13: Microbiology, Food Microbiology and Disease Transmission - Biology

13: Microbiology, Food Microbiology and Disease Transmission - Biology

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Learning objectives

  • To classify individual bacteria by shape
  • To obtain data concerning the relative abundance of bacteria in common environments
  • To describe bacterial colony shapes and growth patterns
  • To utilize the process of fermentation to make yogurt
  • To engage in an epidemiological investigation of disease transmission

Thumbnail: A neutrophil (a type of white blood cell, shown in blue-gray) interacting with Klebsiella pneumoniae bacteria (shown in pink). Image used with permission CC-BY 2.0, NIAID).

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Mother-to-Infant Microbial Transmission from Different Body Sites Shapes the Developing Infant Gut Microbiome

The acquisition and development of the infant microbiome are key to establishing a healthy host-microbiome symbiosis. The maternal microbial reservoir is thought to play a crucial role in this process. However, the source and transmission routes of the infant pioneering microbes are poorly understood. To address this, we longitudinally sampled the microbiome of 25 mother-infant pairs across multiple body sites from birth up to 4 months postpartum. Strain-level metagenomic profiling showed a rapid influx of microbes at birth followed by strong selection during the first few days of life. Maternal skin and vaginal strains colonize only transiently, and the infant continues to acquire microbes from distinct maternal sources after birth. Maternal gut strains proved more persistent in the infant gut and ecologically better adapted than those acquired from other sources. Together, these data describe the mother-to-infant microbiome transmission routes that are integral in the development of the infant microbiome.

Keywords: infant microbiome microbiome transmission shotgun metagenomics strain-level profiling.

Copyright © 2018 The Author(s). Published by Elsevier Inc. All rights reserved.

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For courses in introductory microbiology.

This package includes Mastering Microbiology.

Explore the invisible world of microbiology and why it matters to human life

Known for its unique art program and conversational writing style, Robert Bauman’s Microbiology with Diseases by Taxonomyconsistently emphasizes why microbiology matters, especially in health care. The taxonomic organization of the disease chapters (Chapters 19–27) presents microbial diseases by type of pathogenic microbe, helping students recognize shared characteristics among categories of microbes.

The 6th Edition presents a revitalized and strengthened pedagogical framework based on how students learn best. Checkpoints appear throughout the text and direct students to interactive versions of text features in Mastering Microbiology. The interactive features provide just-in-time remediation that helps fill skill gaps and give students immediate feedback on their progress with the material. New interactive concept maps provide opportunities for students to make connections between concepts and can also be assigned in Mastering Microbiology. To emphasize how our understanding of microbiology is constantly expanding, the new edition integrates cutting-edge microbiology research that is critical for today’s students. New Research on Microbial Metabolism is introduced in Chapter 5 as well as recent findings on recombinant DNA technology and CRISPR technique are found in Chapter 8.

Reach every student by pairing this text with Mastering Microbiology

Mastering™ is the teaching and learning platform that empowers you to reach every student. By combining trusted author content with digital tools developed to engage students and emulate the office-hour experience, Mastering personalizes learning and improves results for each student. Mastering Microbiology provides tutorials, animations and career relevant applications that enable students to see the invisible world of microbiology, to master key microbiology concepts, and to apply those concepts to human life. Learn more about Mastering Microbiology.

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is a simple-to-use, mobile-optimized, personalized reading experience available within Mastering Microbiology. It lets students highlight, take notes, and review key vocabulary all in one place – even when offline. Seamlessly integrated videos and other rich media engage students and give them access to the help they need, when they need it. Educators can easily customize the table of contents and share their own notes with students so they see the connection between their eText and what they learn in class.

For instructors not using Mastering Microbiology, Pearson eText can also be adopted on its own as the main course material. Learn more about Pearson eText or contact your rep for purchase options.

The mechanism of action of gut bacteria in intestinal disease development

Most studies have shown that intestinal bacteria are associated with the development of various diseases, but few have systematically reported the molecular mechanisms by which intestinal bacteria affects diseases. Most bacteria in intestine form complex networks, including the beneficial bacteria and harmful bacteria (Fig. 1). Under normal circumstances, they exist optimally and are beneficial to the host health, but when imbalanced, it increases the risk for diseases. The secretion of bacterial biofilm is also one of the factors that lead to development of human diseases. The metabolites, such as the SCFA, toxic products, bile acid, etc. of intestinal microbiota can also affect the health of the host. In contrast, they can protect the host from pathogen invasion by activating immune defense.

‘Good’ bacteria and ‘Bad’ bacteria

There is a considerable body of evidence to support the hypothesis that the endogenous intestinal microbiota plays a crucial role in the pathogenesis of intestinal disease such as IBD and its variants and related disorders (Weingarden and Vaughn 2017 ). In recent years, the prevalence of these diseases has increased significantly, which may be related to changes in the environment and lifestyle. The change of life style may have altered the initial development or stable maintenance of microbiota, thus changes the ‘normal’ or healthy composition of microbiota, namely dysbiosis (Round and Mazmanian 2009 ). Clinical, epidemiological and immunological studies indicate that a change of intestinal microbiota may be an important factor in the occurrence of many inflammatory diseases (Levy et al. 2017 ). Intestinal bacteria are an important part of immune system development and function. Therefore, the lack of beneficial micro-organisms to promote appropriate immune development (due to ecological imbalance) may lead to inflammatory response, which is the basis of various human immune diseases.

The intestinal bacterial population in healthy adults is rich and has a high diversity. The composition of microbial community is significantly different in different niche of GIT. In human body, Proteobacteria and Clostridium species are mainly located in the small intestine Bacteroidae and Clostridiaceae families are mainly located in colon and cecum, and Lactobacilli, Streptococci and Enterococcus are mainly located in jejunum and ileum. In mice, Ruminococccae, Rikenellaceae and Lachnospiraceae are mainly located in cecum, Bacteroidaceae, Rikenellaceae and Prevotellaceae are mainly located in colon Bacteroides and Firmicutes are mainly located in intestinal cavity, and SFB and H. pylori are mainly located in mucous layer of the small intestine (Donaldson et al. 2016 ).

Each type of bacteria plays a role in maintaining their dynamic balance. Beneficial bacteria in the gut are called probiotics and harmful bacteria are pathogenic microbes. ‘Good’ bacteria in gut alleviate many intestinal diseases and play a positive role in human health. Lactobacillus rhamnose GG secretion (LSM, Lactobacillus soluble medium) were recovered from the PBMC culture (Ludwig et al. 2018 ), and the LSM regulate the function of DC by strengthening the ability of the T cell response, evidenced by increase IL-2 and IFN-γ producing T cells. Enhanced Foxp3 + expression is also observed and this study reveals that LSM can modulate DC function suggesting that LSM can provide alternative approach to improve adaptive immune defense system when live bacteria transplantation is not feasible. The expression of inflammatory markers (IL-1β, IL-12) and epithelial-integrity related proteins (TGFβ, ICAM1) in the colon alters the expression of microRNA, changes in the ratio of Firmicutes to Bacteroides induced by DSS (Rodriguez-Nogales et al. 2018 ). Bacillus coagulans MTCC 5856 can improve depression and gastrointestinal symptoms in patients with severe IBS (Majeed et al. 2018 ), and Bifidobacterium longum NCC3001 also shows similar effect in IBS patients (Pinto-Sanchez et al. 2017 ). In cancer, through mass spectrometric analysis, it is observed that Lactobacillus casei ATCC 334 can produce iron pigment, which plays a role in inhibiting tumour progression by activating JNK signalling pathway (Konishi et al. 2016 ). A randomized clinical trial showed that a combination of probiotic supplements containing five strains of Lactobacillus and Bifidobacterium could improve the symptoms of CD in patients with IBS (Francavilla et al. 2019 ). It was also observed that patients had increased intestinal Lactobacillus, Staphylococcus and Bifidobacterium, so their effects were related to the changes of intestinal microbiota. The Bifidobacterium adolescentis can treat constipation (Wang et al. 2017 ).

