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Protecting against pneumococcal disease: critical interactions between probiotics and the airway microbiome.

Licciardi PV, Toh ZQ, Dunne E, Wong SS, Mulholland EK, Tang M, Robins-Browne RM, Satzke C - PLoS Pathog. (2012)

View Article: PubMed Central - PubMed

Affiliation: Pneumococcal Research, Murdoch Childrens Research Institute, Royal Children's Hospital, Melbourne, Australia. paul.licciardi@mcri.edu.au

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Streptococcus pneumoniae (the pneumococcus) is a predominant cause of pneumonia, meningitis, and bacteremia... Most deaths occur in African and Asian developing countries; however, pneumococcal disease is also a significant problem in particular populations of developed countries, such as the North American Indians, and indigenous Alaskans and Australians –... In this opinion piece, we discuss the potential complementary role of probiotics to vaccines in preventing pneumococcal disease through targeting the microbiome of the upper respiratory tract... A prerequisite for pneumococcal disease is adherence of the bacterium to host nasopharyngeal epithelium leading to colonization (carriage)... It has now been demonstrated that in early infancy, colonization with pneumococci prior to conjugate vaccination causes impaired immune responses to the carried serotype, ... Exploiting the beneficial effects of probiotics on microbial colonization and immunity represents a novel approach to prevent or reduce pneumococcal colonization and disease... The World Health Organization (WHO) defines probiotics as live micro-organisms that confer a health benefit to the host and are generally regarded as safe in humans... In otitis media-prone children given antibiotics prior to oral treatment with a powdered S. salivarius K12 formula, 33% were newly colonized with K12 while two of 19 children were shown to expand the pre-existing S. salivarius population... No impact on clinical outcomes was reported in this study, and the small sample size used makes it difficult to draw meaningful conclusions... In contrast, when otitis-prone children (n = 155) were given a daily probiotic mix containing LGG, L. rhamnosus LC705, B. breve 99, and Propionibacterium freudenreichii JS for 24 weeks, no effect on nasopharyngeal carriage of otitis pathogens was observed... Furthermore, this probiotic formula did not prevent the occurrence of otitis media in these children, although there was a trend of reduced recurrent respiratory infections... To date, the effect of probiotics on the gastrointestinal microbiome have provided the best evidence for host–microbe interactions such as pathogen exclusion, enhanced mucus secretion, production of anti-bacterial factors, and modulation of host immunity... However, no change in diphtheria toxoid or tetanus toxoid IgG levels was observed, suggesting that the effects of probiotics may vary depending on the vaccine antigen used... Recently, Lactobacillus casei was reported to significantly enhance the pneumococcal protective protein A (PppA)-specific IgG and IgA response in the serum and mucosa following nasal vaccination with PppA and was associated with a significantly reduced pathogen load in the nasal lavage by day 42 post-immunization.

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Paradigm for the proposed biological effects of probiotic bacteria in protection against pneumococcal infection.Commensal and/or probiotic bacteria can prevent pathogens (pneumococci) from attaching to and colonizing the respiratory epithelium by associating with specific cell surface receptors and by enhancing mucus secretion and the production of secretory IgA. Probiotic bacteria interact with underlying dendritic cells (DCs) which signal to the adaptive immune system to trigger a variety of effector cell types, including Th1, Th2, and Th17 as well as regulatory T cells and B cells depending on the local cytokine/chemokine microenvironment. Furthermore, probiotic bacteria also maintain the epithelial barrier integrity by upregulating the expression of specific tight junction proteins on damaged epithelium as a result of localized inflammatory responses following pathogen (pneumococcal) encounter and invasion. Refer to references [49]–[52] for more detail on probiotic–host effects. Th, T helper cell.
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ppat-1002652-g001: Paradigm for the proposed biological effects of probiotic bacteria in protection against pneumococcal infection.Commensal and/or probiotic bacteria can prevent pathogens (pneumococci) from attaching to and colonizing the respiratory epithelium by associating with specific cell surface receptors and by enhancing mucus secretion and the production of secretory IgA. Probiotic bacteria interact with underlying dendritic cells (DCs) which signal to the adaptive immune system to trigger a variety of effector cell types, including Th1, Th2, and Th17 as well as regulatory T cells and B cells depending on the local cytokine/chemokine microenvironment. Furthermore, probiotic bacteria also maintain the epithelial barrier integrity by upregulating the expression of specific tight junction proteins on damaged epithelium as a result of localized inflammatory responses following pathogen (pneumococcal) encounter and invasion. Refer to references [49]–[52] for more detail on probiotic–host effects. Th, T helper cell.

