 2). This coagulase type is capable of producing the potent Enterotoxin enterotoxin /en·tero·tox·in/ (en´ter-o-tok?sin) 1. a toxin specific for the cells of the intestinal mucosa. 2. a toxin arising in the intestine. 3. B, which can cause severe food poisoning (Nagase et al., 2002a; Nagase et al., 2002b; Shimizu et al., 2000; Ushioda et al., 1981). Through comparison with results from the 2005 study by Shale and co-authors (2005) on red meat in the same environment, it can be concluded that airborne coagulase types were not the source of meat contamination. In contrast to the many coagulase types isolated in the meat, only types I, III, VII, and VIII were found in bioaerosols. Abattoir C, for example, did not contain any coagulase types in the air, although coagulase types were found in the meat samples. The reason fewer staphylococci were found in the air may be that their way of forming clusters makes them too heavy to be carried into the air as compared to other microbes. From the data collected in the study reported here, it can be concluded that both TVC and staphylococci bioaerosol counts were higher in Abattoir B deboning rooms than in the deboning areas of other abattoirs. The deboning area of the Grade B abattoir differed from those of the Grade A, Grade C, and Grade D abattoirs in that it did not consist of an enclosed room, but was merely a separate area where the deboning was performed. This circumstance, rather than temperature levels, may be the reason for the observed bioaerosol counts. Properly regulated and separate deboning rooms therefore appear to be a definite advantage in leveling off the increase of undesirable airborne contaminants. When the species distribution of staphylococci in the bioaerosols of the various abattoirs was investigated, it became clear that staphylococci from various sources and primary reservoirs are abundant in the airborne environment. The primary reservoirs of such organisms are not only humans, and the presence of these organisms should therefore not be exclusively attributed to food handlers. Many species may in fact originate from poor slaughtering techniques and lack of proper abattoir management. The contribution of humanborne staphylococcal bacteria to the bioaerosol population is, however, considerable--an issue that should be addressed through the implementation of proper quality control and good manufacturing procedures (GMPs). The literature cited also has shown that airborne staphylococci originate from various environments--a fact that could be addressed through proper management and implementation of GMPs and prerequisite programs. The presence of airborne Staphylococcus aureus coagulase types capable of producing toxins hazardous to consumers as well as to food handlers is of importance, as these hazardous microbiota are probable contaminants of meat products via the air. Specific recommendations for contributing to overall air quality include 1) directing the airflow so that it is countercurrent countercurrent /coun·ter·cur·rent/ (-kur?ent) flowing in an opposite direction. countercurrent flowing in an opposite direction. to the production flow, a practice not in place in any of the sampled abattoirs; 2) keeping temperature without exception lower than 12[degrees]C in the deboning rooms and 7[degrees]C for the meat itself throughout the deboning period to prevent growth of microorganisms; 3) using face masks to minimize the spread of microbes from food handlers; 4) drafting guidelines for red-meat abattoirs that stipulate the maximum number of microorganisms permitted in the air per deboning area; 5) using 3-hydroxy fatty acids as biomarkers for the quantification and characterization of Gram-negative bacteria and endotoxins within food-processing areas (Lee, Chan, Fang, & Lan, 2004); and 6) using electrostatic fields to inactivate in·ac·ti·vate v. 1. To render nonfunctional. 2. To make quiescent. in·ac ti·va airborne and
surface microorganisms (Yao, Mainelis, & An, 2005).
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TABLE 1 Staphylococcal Species Found in the Air of Deboning Areas of
Various Abattoirs
Abattoir Coagulase
Species Type
Abattoir Abattoir Abattoir Abattoir
A B C D
n % n % n % n %
S. aureus 2 5.9 4 13 0 0 5 23.8 +
S. capitis 1 2.9 7 23 6 35.3 0 0 -
S. caprae 4 11.9 0 0 0 0 0 0 -
S. chromogens 0 0 0 0 0 0 9 43 -
S. cohnii 2 5.9 1 3.3 6 35.3 1 4.7 -
S. epidermidis 0 0 0 0 0 0 2 9.5 -
S. haemolyticus 1 2.9 7 23 0 0 2 9.5 -
S. lentus 3 8.8 0 0 0 0 0 0 -
S. saprophyticus 16 47 0 0 0 0 0 0 -
S. simulans 1 2.9 0 0 1 5.9 0 0 -
S. warneri 0 0 0 0 4 23.5 0 0 -
S. xylosus 4 11.8 11 36.8 0 0 2 9.5 -
Total 34 100 28 100 17 100 21 100
TABLE 2 Staphylococcus aureus Coagulase Types Found in the Deboning
Areas of Various Abattoirs
Type Abattoir
Abattoir A (%) Abattoir B (%) Abattoir C (%) Abattoir D (%)
I 0 (0%) 2 (50%) 0 (0%) 2 (40%)
III 1 (50%) 0 (0%) 0 (0%) 0 (0%)
VII 0 (0%) 1 (25%) 0 (0%) 1 (20%)
VIII 1 (50%) 1 (25%) 0 (0%) 2 (40%)
Total 2 (200%) 4 (100%) 0 (0%) 5 (100%)
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