‘Bad’ bacteria in gut on the other hand promote many intestinal diseases and play a negative role in human health. Bacteria can produce multilayered agglomerations, called biofilms, which protect them from physical stress (fluid flow, scraping, epithelial turnover) in intestine lumen, and help spread resistance genes (Balcazar et al. 2015 ). By destroying mucus and depleting goblet cells, the intestinal pathogenic bacteria create the microbial biofilm that contact the epithelium, and the plankton can spontaneously migrate out of the damaged biofilm. Enteropathogenic bacteria can also increase the virulence of phytoplankton symbionts, induce their adhesion and infiltration, weaken the epithelial barrier and promote inflammatory response. The role of biofilms in disease-related micro-organisms in IBD, CRC and intestinal damage has been confirmed. Microscopic results showed that patients with IBD had dense Bacteroides fragilis biofilms (Swidsinski et al. 2005 ). In addition, the mean value of mucosal biofilm density with IBD was significantly different, about 100 times (Swidsinski et al. 2005 ), compared to IBS patients and healthy subjects. Intestinal diseases such as IBD are associated with imbalance of microbiota and destruction of mucosal epithelium, thus promoting species migration. Biofilms help pathogens escape their hosts' defenses, which can lead to disease progression (Hoarau et al. 2016 ).

Many anaerobic and aerobic micro-organisms, such as Klebsiella pneumoniae, E. coli and Fusobacillus nuclei, settle in the intestines and wounds all over the body (Bertesteanu et al. 2014 ). When bacteria colonized at the wound forms biofilms that slows or prevent wound healing. Biofilms containing enterotoxigenic B. fragilis (ETBF) and F. nucleatum were detected in tumour tissues (Kim et al. 2019 ). Biofilms are also observed in the nontumour mucosa tissue. Therefore, mature biofilms, when present in healthy tissues near CRC or IBD infected tissues, serve as an early warning signal for the critical transformation of the intestinal environment to imbalance, injury and pathogen infection. Bacteria that form pathogenic biofilms and their secretions can be used as signals to detect intestinal diseases. Such as Intestinal markers: (i) CRC: nucleatum, enterotoxigenic B. fragilis (ETBF, pks+E. coli, N1N12diacetyl-spermine) (ii) Gut wounds: F. nucleatum, E. coli, K. pneumoniae (iii) IBD: B. fragilis. Intestinal contact with enteropathogenic bacteria, especially Giardia sp. and Campylobacter sp. results to pathogenic imbalance of mucosal microbiota bacteria. Campylobacter sp. and Giardia sp. are also a typical risk factor for the occurrence of post infectious IBS (PI-IBS) (Svendsen et al. 2019 ). Also, Citrobacter rodentium colitis infections causes intestinal allergy in mice. Infectious gastroenteritis worsens IBD symptoms, with Campylobacter jejuni, Salmonella sp. or E. coli. The pathogenesis of IBD is mainly disruption of balance between gut microbes and host immunity.

The expression of Firmicutes in patients with IBD was decreased whereas the number of pathogenic deformation bacteria was increased (Kolho et al. 2015 ). The decrease of Prevotella sp., Clostridium leptum and microbial diversity leads to increase of faecal calprotectin, which indicates inflammation. As a result, it appears that IBD is not only affected by a single microbe but by multiple micro-organisms. However, the mechanism and role of underlying pathogens in causing IBD is not yet clear, and these problems need to be further addressed. In IBD, abdomen often have clinical complications, such as gastroenteritis, and it has been shown that C. jejuni plays a role in the development of complications (Rostami et al. 2015 ).

Escherichia coli was isolated from the intestines of mice with colitis, concurrently DNA damage and cancer were also observed (Arthur et al. 2014 ). Campylobacter jejuni also damage the polarity of TLR9, which in turn destroys the TLR9 induced epithelial barrier and increases CXCL8 production indicating that the infection of C. jejuni could induce the inflammatory response of experimental colitis in mice (Reti et al. 2015 ). Giardia sp. and C. jejuni can advance the release of plankton micro-organisms, and C. jejuni can activate the potential toxic genes of E. coli to promote adhesion of E. coli to human intestinal cells. This process is aided by the up-regulation of pro-inflammatory interleukin 8 (CXCL8) expression and down-regulation of toll-like receptor 4 (TLR4) expression. These findings may shed light on how intestinal pathogens can turn symbiotic bacteria into pathogens during the acute phase of infection.


Fatty acids

It is reported in the literatures that fatty acids including SCFAs, medium-chain fatty acids (MCFAs), long-chain fatty acids (LCFAs) could influence the intestinal microbiota (Bichkaeva et al. 2018 ). Anaerobic micro-organisms ferment undigested food and other host metabolites in the large intestine to produce beneficial SCFAs, including formic acid (C1), acetic acid (C2), propionic acid (C3), butyric acid (C4), isobutyric acid (C4), isovaleric acid (C5), hexanoic acid (C6). SCFA are absorbed from the intestinal cavity, but their subsequent distribution and metabolism within the host cells are different. Butyrate mainly provides energy for ECs, propionate is mainly responsible for metabolism in the liver and acetate can exist in a higher concentration in peripheral blood. Recent studies have shown that SCFAs have some anti-inflammatory effects and can modulate regulatory T cells in the colon of mice (Yu et al. 2019 ). Also, the anti-inflammatory effects of SCFAs have important effects on host cells and intestinal microbiota. SCFAs, produced by the intestinal bacteria through fermentation can increase the number of intestinal TReg cells and activate to secrete IL-10 in specific pathogen free mice (Smith et al. 2013 ). Extracellular SCFAs interact with host cell surface receptors. All host cells expressed GPR41 (FFA1), GPR43(FFA2) and GPR109A. GPR43 interacts with propionate, butyrate and acetate, GPR41 interact with propionic acid in strongest saline condition but GPR109A only interact with butyrate (Feng et al. 2018 Li et al. 2018 ). The interaction of butyrate with GPR109A may induce anti-inflammatory effect. Butyrate can also play an anticancer role by restraining the proliferation and selectively promoting apoptosis of CRC cells (Fung et al. 2012 ).

