Interactions between probiotics and pathogenic microorganisms in hosts and foods: A review
Graphical abstract
Introduction
Foodborne diseases can be considered as one of the most critical public health issues around the world (CDC, 2015). Despite the development in the areas of medicine, nutrition and food science and technology, foodborne disease cases and outbreaks caused by foodborne pathogens still cause severe public health and economic burdens (Hossain, Sadekuzzaman, & Ha, 2017). Some foodborne pathogens especially bacteria, may be very risky due to the high mortality rates associated, while others may present high-frequency occurrence (Budden et al., 2017). Another contemporary concern is the increased report regarding the cases on the occurrence of antibiotic-resistant human pathogens as a consequence of spread use of synthetic antibiotics (Andersson, Hughes, & Kubicek-Sutherland, 2016; Chammem, Issaoui, Almeida, & Delgado, 2018).
The gut can be considered as the main site of action of the most important bacterial pathogens transmitted via foods. The commonest symptoms are diarrhea, vomiting, fever and headache even though in some cases foodborne diseases can result to neurologic problems or even death (Duarte et al., 2018). Several of these diseases have been linked with a misbalanced gastrointestinal (GIT) microbiota (Valdes, Walter, Segal, & Spector, 2018; Carding, Verbeke, Vipond, Corfe, & Owen, 2015; Danneskiold-Samsøe et al., 2019). In this regard, several strategies have been considered for dealing with these diseases and for the recovery of the balance of gut microbiota (Danneskiold-Samsøe et al., 2019). One of these strategies is the consumption of probiotics, either as supplements or through food products (Esaiassen et al., 2018; de Almada, Martinez, & Sant’Ana, 2015).
It has been well demonstrated that probiotics, principally probiotic strains of lactic acid bacteria (LAB), can modulate the human GIT microbiota through inhibiting the growth of opportunistic bacteria (Lau & Chye, 2018; Liévin-Le Moal, 2016). Thus, the stimulation of the growth and activity of probiotic strains in GIT can be considered a potential approach to control foodborne enteric pathogens (Peng & Biswas, 2017).
In this context, the probiotics have different mechanisms of action against foodborne pathogens in GIT. According to recent investigations, the antimicrobial activity of probiotic strains could be correlated with producing or releasing antimicrobial substances such as lactic acids, antimicrobial peptides, and hydrogen peroxide. The so-called bacteriocin-like inhibitory substances (BLIS) are among natural food bio preservatives which could play an important role in the inhibition of several foodborne pathogens (Martinez, Domínguez, Converti, & Oliveira, 2015). Moreover, probiotics can significantly reduce the invasiveness of pathogens by either competing for host cell receptors or even secreting antioxidants. Also, the probiotics can play their antimicrobial role through changing the gene expression that is responsible for colonization of enteric bacterial pathogens. Results of studies revealed that low concentrations of polyunsaturated fatty acids (PUFAs) and short-chain fatty acids (SCFAs) mainly butyrate, might probably decrease the pathogenicity of Enterohemorrhagic E. coli (EHEC) by changing in genes which encoded chromosomal pathogenicity and supports the creation of lesions on the mucosal epithelium. High amounts of butyrate excreted by probiotics also can significantly prevent the transcription of L. monocytogenes virulence genes which are responsible for intestinal colonization (Sun, Wilkinson, Standiford, Akinbi, & O’Riordan, 2012). SCFAs in both ex vivo and in vivo models have shown the ability to prevent the invasion of Campylobacter jejuni by regulation of nonspecific virulence gene expression. Shreds of evidence demonstrated certain metabolites such as butyrate and SCFAs produced by probiotics can down-regulate expression of virulent genes of Salmonella Enteritidis and S. Typhimurium (Peng & Biswas, 2017). Even though the mechanisms of probiotics interaction and bacterial pathogens in the GIT have been well elucidated (Plaza-Diaz, Ruiz-Ojeda, Gil-Campos, & Gil, 2019), while the interactions of probiotic bacteria and bacterial pathogens in foods has not been approached. A bunch of foods has been recently investigated regarding their potential approaches to carry probiotic microorganisms, including meat, dairy, vegetables, and beverages (Marcial-Coba, Pjaca, Andersen, Knøchel, & Nielsen, 2019; Rivera-Espinoza & Gallardo-Navarro, 2010; Espitia-De La Hoz 2016). However, little information is available considering factors which play key roles in the interaction between probiotics and foodborne pathogens in foods. That information could be used to further enhance the development of probiotic strains that may also contribute with the development of more robust formulations. In this context, the current review was aimed to provide insights regarding the interactions between probiotic microorganisms and foodborne pathogens in hosts and foods. The overall concepts and characteristics of probiotics and foodborne pathogens, as well as the action mechanism of probiotics on pathogens, human host and foods are underlined.
