Interactions between probiotics and pathogenic microorganisms in hosts and foods: A review

https://doi.org/10.1016/j.tifs.2019.11.022Get rights and content

Highlights

  • Probiotics are microorganisms with great health benefits and protect host against foodborne illness.

  • The demand for food products containing probiotic is continuously increasing.

  • The effectiveness is associated with the interaction with pathogens, host's immune system and GUT.

  • Delivery systems can protect probiotics from environmental stress and enhance their efficiency.

Abstract

Background

Foodborne diseases can be highlighted as one of the most significant health concerns among the last decades. Probiotic food products can be considered as the promising approaches for modulating of gastrointestinal (GIT) microbiota due to their interactions within the GIT. However, no comprehensive review regarding the involved mechanisms in inhibiting foodborne pathogens in foods by probiotics, besides their interaction is available.

Scope and approach

The current article provides an overview considering the interactions between probiotics and pathogens in hosts as well as in foods aiming to gain insights regarding relevant properties to be used in further developments of probiotic-based food products.

Key findings and conclusions

The interaction between probiotics and pathogens in foods and in the hosts and different mechanism of probiotics in control of enteric pathogens colonization were reviewed in the current study. While the mechanisms of action correlated with probiotic strains in the GIT are diverse and well-studied, their interactions with pathogens in foods is overlooked. Revealing how probiotic strains interact with foodborne pathogens in foods is of key relevance in a contemporary context that demand the development of more robust formulations. Although several mechanisms such as production of substances such as organic acids, bacteriocins, and hydrogen peroxide have been suggested regarding probiotics actions in food matrices, still substantial challenges exist concerning the molecular mode of their antimicrobial action. Additionally, it is required to comprehend the appreciate dose, species, and a combination of probiotics in controlling the pathogens.

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).

References (147)

  • Y.H. Chiu et al.

    Characterisation of bifidobacteria with immunomodulatory properties isolated from human breast milk

    Journal of functional foods

    (2014)
  • C. Collazo et al.

    Effect of Pseudomonas graminis strain CPA-7 on the ability of Listeria monocytogenes and Salmonella enterica subsp. enterica to colonize Caco-2 cells after pre-incubation on fresh-cut pear

    International Journal of Food Microbiology

    (2017)
  • A.B. Dantas et al.

    Manufacture of probiotic minas frescal cheese with lactobacillus casei zhang

    Journal of Dairy Science

    (2016)
  • L.J. Fooks et al.

    Prebiotics, probiotics and human gut microbiology

    International Dairy Journal

    (1999)
  • A. Gálvez et al.

    Bacteriocin-based strategies for food biopreservation'

    International Journal of Food Microbiology

    (2007)
  • Y. Haraguchi et al.

    Inhibitory effect of Lactobacillus plantarum Tennozu-SU2 and Lactococcus lactis subsp. lactis BF1 on Salmonella Typhimurium and Listeria monocytogenes during and post fermentation of soymilk

    LWT- Food Science and Technology

    (2019)
  • M.I. Hossain et al.

    Probiotics as potential alternative biocontrol agents in the agriculture and food industries, a review

    Food Research International

    (2017)
  • M.B. Iglesias et al.

    Adhesion and invasion of Listeria monocytogenes and interaction with Lactobacillus rhamnosus GG after habituation on fresh-cut pear

    Journal of Functional Foods

    (2017)
  • F.F. Jia et al.

    Complete genome sequence of bacteriocin-producing Lactobacillus plantarum KLDS1. 0391, a probiotic strain with gastrointestinal tract resistance and adhesion to the intestinal epithelial cells

    Genomics

    (2017)
  • R. Kaji et al.

    Probiotic induction of interleukin-10 and interleukin-12 production by macrophages is modulated by co-stimulation with microbial components

    Journal of Dairy Science

    (2018)
  • R.M. Kamal et al.

    Bio-controlling capability of probiotic strain Lactobacillus rhamnosus against some common foodborne pathogens in yoghurt

    International Dairy Journal

    (2018)
  • B. Karska-Wysocki et al.

    Antibacterial activity of Lactobacillus acidophilus and Lactobacillus casei against methicillin-resistant Staphylococcus aureus (MRSA)

    Microbiological Research

    (2010)
  • M. Kawahara et al.

    Anti-inflammatory properties of fermented soy milk with Lactococcus lactis subsp. lactis S-SU2 in murine macrophage RAW264. 7 cells and DSS-induced IBD model mice

    International Immunopharmacology

    (2015)
  • M.E. Kiymaci et al.

    Quorum sensing signals and related virulence inhibition of Pseudomonas aeruginosa by a potential probiotic strain's organic acid

    Microbial Pathogenesis

    (2018)
  • J.-P. Lavigne et al.