Medium-chain fatty acids, including octanoic acid (C8), capric acid (C10), lauric acid (12), must be ingested and not produced by gastrointestinal micro-organisms. MCFA isolated from skin lipids and milk with high concentrations has direct antibacterial effects on a variety of pathogenic Gram-positive and Gram-negative micro-organisms (Fischer et al. 2012 ), including Clostridium perfringens, Listeria monocytogenes and C. jejuni. However, studies in broiler chickens and piglets have shown that supplementation of MCFA capric acid, lauric acid and caprylic acid can enrich some pathogenic Enterobacteriaceae populations, such as Citrobacter sp. and E. coli, while inhibiting symbiotic species belonging to Enterobacteriaceae, such as Lactobacillus sp. (van der Hoeven-Hangoor et al. 2013 ). The mechanism of these changes in intestinal microbiota caused by MCFA on host physiology and immunity is not clear. In addition, MCFAs seems to be able to enrich and inhibit ‘symbiotic’ microbiota and pathogenic micro-organisms. The contradictory role of MCFAs in shaping intestinal microbiota may be due to the internal differences of intestinal microbiota among animals used in vivo models, the types of MCFA supplementation and the location of 16S rRNA sequencing and analysis of intestinal microbiota collected from animals.

Like MCFA, LCFAs, including myristic acid (C14), palmitic acid (C16), must be ingested. Among them, omega-6 fatty acids—derived lipid metabolites are produced by symbiotic bacteria, especially Lactobacillus (Hirata and Kunisawa 2017 ). It was also found that high saturated long-chain fatty (LCFA) was associated with increased intestinal motility in NMS rats. The increased saturated long-chain fatty was positively correlated with the increased abundance of Prevotella, Lactobacillus and Alistipes (Zhao et al. 2018 ). Most studies on LCFAs are focused on macrophages, however, the function of most immune cells may be interfered by the number and type of LCFA in the environment. Omega-3 LCFAs plays an anti-inflammatory role by acting at various levels. GPR40 and GPR120 are two known GPCRs that are sensitive to the metabolites of LCFA, especially omega-3 LCFA. In macrophages, activation of GPR40 and GPR120 has been shown to inhibit the stimulation of NLRP3 inflammatory bodies, and GPR120 can additionally inhibit NF-κB signalling (Zhang and Qiu 2019 ). These anti-inflammatory effects involve the recruitment of β-arrestin 2 and insulin sensitization. A high-fat diet stimulates inflammatory signalling pathways and is also associated with increased intestinal permeability by affecting intestinal microbiota (Xie et al. 2020 ).

Protein and toxic compounds

It's not just the microbes in the gut that can affect the health, but the proteases that are secreted by these microbes are also very important in developing diseases, like enteritis. AimA is an immuno-regulatory protein that is secreted by Aeromonas (Rolig et al. 2018 ). The symbiotic bacteria inhibit the harmful bacteria and intestinal inflammation in the host. In zebrafish model, this bacterium reduces inflammation and in chemical model, AimA prevent the excessive buildup of neutrophils, and prevent septic shock. Some bacteria also secrete amino acid-derived antibiotics to fight disease. Gut bacteria, Clostridium scindens and Clostridium sordellii, secrete tryptophan derived antibiotics 1-acetyl-β-carotine and turbomycin A, respectively (Kang et al. 2019 ). These two antibiotics inhibit the growth of Clostridium difficile and other intestinal bacteria by inhibiting the formation of the diaphragm during bacteria’s split phase. Olsenella scatoligenes (Liu et al. 2018 ) can secrete indoleacetic decarboxylase in the intestinal tract, which plays a key role in the process of tryptophan fermentation to form faecosine.

Bacterial fermentation of aromatic amino acids produces a range of metabolites, some of which are toxic, including certain nitrogen compounds, ammonia, amine and sulphides, etc. Some nitrogenous compounds, especially nitrites, increase the risk of cancer through DNA alkylation (Li et al. 2017 ). Ammonia is also a carcinogen at low concentrations and has been shown to be associated with mucosal damage and colorectal adenocarcinoma in animal models (Windey et al. 2012 ). Polyamine synthesis has been found in intestinal bacteria. High concentration of polyamine is toxic, which is involved in various diseases such as oxidative stress and cancer, and many studies suggest that oxidative stress caused by polyamine catabolism is the mechanism of toxicity (Olin-Sandoval et al. 2019 ). Pathogens, such as Shigella flexneri, Priceenterica subsp., Streptococcus pneumoniae, H. pylori and Enterica serovar Typhimurium employ polyamines to enhance their virulence (Di Martino et al. 2013 ). A small amount of sulphate reducing bacteria (such as Desulfovibrio) has been detected in most individuals that use lactate salts as a common substrate for growth and sulphide formation. Sulphide is not only toxic to colon cells but also inhibits the oxidation of butyrate and thereby destroys the integrity of the colon cell barrier (Blachier et al. 2017 ). This study observed that at a very low concentration (0·25–2 mmol l −1 ), sulphide produces ROS that is known to induce DNA damage resulting in cancer development.

Bile acid

Bile acid is a natural surfactant derived from cholesterol. They are important for lipid digestion, antimicrobial defense and glucose metabolism (Shapiro et al. 2018 ). Some bile acids destroy cell membrane because of their hydrophobicity, while others protect intestinal epithelium and are resistant to pathogens such as C. difficile (Buffie et al. 2015 ). Bile acids also have effects on gut related inflammation, which may be realized by regulating intestinal mucosal immune cells. The immunoregulation of bile acids is mostly studied in the background of innate immunity. Bile acids play an anti-inflammatory role in the innate immune system by inhibiting NF-κB-dependent signalling pathways and NLRP3-dependent inflammatory activities, but it is not clear whether they will affect adaptive immune cells, such as express IL-17a (TH17 cells) or regulatory T cells (T reg cells). Two lithocholic acid (LCA) metabolites found in humans and rodents directly affect CD4 (+) T cells (Kakiyama et al. 2014 ): the 3-OxoLCA can inhibit the differentiation of TH17 cells by directly binding with the key transcription factor retinoid-related orphan receptor-γt (RORγt) the isoalloLCA promotes the differentiation of T reg cells by producing mitochondrial ROS (mitoROS), which leads to the increase of Foxp3 expression (Hang et al. 2019 ). This suggests that bile acid metabolites control the host immune response by directly regulating the balance of TH17 and T reg cells.

Bile acids have strong antibacterial activity and may affect the composition of intestinal microbiota. The intestinal microbiome cannot transform primary bile acids, and when part of the residual bile acid passes through large intestine, the microbiome population in the large intestine changes significantly. The primary bile acid transforms into several different secondary bile acids, mainly deoxycholic acid and licholic acid. Mice when fed a diet with deoxycholic acid showed reduced generation of SCFAs and altered microbiota diversity, such as reduction of bacteroides, relative increase of Gammaproteobacteria and certain Firmicutes (Zeng et al. 2019 ). Bile acids activates reactive oxygen (ROS) and reactive nitrogen (RNS) species production during metabolism, and they can damage DNA, so they have a carcinogenic effect (Li and Cao 2016 ). The mechanism for controlling the toxicity of bile acid in cells is complex. Secondary bile acids are more capable of destroying cell membranes, and destroy membrane-related proteins (NAD(P)H oxidases and phospholipase (A2)) that cause ROS production, but may also do so by other mechanisms. For example, bile acids interact with nuclear receptors to activate signalling pathways that induce apoptosis. However, some bile acids also act as detoxification. Ursodeoxycholic acid seems to inhibit ROS and protect cells from deoxycholic acid. Song et al. showed that the primary bile acids (such as ursodeoxycholic acid) and some effective secondary bile acids (such as cholelithic acid) in the gut regulate RORγt + Treg cells through BAR VDR (bile acid receptor vitamin D receptor) (Song et al. 2020 ). One of the causes of human IBD and colorectal cancer is the disorder of intestinal bile acid (Postler and Ghosh 2017 ). Therefore, human VDR gene variation associated with IBD may affect the susceptibility of the disease through the wrong control of intestinal Treg cell pool.