Section snippets
Foodborne illness – a persistent problem
Foodborne illness takes place as a result of food contamination by pathogenic microorganisms during the food supply chain, pre, and post-harvest procedures; production, distribution and even before consumption. Depending on the food and storage conditions, growth can take place up to levels required to demonstrate the symptoms of disease. They may affect only a single person or sometimes could cause some outbreaks (Hall et al. 2012). Also, foodborne diseases are among most notable concerns for
Host's GIT microbiota
The intestinal microbiota plays a significant role in the homeostasis of humans. This microbiota acquires a unique community during the first year of life and keeps steadily developing throughout childhood and adolescence. During this first year, bacterial colonization of the infant's gut occurs in utero (Gosalbes et al., 2013), and microbial growth dramatically increases during the first months of life (Fallani et al., 2010). However, during this period, abnormal development of intestinal
Probiotics: origin, definition, and characteristics
The word “probiotic” comes from the Greek language “pro” and “bios” which means “for life,” which is opposite of “antibiotics” which means “against life”. The probiotic as life promoters naturally could improve the overall health state of the host organism (Fig. 1) (Sanders, 2008). This statement was first theorized by Elie Metchnikoff over a century ago. According to Elie Metchnikoff, the health could be improved by manipulating the intestinal microbiome using host-friendly bacteria (
Probiotics in food products
The probiotics have been widely approached in the food industry as well as nutrient studies as an appropriate solution to overcome the common issues mainly about gastrointestinal disorders and their response to enteral infections such as treatment of diarrhea. Due to several prompted health benefits such as antimicrobial and antioxidant activities in addition to further improvements in the immunosuppression; the consumption of probiotics in different forms among a wide range of customers was
Food pathogens and pathogenicity mechanisms
Human food and water supplies can be easily contaminated by a broad range of microbial pathogens and cause severe illness due to their ingestion or uptake of their toxins. The vast range of foodborne pathogens, including bacteria, viral pathogens, and parasites, as well as marine dinoflagellates, can result in some health issues (Smith & Fratamico, 2018). Among all, bacterial pathogens are known to cause the most foodborne outbreaks. In addition to new emerging infectious diseases, the
Interaction between probiotics and pathogenic bacteria in the host GIT tract
The interaction between probiotics and pathogens can be categorized in three steps; the physical interaction between the probiotic and the epithelium; the interaction between probiotics and the immune system and, finally, direct interaction between bacteria-bacteria (probiotic-pathogens) as shown in Fig. 2 (Oelschlaeger, 2010; Salminen et al., 2010). Although probiotics may interact with pathogens in different ways, directly or indirectly, their consumption could offer health benefits.
Interaction between probiotics and pathogenic bacteria in the foods
Nowadays, bio-preservation is an alternative approach to improve the safety of food products comparing to chemical preservation methods (Fig. 3). Bio-preservation is the term of using beneficial microorganisms in food matrices to inhibit the proliferation of undesirable microorganisms. Although the exact routes that enabled probiotics to control the growth of opportunistic microorganisms are still obscure, production of substances such as organic acids, bacteriocins, and hydrogen peroxide is
Interaction between probiotics and foodborne viruses
GIT viral pathogens are another source of food-related illnesses. Several global outbreaks of acute gastroenteritis caused by noroviruses and rotaviruses, especially in children, have been reported. Although acute diarrhea in children is often self-limiting within a few days, the risk of developing dehydration in toddlers and young infants, deteriorate general health. Extensive clinical studies suggest specific probiotics reduce the risk and shorten the length of norovirus or
Interaction between probiotic microorganisms and food matrices
As the benefits of probiotic bacteria in food products has been explored more after its direct consumption, its industrial applications also increase (El Hage, Hernandez-Sanabria, & Van de Wiele, 2017). The impact of probiotics on food quality has been less investigated and has been studied recently. The investigation of this aspect is critical due to its significant influence on consumer acceptability.
Overall, among probiotic foods carriers, whey matrices offer a suitable condition for
Concluding remarks
Despite the recent advancements in preventing foodborne diseases via decreasing contamination of water, food and ready to eat products, still foodborne pathogens are a global concern. In recent decades, implementing the food safety using new approaches such as incorporating of probiotics in food matrices, bio-preservation, is a preference option comparing to traditional preservation methods. The interaction between probiotics and pathogens in foods and in the hosts and different mechanism of
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
The authors would like to thank the support of Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Grants #302763/2014-7 and #305804/2017-0). This study was financed, in part, by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. M. B. Soares acknowledges the financial support from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Grant #13/21544-9).
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