    Molecular evolution of Salmonella enterica serovar Typhimurium and pathogenic Escherichia coli, from pathogenesis to therapeutics

    Infection, Genetics and Evolution

    (2008)
  • S.M. Lim et al.

    A mixture of the probiotic strains Bifidobacterium longum CH57 and Lactobacillus brevis CH23 ameliorates colitis in mice by inhibiting macrophage activation and restoring the Th17/Treg balance

    Journal of Functional Foods

    (2016)
  • A.R. Madureira et al.

    Effect of the incorporation of salted additives on probiotic whey cheeses

    Food Bioscience

    (2015)
  • M.S. Marcial-Coba et al.

    Dried date paste as carrier of the proposed probiotic Bacillus coagulans BC4 and viability assessment during storage and simulated gastric passage

    LWT- Food Science and Technology

    (2019)
  • P.L.H. McSweeney et al.

    Metabolism of residual lactose and of lactate and citrate

    Cheese, Chemistry, Physics and Microbiology

    (2004)
  • P. Nadelman et al.

    Probiotic fermented sheep's milk containing Lactobacillus casei 01, Effects on enamel mineral loss and Streptococcus counts in a dental biofilm model

    Journal of Functional Foods

    (2019)
  • T.A.J. Oelschlaeger

    Mechanisms of probiotic actions–a review

    International Journal of Medical Microbiology

    (2010)
  • M.Á. Abengózar et al.

    Enterocin AS-48 as evidence for the use of bacteriocins as new leishmanicidal agents

    Antimicrobial Agents and Chemotherapy

    (2017)
  • K. Abhari et al.

    The effects of prebiotic, probiotic and synbiotic diets containing Bacillus coagulans and inulin on serum lipid profile in the rat

    Veterinary Science Development

    (2015)
  • I. Adlerberth et al.

    Establishment of the gut microbiota in Western infants

    Acta Paediatrica

    (2009)
  • C. Aguilar et al.

    Antagonistic effect of Lactobacillus strains against Escherichia coli and Listeria monocytogenes in milk

    Journal of Dairy Research

    (2011)
  • C.N. Almada et al.

    Characterization of the intestinal microbiota and its interaction with probiotics and health impacts

    Applied Microbiology and Biotechnology

    (2015)
  • A. Amaretti et al.

    Antioxidant properties of potentially probiotic bacteria, in vitro and in vivo activities

    Applied Microbiology and Biotechnology

    (2013)
  • O.A. Arias et al.

    Antagonistic effect of probiotic strains against two pathogens, Salmonella Typhimurium and E. coli O157, H7 resistant to antibiotics

    E-Gnosis

    (2013)
  • T. Asahara et al.

    Probiotic bifidobacteria protect mice from lethal infection with Shiga toxin-producing Escherichia coli O157, H7

    Infection and Immunity

    (2004)
  • M. Bielaszewska et al.

    Effects of antibiotics on Shiga toxin 2 production and bacteriophage induction by epidemic Escherichia coli O104, H4 strain

    Antimicrobial Agents and Chemotherapy

    (2012)
  • N.E. Bondareva et al.

    The role of chlamydial colonization of the gastrointestinal tract in the development and persistence of chronic chlamydial infections

    Molecular Genetics, Microbiology and Virology

    (2018)
  • M. Brown

    Modes of action of probiotics, recent developments

    Journal of Animal and Veterinary Advances

    (2011)
  • L. Brown et al.

    YebC, a putative transcriptional factor involved in the regulation of the proteolytic system of Lactobacillus

    Scientific Reports

    (2017)
  • K.F. Budden et al.

    Emerging pathogenic links between microbiota and the gut–lung axis

    Nature Reviews Microbiology

    (2017)
  • C. Caballero-Franco et al.

    The VSL# 3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells

    Liver Physiology

    (2007)
  • P. Calo-Mata et al.

    Current applications and future trends of lactic acid bacteria and their bacteriocins for the biopreservation of aquatic food products

    Food and Bioprocess Technology

    (2008)
  • D. Campaniello et al.

    How to routinely assess transition, adhesion and survival of probiotics into the gut: A case study on propionibacteria

    International Journal of Food Science and Technology

    (2018)
  • S. Carding et al.

    Dysbiosis of the gut microbiota in disease

    Microbial Ecology in Health and Disease

    (2015)
  • CDC

    Surveillance for foodborne disease outbreaks, United States, 2013, annual report

    (2015)
  • N. Chammem et al.

    Food crises and food safety incidents in European Union, United States, and Maghreb Area, current risk communication strategies and new approaches

    Journal of AOAC International

    (2018)
  • Cited by (0)

    View full text