The immune response

The immune defense system of the intestinal tract can control the imbalance of intestinal environment caused by bacterial microbiota and pathogenic bacteria. The first step in gut defense uses antimicrobial peptides secreted by gut ECs. Antimicrobial peptides (Amp), respond to colonization of the gut microbiome. Epithelial cells secrete antimicrobial peptides against immune intolerant pathogens or symbionts within mucosal layers. Paneth cell and ECs identify signature of microbe associated molecular patterns (MAMPs), through receptors such as MAMPs, NLRs, TLRs 2,4,5,9 and other RIG molecules. When mice treated with antibiotics after supplementation with probiotics (e.g., Lactobacillus), can trigger intracellular TLR-MyD88 pathway and restore certain intestinal defense capacity.

At birth, IgAs is produced by the induction of intestinal microbial factors by AHR ligands, such as indoles (Culbreath et al. 2015 ). The less the immunoglobulin secreted, the lesser the intestinal barrier integrity preserves. Breast milk can provide IgAs and play a protective role before the complete establishment of the intestinal immune defense system (Rogier et al. 2014 ). Immunoglobulin IgAs bind to the surface of bacteria and produce effective signals to gut immune cells to identify the bacteria and perform phagocytosis. So, IgAs can act as a second line of defense for gut immunity. Studies have shown that the gut immune system not only protects host cells, but also assists in the growth of certain symbiotic bacteria (Dishaw et al. 2016 ). IgA cross-linked bacteria can effectively block epithelial barrier translocation and thus inhibit the formation of biofilms. Many studies showed that IgA also exhibit a host–microbial symbiosis system, in addition to removing pathogens (Donaldson et al. 2018 ). IgA also help bacteria to grow and interact with the environment (Moor et al. 2017 ). Innate and adaptive immune cells act as a third line of defense.

During inflammatory response in the bacteria–host barrier surface, lymphoid cells (ILCs) serve as the first line of defense for lymphatic defense (especially the intestinal epithelium). When subjected to irritation, they do not exhibit specific T cell receptor (TCRs) to precise antigens, nor do they undergo clonal selection and expansion, but, a rapid response can be made in case of bacterial invasion and tissue damage by activating AMP production and triggering local immune responses. This mechanism is associated with the production of many cytokines. The nuclear hormone receptor, retinoid-related orphan receptor and ɤ-T trigger inflammatory responses in lymphocytes differentiate ILC1, ILC2 and ILC3. ILC3 secrete IL22 and IL17 that can act on ECs, improve the secretion of antimicrobial peptides (Amp) and nonspecifically protect commensals. The function of ILCs is to regulate adaptive immune CD4 (+) T cells. Targeting ILCs in mice through genetic or antibody mediated depletion strategies could be beneficial to maintain proper adaptive immune system (Eberl et al. 2015 ). ILCs interact with CD4 (+) T cells via MHCII dependence, which limits the response of histopathological adaptive immune cells to symbiotic bacteria, thus maintaining intestinal homeostasis (Hepworth et al. 2013 ). TRegs lymphocytes that secrete IL-10 play an anti-inflammatory role. Intestinal TRegs is controlled by GM-CSF derived from ILCs in the gut. The ability of ILC to produce GM-CSF without macrophages induces microbial signals and the production of interleukin-1β (Mortha et al. 2014 ).

It is observed that symbiotic microbes enhance communication between lymphocytes and innate myeloid cells and maintain immune homeostasis in the gut. Mice lacking GM-CSF regulate the effector function of mononuclear phagocytes and reduce the number of TRegs, and their role in bacterial translocation into tissue may be affected. When different subunits of typical DCs interact with ILCs and T cells, they also promote the ILC1/Th1/ CTL- or ILC3/ Th17 response (Murphy et al. 2016 ). Therefore, DCs can also control ILCs. Dendritic cells further activate T lymphocytes and promote the secretion of epithelial AMP by regulating ILCs. Other ILCs thought to be mucosa-associated invariant T cells (MAIT) that are mainly found in the intestinal epithelium, which also incorporate a rapid response to the microbiota, which can trigger inflammation, especially when identifying microbial derivatives (such as riboflavin derivatives) (Powell and MacDonald 2017 ). However, more data are needed on these cells for further conclusion.

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Contamination of Milk by Microorganisms | Milk Microbiology

The following points highlight the four mediums of contamination of milk by microorganisms. The mediums are: 1. The Dairy Cattle 2. The Milking Area 3. The Milking Equipment 4. Persons Handling Milk.

Medium # 1. The Dairy Cattle:

Milk contains microorganisms at the time of the its being drawn (milking) from the dairy cattle. A number of diseases like tuberculosis, brucellosis, fever, Streptococcus- and Staphylococcus- infections may be transmitted through milk to man.

These organisms are mechanically pushed out during milking. The number present at the time of milking has been reported between several hundred to several thousands per ml of milk.

Particles of manure, soil, etc. adhering to the skin of the udder and teats can gain entry into milk during milking causing contamination.

To avoid all these the health of the dairy cattle should be given due care and the udder and teats should be essentially cleaned properly before milking. The flanks of the animal should be clipped closely to minimise the chances of hair as well as adhering particles of dust which harbour bacteria from falling into milk during milking.

Medium # 2. The Milking Area:

The microbial content of the air is greatly affected by many conditions and practices. Accumulation of manure, dirt and throwing of hay in milking area adds to the microbial population of air. These airborne microorganisms may contaminate the milk. Air is generally considered to be a minor factor among the sources of contamination.

But, under certain conditions, it assumes great importance especially when wide mouth pails are used and outdoor milking is done in dusty yards without prior washing. Maintenance of clean area and minimization of activities that create dust certainly reduce the potential of contamination from this source.

Medium # 3. The Milking Equipment:

Use of unclean milking machines, milk cans, pipe lines, strainers, bulk tanks, and other equipment’s prove to be the most important source of milk contamination. Negligence in their proper cleaning before use affords ideal conditions for the growth of microorganisms.

The thermoduric and thermophilic bacteria surviving pasteurization multiply rapidly, contributing to high counts in the finished products. Therefore, it is very necessary that the milking equipment’s be thoroughly cleaned and effectively treated with bactericidal agents. High temperature (hot water or steam) or chlorine or quaternary ammonium compounds are commonly used as sanitizing agents.

Medium # 4. Persons Handling Milk:

Persons concerned with milking and handling of milk may also contaminate milk. Therefore, all persons involved in the milking process must be in good health and must follow procedures consistent with good sanitary techniques. Milkers must wash their hands properly, rinse them with some bactericidal solution and dry with clean towel before commencement of milking.

The possibility of diseased milkers contributing to pathogenic organisms is of great importance. Streptococcus spp. and Corynebacterium diphtheriae may be transmitted directly from the throat to the milk by coughing or sneezing. Dysentery bacilli may contaminate the milk through the hands of the person concerned.

Staphylococcus aureus and Staphylococcal Food-Borne Disease: An Ongoing Challenge in Public Health

Staphylococcal food-borne disease (SFD) is one of the most common food-borne diseases worldwide resulting from the contamination of food by preformed S. aureus enterotoxins. It is one of the most common causes of reported food-borne diseases in the United States. Although several Staphylococcal enterotoxins (SEs) have been identified, SEA, a highly heat-stable SE, is the most common cause of SFD worldwide. Outbreak investigations have found that improper food handling practices in the retail industry account for the majority of SFD outbreaks. However, several studies have documented prevalence of S. aureus in many food products including raw retail meat indicating that consumers are at potential risk of S. aureus colonization and subsequent infection. Presence of pathogens in food products imposes potential hazard for consumers and causes grave economic loss and loss in human productivity via food-borne disease. Symptoms of SFD include nausea, vomiting, and abdominal cramps with or without diarrhea. Preventive measures include safe food handling and processing practice, maintaining cold chain, adequate cleaning and disinfection of equipment, prevention of cross-contamination in home and kitchen, and prevention of contamination from farm to fork. This paper provides a brief overview of SFD, contributing factors, risk that it imposes to the consumers, current research gaps, and preventive measures.

1. Introduction

Food-borne diseases are a major public health concern worldwide [1, 2]. WHO defines food-borne disease (FBD) as “disease of infectious or toxic nature caused by, or thought to be caused by, the consumption of food or water” [2]. Annually, an estimated 76 million illnesses, 325,000 hospitalizations, and 5,000 deaths are caused by food-borne diseases in the United States [3]. Among these cases, 31 known pathogens cause 9.4 million illnesses, 56,000 hospitalizations, and 1300 deaths [4]. Using data from 2000–2008, researchers estimated that pathogens that were implicated in most FBD were norovirus (5.5 million, 58%), nontyphoidal Salmonella spp. (1.0 million, 11%), Clostrodium perfringens (1.0 million, 10%), and Campylobacter spp. (0.8 million, 9%). Among many food-borne pathogens, nontyphoidal Salmonella spp. and Campylobacter spp. are the leading causes of FBD in the United States, England, and Australia [4].

S. aureus is a significant cause of FBD, causing an estimated 241,000 illnesses per year in the United States [4]. However, the true incidence of Staphylococcus aureus food-borne disease (SFD) could be a lot higher as sporadic food-borne disease caused by S. aureus is not reportable in the United States [5]. Some other contributing factors for the low incidence of SFD include misdiagnosis, improper sample collection and laboratory examination [6], lack of seeking medical attention by the affected persons complicating the laboratory confirmation [5, 7], and lack of routine surveillance of clinical stool specimens for S. aureus or its enterotoxins [5, 8, 9]. Unavailability of implicated foods for confirmation of laboratory testing at the time of outbreak investigation further complicates the matter [5]. It is essential to note that FBD that is confirmed by laboratory testing and reported to public health agencies accounts for only a small fraction of illnesses [4]. FBD impose a great economic burden, accounting for $50–$80 billion annually in “health care costs, lost productivity, and diminished quality of life” in the United States [10, 11]. It is estimated that each case of SFD costs $695, representing a total cost of $167,597,860 annually in the United States [10]. The Institute of Medicine recognized FBD as a high priority [12]. “The potential for foods to be involved in the emergence or reemergence of microbial threats to health is high, in large part because there are many points at which food safety can be compromised.” Although FBD has decreased in recent years, it is still higher than Healthy People 2020 goals [10]. The presence of food-borne pathogens in ready-to-eat foods, meat, and meat products puts consumers at high risk and imposes grave economic losses to producers due to recalls of implicated food products [13, 14].

2. Staphylococcus aureus

S. aureus is a commensal and opportunistic pathogen that can cause wide spectrum of infections, from superficial skin infections to severe, and potentially fatal, invasive disease [15]. This ubiquitous bacterium is an important pathogen due to combination of “toxin-mediated virulence, invasiveness, and antibiotic resistance.” This organism has emerged as a major pathogen for both nosocomial and community-acquired infections. S. aureus does not form spores but can cause contamination of food products during food preparation and processing. S. aureus can grow in a wide range of temperatures (7° to 48.5° C optimum 30 to 37°C), pH (4.2 to 9.3 optimum 7 to 7.5), and sodium chloride concentration up to 15% NaCl. S. aureus is a dessication tolerant organism with the ability to survive in potentially dry and stressful environments, such as the human nose and on skin and inanimate surfaces such as clothing and surfaces [16]. These characteristics favor growth of the organism in many food products [2]. S. aureus can remain viable on hands and environmental surfaces for extended durations after initial contact [17, 18].

3. Staphylococcal Food-Borne Disease

SFD is one of the most common FBD and is of major concern in public health programs worldwide [1, 2, 19]. It is one of the most common causes of reported FBD in the United States [1, 20–22]. The first documented event of SFD due to the consumption of contaminated cheese was investigated by Vaughan and Sternberg in Michigan, USA, in 1884 [19]. A typical FBD caused by S. aureus has a rapid onset following ingestion of contaminated food (usually 3–5 hours). This is due to the production of one or more toxins by the bacteria during growth at permissive temperatures [2]. However, the incubation period of SFD depends on amount of toxin ingested [22]. Very small dose of SEs can cause SFD. For example, one report indicated that approximately 0.5 ng/mL concentration of SEs contaminated with chocolate milk caused a large outbreak [22, 23].

The onset of SFD is abrupt. Symptoms include hypersalivation, nausea, vomiting, and abdominal cramping with or without diarrhea. If significant fluid is lost, physical examination may reveal signs of dehydration and hypotension [1, 6, 22, 24]. Abdominal cramps, nausea, and vomiting are the most common [2]. Although SFD is generally self-limiting and resolves within 24–48 hours of onset, it can be severe, especially in infants, elderly, and immune-compromised patients [1, 6, 22]. Antibiotics are not used for therapy [7]. Approximately 10% of individuals inflicted with SFD will present to a hospital [22, 24]. Management of SFD is supportive. The attack rate of SFD can be up to 85% [22]. S. aureus may not be detected by culture in the events when food is contaminated and toxin is formed prior to cooking [22, 25]. A study involving 7126 cases indicated that case fatality rate of SFD is 0.03%. all deaths were in elderly patients [22]. Recovery is complete in approximately 20 hours [22, 24].

The conclusive diagnostic criteria of SFD are based upon the detection of staphylococcal enterotoxins in food [26], or recovery of at least 10 5 S. aureus

from food remnants [19]. S. aureus enterotoxin can be detected on the basis of three types of methods: bioassays, molecular biology, and/or immunological techniques [19, 27]. Polymerase chain reaction (PCR), reverse transcription PCR (RT-PCR), and RT-quantitative PCR can be carried out to evaluate the toxic potential of strain [19]. The enzyme immunoassay and enzyme-linked fluorescent assay are the most commonly used immunological methods based on the use of antienterotoxin polyclonal or monoclonal antibodies [19]. Several molecular typing methods are widely used for the genetic characterization of S. aureus such as multilocus sequence typing, spa typing, SCCmec typing, and Pulse-field gel electrophoresis (PFGE). These techniques provide means to trace epidemiologically related strains leading to the tracking back to the origin of contamination [28]. However, these methods have variation in their discriminating powers and can be increased by combining the methods [29]. Molecular-based methods provide information about the source of contamination (human or animal origin). The PFGE and spa typing can be used alone or in association to gather the information regarding the origin of S. aureus contamination [19].

Various types of foods serve as an optimum growth medium for S. aureus. Foods that have been frequently implicated in SFD are meat and meat products, poultry and egg products, milk and dairy products, salads, bakery products, especially cream-filled pastries and cakes, and sandwich fillings [2, 6, 30]. Foods implicated with SFD vary from country to country, particularly due to variation in consumption and food habits [2]. If food is prepared in a central location and widely distributed, SFD outbreaks can have grave consequences impacting thousands of people. For example, over 13,000 cases of SFD occurred in Japan in 2000 as a result of contamination of milk at a dairy-food-production plant [22, 31].

4. Staphylococcal aureus Enterotoxins

S. aureus produces wide arrays of toxins. Staphylococcal enterotoxins (SEs) are a family of nine major serological types of heat stable enterotoxins (SEA, SEB, SEC, SED, SEE, SEG, SEH, SEI, and SEJ) that belong to the large family of pyrogenic toxin superantigens [1, 6]. Pyrogenic toxins cause superantigenic activity such as immunosuppression and nonspecific T-cell proliferation [2]. It is hypothesized that superantigenic activity of SEs helps facilitate transcitosis that allows the toxin to enter the bloodstream, thus enabling it to interact with antigen-presenting cells and T cells leading to superantigen activity [1, 6, 19]. The majority of effects of SEs in SFD is believed to be triggered by initiating a focal intestinal inflammatory response due to their superantigenic activity or by affecting intestinal mast cells causing their degranulation [1, 22, 32].

SEs are highly stable and highly heat-resistant and resistant to environmental conditions such as freezing and drying [2, 19]. They are also resistant to proteolytic enzymes such as pepsin or trypsin and low pH, enabling them to be fully functional in the gastrointestinal tract after ingestion [2, 6]. The heat stability characteristic of S. aureus imposes a significant threat in food industries [1]. The mechanisms of SEs causing food poisoning are not clearly known. However, it is believed that SEs directly affect intestinal epithelium and vagus nerve causing stimulation of the emetic center [2, 19]. All staphylococcal enterotoxins cause emesis [22, 32]. An estimated 0.1 μg of SEs can cause staphylococcal food poisoning in humans [2].

SEs produced by some strains of S. aureus are the causative agents of SFD, and SEA is the most common toxin implicated in such events. SEA is highly resistant to proteolytic enzymes. SEA was recovered from 77.8% of all SFD outbreaks in the United States followed by SED (37.5%) and SEB (10%) [1, 6]. SEA is the most commonly found enterotoxin among SFD outbreaks in Japan, France, and UK [6]. However, SEC and SEE are also implicated with SFD. The outbreak of gastrointestinal illness via contaminated coleslaw in the United States was caused by SEC produced by methicillin-resistant S. aureus (MRSA) from an asymptomatic food handler [33]. SEC was linked to the SFD outbreak in 1980 in Canada [34]. SEC was also involved in the SFD outbreak during 2001–2003 in Taiwan [35] and 2009 outbreak in Japan [36]. S. aureus is often implicated with caprine mastitis [37]. In sheep, goats, and cattle, SEC was the predominant toxin type detected in S. aureus isolated from mastitis milk [38]. Other studies have documented SEC producers as the most prevalent enterotoxin-producing S. aureus isolated from goat’s milk [39] and goat’s skin of udder, teats, and milk [40]. Six SFD outbreaks in France in 2009 were caused by SEE present in soft cheese made from unpasteurized milk [26]. Although rare, SEE has also been implicated in the SFD outbreaks in USA and UK [6]. Various new SEs (SEG to SElU2) have been identified. However, only SEH-producing strains have been involved in SFD outbreaks [6].

S. aureus can survive in multiple host species. Molecular typing such as multilocus sequence typing (MLST) has helped to gain insights about population structure of S. aureus. Studies have identified over 2200 sequence types (STs) of S. aureus using the MLST techniques. The STs can be grouped into clonal complexes (CC). Several studies have indicated that majority of the livestock-associated STs belong to a small number of animal-associated clones. For example, CC97, ST151, CC130, and CC126 are commonly found on bovine infections. CC133 are common among small-ruminants such as sheep or goats. ST1, ST8, CC5, ST 121, and ST398 are found in human host species [41]. ST5 is predominant among poultry isolates [42]. CC133 and ST522 are mostly implicated with mastitis in sheep and goats. One Danish study indicated that ST133 was the predominant lineage in sheep and goats [42].

5. Contributing Factors

In the United States, approximately 30% and 1.5% of the population are colonized with methicillin-susceptible S. aureus (MSSA) [43] and MRSA, respectively, [43–45] with the most important site for colonization being the anterior nares (nostrils) [46]. While colonization itself does not harm the host, it is a risk factor for developing subsequent symptomatic infections [43, 47]. These colonized healthy persons categorized as persistent carriage and intermittent carriage serve as S. aureus careers and are able to transmit the bacterium to susceptible persons [46].

S. aureus is a common causative agent of bovine mastitis in dairy herds. A study conducted in Minnesota to estimate the heard prevalence of S. aureus from bulk tank milk found that heard prevalence of MSSA and MRSA was 84% and 4%, respectively [48]. Other studies estimated that the prevalence of S. aureus in bulk milk tank was 31% in Pennsylvania and 35% in cow milk samples in Louisiana [48]. Studies from Argentina [49], Brazil [50], Ireland [51], and Turkey [52] have documented the presence of staphylococcal enterotoxin genes and production of SEs by S. aureus of bovine origin. The udders with clinical and subclinical staphylococcal mastitis can contribute to the contamination of milk by S. aureus via direct excretion of the organisms in the milk [38] with large fluctuations in counts ranging from zero to 10 8 CFU/mL [53]. For example, cattle mastitis was the sole source of contamination in 1999 S. aureus outbreak in Brazil that affected 328 individuals who consumed unpasteurized milk [54]. Similarly, 293 S. aureus isolates were recovered from 127 bulk tank milk samples of goats and sheep from Switzerland [38]. Recently, S. aureus isolates were recovered from mammary quarter milk of mastitic cows and from bulk tank milk produced on Hungarian dairy farms indicating that S. aureus from infected udders may contaminate bulk milk and, subsequently, raw milk products [53]. However, S. aureus contamination in milk can occur from the environment during handling and processing of raw milk as well [53].

Improper food handling practices in the retail food industry are thought to contribute to a high number of FBD outbreaks [55]. Studies have indicated that the majority of FBD outbreaks result from such practices [55, 56]. It was reported that the hands of food handlers were implicated in 42% of food-borne outbreaks that occurred between 1975 and 1998 in the United States [55, 57].

In a recent study [13] investigating the microbiological contamination in ready-to-eat food products processed at a large processing plant in Trinidad, West Indies, S. aureus was the most common pathogen detected. S. aureus was isolated from precooked food samples of franks, bologna, and bacon and postcooked bologna and bacon. The overall prevalence of S. aureus detected in air, food, and environmental samples was 27.1% (46/170). It was determined that the counts of S. aureus increased after heat treatment, and only postcooking environmental surfaces that came into contact with ready-to-eat foods that were contaminated with S. aureus during slicing and packaging harbored S. aureus. S. aureus was also frequently found on food handler’s gloves [13]. Pathogenic microbes can adhere to the surface of the gloves worn by retail food employees and can serve as a source of cross-contamination if not changed frequently [55]. The practice of wearing gloves without proper hand washing can contaminate both the interior and exterior of the gloves. Hand washing is often neglected when gloves are used, which may promote rapid microbial growth on the hands as gloves provide a warm, moist environment for bacterial growth on the hands [55, 57]. Hand-washing, an easy method of preventing many microbial contamination, is too often forgotten [55].

The finding of high bacterial counts in the air and on food contact surfaces in the postprocessing environment is suggestive of cross-contamination of postcooked products and is the most important risk factor affecting microbiological quality of food [13]. A study [58] found that processed foods that require more handling during preparation are more vulnerable to S. aureus contamination [13]. Another study [59] demonstrated that increased human handling contributed to contamination by S. aureus in a pork processing plant.

Analysis of the data of FBD outbreaks reported to the Food-borne Disease Outbreak Surveillance System during 1998 to 2008 [5] indicate that meat and poultry dishes were the most common foods (55% of S. aureus outbreaks) reported in S. aureus outbreaks in the United States. Foods implicated with S. aureus outbreaks were most often prepared in a restaurant or deli (44%). Errors in food processing and preparation (93%) were the most common contributing factor in FBD outbreaks. Forty-five percent and 16% of these errors occurred in restaurants and delis and homes or private residences, respectively. The study identified various errors in food processing and preparation that include (i) insufficient time and temperature during initial cooking (40%) hot holding (33%) and reheating process (57%) (ii) prolonged exposure of foods at room or outdoor temperature (58%) (iii) slow cooling of prepared food (44%) (iv) inadequate cold holding temperatures (22%) (v) and preparing foods for extended periods of time prior to serving [5]. Cross-contamination in the vicinity of food preparation and processing was another contributing factor in S. aureus food-borne outbreaks. Insufficient cleaning of processing equipment or utensils (67%) and storage in contaminated environments (39%) were the most common errors reported [5].

6. Farm, Food, and Beyond

In recent years, a new strain of S. aureus, livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA), has been recognized as a novel pathogen that has become a rapidly emerging cause of human infections [60, 61]. LA-MRSA was first detected in 2005 in swine farmers and swine in France and in The Netherlands [62–64]. Researchers have isolated LA-MRSA from number of countries in Asia [65–67], Europe [68–74], and North America [75, 76]. Studies have found increased human colonization and infection of LA-MRSA belonging to the multilocus sequence type 398 (ST398) lineages in livestock-dense areas in Europe [77–80]. Investigators in The Netherlands have shown that ST398 now accounts for 20% of human MRSA cases [81] and this strain accounts for 42% of newly detected MRSA in that country, suggesting that animals may be an important reservoir for human MRSA infections [77]. Compared to the general population, Dutch pig farmers are 760 times more likely to be colonized with MRSA [82].

In several studies, MRSA has been found at high levels on US and European farms and in commercially-distributed meats, emerging as a potential concern for meat handlers and consumers [28, 64, 68, 75–77, 83–88]. Several species of meat-producing animals are frequently implicated including pigs [68, 75, 76], poultry [89–91], and cattle [73, 92]. The presence of MRSA on raw retail meat products is well documented, with prevalence ranging from less than 1 percent in Asia [93, 94] to 11.9% in The Netherlands [95], with intermediate prevalence found in other studies [87, 96, 97]. A recent study carried out in the United States found that 45% (45/100) of pork products and 63% (63/100) of beef products tested in Georgia were positive for S. aureus. The MRSA prevalence in this study was 3% and 4% in retail pork and beef, respectively [28]. Another US study testing retail meat in Louisiana isolated MRSA from 5% (6/120) of meat samples tested, while 39.2% (47/120) of samples were positive for any type of S. aureus [87]. Very high prevalence of S. aureus (64.8%, 256/395) was observed on retail pork products collected from Iowa, Minnesota, and New Jersey [85]. The prevalence of MRSA in this study was 6.6%. Other studies in US have found S. aureus in 16.4% (27/165) and MRSA in 1.2% (2/165) of meat samples [84], multidrug resistant (MDR) S. aureus in 52% (71/136) of meat and poultry samples [86], and any S. aureus in 22.5% (65/289) and MRSA in 2% (6/289) of meat and poultry samples [88]. These studies provide some insights regarding the role of commercially distributed meat as a potential vehicle for S. aureus transmission from the farm into the general human population.

The first report of an outbreak of gastrointestinal illness caused by a community-acquired methicillin resistant S. aureus in the United States affected 3 members of the same family. Contaminated coleslaw from an asymptomatic food handler was the source of MRSA [6, 33]. All 3 members of the family who ate foods (shredded pork barbeque and coleslaw) 30 minutes after purchasing at a convenient-market delicatessen developed gastrointestinal symptoms. The S. aureus isolates recovered from the stool samples of the three ill family members and coleslaw and nasal swab of food preparer were identical in PFGE analysis. The implicated strain produced Staphylococcal toxin C and was identified as MRSA [33].

This outbreak provides an evidence of MRSA-contaminated foods as the vehicle in the clusters of illness affecting low-risk persons within the community. The food handlers involved in this outbreak had visited a nursing home. It is important to note that many S. aureus isolates obtained as a part of outbreak investigation may not be tested for antibiotic susceptibility, as antibiotics are not used in the treatment regimen. As such, it is plausible that food-borne outbreak caused by methicillin-resistant strains of S. aureus may go unnoticed. Previously food has been implicated as a source of MRSA transmission in one outbreak of blood and wound infections in hospitalized immunocompromised patients [33, 98].

7. Gaps in Research

Many outbreak investigations successfully traced food handlers as a source of contamination matching the strains of S. aureus in food products and handlers. However, these retrospectively carried-out studies have some limitations and cannot ascertain that the handler was not also colonized due to the exposure to S. aureus contaminated food.

Although numerous studies have focused on documenting risk imposed by S. aureus toxins in food industry and consumers’ health, little is known about the potential role of intact bacteria transmitted through the raw meat products and self-inoculation into the nasal cavity of food industry workers and consumers. Additionally, while research has shown the potential for transmission of S. aureus within the home setting [99, 100], the relationship of colonization and transmission of this organism to the food products brought into the home has not been investigated.

Several European studies investigating MRSA in retail meat found ST398 as the most common MRSA type [95, 97, 101]. It has been suggested that meat might be a potential vehicle for the transmission of ST398 from the farm into the community, but additional research needs to be carried out to test this hypothesis.

Researchers have isolated other non-ST398 strains of S. aureus such as ST8, a strain which includes USA 300, the primary cause of community-associated MRSA infections, from US swine farms [102] and retail meat [28, 84–88]. However, it is not clear whether human handlers played any role during the postslaughter processing for the contamination of meat positive for ST8. It is suggested that since S. aureus is also present in intestinal tract [103], raw meat may contain MRSA due to the carcasses contaminated with intestinal content during slaughtering process [95]. Finding of human-associated strains of MRSA from raw chicken meat in Japan and Korea provides some support to this hypothesis [89, 93, 94].

Only few studies have been conducted specifically to investigate the implication of MRSA in SFD [19]. Although MRSA was frequently isolated from food production animals and raw retail meat, the relevance of its contamination is unknown. Further study is warranted to investigate the likelihood of gastrointestinal colonization and extraintestinal infection subsequent to the consumption of foods contaminated with MRSA [104]. Since S. aureus isolates obtained from SFD outbreaks may not be tested for antibiotic susceptibility, the true prevalence of MRSA involved in SFD is unknown [33]. Since other Staphylococcal species are also able to produce SEs and are not routinely tested, further research is warranted [2].

8. Prevention

SFD is preventable [10]. Consumers need to be aware of potential food contamination in home and during cooking in kitchen. Cooking food thoroughly is important, but preventing contamination and cross-contamination and maintaining critical points are the most effective ways to prevent SFD. Since research findings and outbreak investigations have suggested that SFD is largely due to faulty food handling practices, knowledge and skills in food industry workers are warranted. Nevertheless, public health intervention should be designed to prevent S. aureus from pre- and postslaughter in meat processing facilities. Public awareness regarding safe meat handling would help to prevent cross-contamination [104] as well as potential colonization of handlers from contaminated food products. Other public health interventions such as personalized and tailored food safety education program targeting diverse sociodemographic people could be a cornerstone in preventing the SFD outbreak [10].

1985’s staphylococcal food poisoning due to contaminated chocolate milk in Kentucky, USA, and 2000’s extensive outbreak of staphylococcal food poisoning due to contaminated low-fat milk in Japan, are the classical examples of SFD that illustrate the stability and heat resistance of SEs as well as the importance of illumination of any contamination sources during the processing and refrigeration of food and food ingredients. In both cases, high temperature used in pasteurization killed the bacteria but had no effect on SEs [2, 31].

The permissive temperature for the growth and toxin production by S. aureus is between 6°C and 46°C. Thus, the ideal cooking and refrigerating temperature should be above 60°C and below 5°C, respectively. A study reviewing the performance of domestic refrigerators worldwide found that many refrigerators were running above the recommended temperature [105]. Another study conducted in Portugal found that more than 80% of participants cleaned their fridge only monthly [106]. While these studies indicate the need of consumer awareness in food safety, other preventive measures such as the practice of serving food rapidly when kept at room temperature, wearing gloves, masks, hairnets during food handling and processing, frequent hand washing, good personal hygiene of food handlers, and use of “sneeze-bars” at buffet tables could help prevent SFD [22, 58].

Maintaining the cold chain is essential for preventing the growth of S. aureus in food products [5]. Other preventive measures such as control of raw ingredients, proper handling and processing, adequate cleaning, and disinfection of equipment used in food processing and preparation should be deployed [19, 104]. Strict implementation and adherence to the microbiological guidelines such as Hazard Analysis and Critical Control Points (HACCP), Good Manufacturing Practice (GMPs), and Good Hygienic Practices (GHPs) developed by World Health Organization and United States Food and Drug Administration can help to prevent S. aureus contamination [13, 107].

9. Conclusion

SFD is one of the most common causes of FBD worldwide. Outbreak investigations have suggested that improper handling of cooked or processed food is the main source of contamination. Lack of maintaining cold chain allows S. aureus to form SEs. Although S. aureus can be eliminated by heat treatment and by competition with other flora in pasteurized and fermented foods, respectively, SEs produced by S. aureus are still capable of causing SFD because of their heat tolerance capacity. This fact should be considered in risk assessment and devising appropriate public health interventions. Prevention of S. aureus contamination from farm to fork is crucial. Rapid surveillance in the event of SFD outbreak and ongoing surveillance for the routine investigation of S. aureus and SEs implicated in food products along with improved diagnostic methods could help to combat the SFD in 21st century. Recent findings of high prevalence of S. aureus including MRSA in raw retail meat impose a potential hazard to consumers, both as classic SFD and as a potential source of colonization of food handlers. Further study is required to fill the research gap.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.


This work was partially funded by Agriculture and Food Research Initiative Competitive Grant no. 2011-67005-30337 (TCS) from the USDA National Institute of Food and Agriculture.


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In December 2019, SARS-CoV-2 was initially detected in patients who suffered from unusual viral pneumonia in Wuhan, Hubei, China (Kaul, 2020 Naserghandi et al., 2020 Petrosillo et al., 2020). The virus was first named 2019 novel coronavirus (2019-nCoV) by the WHO and later, when it was found that 86.9% of the novel virus genome was similar to the SARS-CoV genome, the virus was renamed SARS-CoV-2 (Chang et al., 2020 The Lancet Infectious Diseases, 2020). COVID-19 is the clinical syndrome caused by SARS-CoV-2 infection which is characterized by a respiratory disease with symptoms ranging from mild influenza (flu-like) to severe pneumonia and acute respiratory distress syndrome (Petrosillo et al., 2020). The clinical manifestations of COVID-19 are non-specific and variable among patients, and between countries. Generally, COVID-19 symptoms involve fever, sore throat, runny or stuffy nose, dry cough, headache, myalgia or fatigue, sputum production, dyspnea, chest pain or pressure, joint pain, chills, loss of taste or smell, and a rash on the skin or discoloration of toes or fingers. Abdominal pain, dizziness, diarrhea, nausea, and vomiting are less common symptoms (Kaul, 2020 Naserghandi et al., 2020 Petrosillo et al., 2020). Borges do Nascimento et al. (2020) found that COVID-19-related symptoms among 59,254 patients in 61 studies were: fever (82%), cough (61%), muscle aches and/or fatigue (36%), dyspnea (26%), headache (12%), sore throat (10%), and gastrointestinal symptoms (9%). On average, the incubation period takes 5𠄶 days for a patient to show the symptoms after infection, however, it may reach up to 14 days (World Health Organization [WHO], 2020).

COVID-19 infection is highly contagious among the population and now almost all countries have reported cases and deaths. On March 11, 2020, COVID-19 was characterized as a pandemic by the WHO. As of early July, over 12 million confirmed cases and 550,000 deaths of COVID-19 have been reported worldwide (World Health Organization [WHO], 2020).

Journal of Microbiology, Biotechnology and Food Sciences

News: Dear colleagues, JMBFS journal is coming with new publishing format: Articles in Press. All accepted articles will publish in Articles in press issue without Volume and Issue number. Articles gets DOI number immediately. Papers will publish here:

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The Journal of Microbiology, Biotechnology and Food Sciences (ISSN 1338-5178) is an Open Access, peer-reviewed online scientific journal published by the Faculty of Biotechnology and Food Sciences (Slovak University of Agriculture in Nitra) from 2011. The major focus of the journal is regular publishing of original scientific articles, short communications and reviews about animal, plant and environmental microbiology (including bacteria, fungi, yeasts, algae, protozoa and viruses), microbial, animal and plant biotechnology and physiology, microbial, plant and animal genetics, molecular biology, agriculture and food chemistry and biochemistry, food control, evaluation and processing in food science and environmental sciences.

Journal of Microbiology, Biotechnology and Food Sciences is published 6 times per year in electronic version only as PDF file and preprint version as html version. We are publishing cca 120 publication per year.

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Watch the video: How a few scientists transformed the way we think about disease - Tien Nguyen (July 2022).


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