Mentions: The World Health Organization (WHO) defines probiotics as live micro-organisms that confer a health benefit to the host and are generally regarded as safe in humans [14]. Moreover, clinical studies have confirmed the safety and feasibility of oral administration of probiotics in infancy [15], [16]. Lactobacillus and Bifidobacterium are the two most widely studied genera of probiotic bacteria [17]. Probiotic activity is highly species- and strain-specific [18], [19]. Principal amongst their pleiotropic effects is the capacity to counteract microbiome disturbances, suggesting the potential to modulate pneumococcal colonization [20]. Indeed, experimental data suggest that probiotics can influence the profile of microbial species in the nasopharynx to reduce pneumococcal colonization [21]–[24]. Probiotics also maintain epithelial barrier integrity and modulate systemic and mucosal immune responses [14]. Furthermore, probiotic-microbiome crosstalk is important, as intestinal microbiota can shape immune responses by controlling the relative activity of regulatory T cells and Th17 cells [25], [26]. A paradigm for the effects of probiotics in modulating host responses in the nasopharynx to protect against pneumococcal infection is proposed in Figure 1. Importantly, while the mechanisms of action proposed are largely supported by animal studies, more research is needed to confirm these effects in humans.


Protecting against pneumococcal disease: critical interactions between probiotics and the airway microbiome.

Licciardi PV, Toh ZQ, Dunne E, Wong SS, Mulholland EK, Tang M, Robins-Browne RM, Satzke C - PLoS Pathog. (2012)

Paradigm for the proposed biological effects of probiotic bacteria in protection against pneumococcal infection.Commensal and/or probiotic bacteria can prevent pathogens (pneumococci) from attaching to and colonizing the respiratory epithelium by associating with specific cell surface receptors and by enhancing mucus secretion and the production of secretory IgA. Probiotic bacteria interact with underlying dendritic cells (DCs) which signal to the adaptive immune system to trigger a variety of effector cell types, including Th1, Th2, and Th17 as well as regulatory T cells and B cells depending on the local cytokine/chemokine microenvironment. Furthermore, probiotic bacteria also maintain the epithelial barrier integrity by upregulating the expression of specific tight junction proteins on damaged epithelium as a result of localized inflammatory responses following pathogen (pneumococcal) encounter and invasion. Refer to references [49]–[52] for more detail on probiotic–host effects. Th, T helper cell.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3369940&req=5

ppat-1002652-g001: Paradigm for the proposed biological effects of probiotic bacteria in protection against pneumococcal infection.Commensal and/or probiotic bacteria can prevent pathogens (pneumococci) from attaching to and colonizing the respiratory epithelium by associating with specific cell surface receptors and by enhancing mucus secretion and the production of secretory IgA. Probiotic bacteria interact with underlying dendritic cells (DCs) which signal to the adaptive immune system to trigger a variety of effector cell types, including Th1, Th2, and Th17 as well as regulatory T cells and B cells depending on the local cytokine/chemokine microenvironment. Furthermore, probiotic bacteria also maintain the epithelial barrier integrity by upregulating the expression of specific tight junction proteins on damaged epithelium as a result of localized inflammatory responses following pathogen (pneumococcal) encounter and invasion. Refer to references [49]–[52] for more detail on probiotic–host effects. Th, T helper cell.
Mentions: The World Health Organization (WHO) defines probiotics as live micro-organisms that confer a health benefit to the host and are generally regarded as safe in humans [14]. Moreover, clinical studies have confirmed the safety and feasibility of oral administration of probiotics in infancy [15], [16]. Lactobacillus and Bifidobacterium are the two most widely studied genera of probiotic bacteria [17]. Probiotic activity is highly species- and strain-specific [18], [19]. Principal amongst their pleiotropic effects is the capacity to counteract microbiome disturbances, suggesting the potential to modulate pneumococcal colonization [20]. Indeed, experimental data suggest that probiotics can influence the profile of microbial species in the nasopharynx to reduce pneumococcal colonization [21]–[24]. Probiotics also maintain epithelial barrier integrity and modulate systemic and mucosal immune responses [14]. Furthermore, probiotic-microbiome crosstalk is important, as intestinal microbiota can shape immune responses by controlling the relative activity of regulatory T cells and Th17 cells [25], [26]. A paradigm for the effects of probiotics in modulating host responses in the nasopharynx to protect against pneumococcal infection is proposed in Figure 1. Importantly, while the mechanisms of action proposed are largely supported by animal studies, more research is needed to confirm these effects in humans.

View Article: PubMed Central - PubMed

Affiliation: Pneumococcal Research, Murdoch Childrens Research Institute, Royal Children's Hospital, Melbourne, Australia. paul.licciardi@mcri.edu.au

AUTOMATICALLY GENERATED EXCERPT
Please rate it.

Streptococcus pneumoniae (the pneumococcus) is a predominant cause of pneumonia, meningitis, and bacteremia... Most deaths occur in African and Asian developing countries; however, pneumococcal disease is also a significant problem in particular populations of developed countries, such as the North American Indians, and indigenous Alaskans and Australians –... In this opinion piece, we discuss the potential complementary role of probiotics to vaccines in preventing pneumococcal disease through targeting the microbiome of the upper respiratory tract... A prerequisite for pneumococcal disease is adherence of the bacterium to host nasopharyngeal epithelium leading to colonization (carriage)... It has now been demonstrated that in early infancy, colonization with pneumococci prior to conjugate vaccination causes impaired immune responses to the carried serotype, ... Exploiting the beneficial effects of probiotics on microbial colonization and immunity represents a novel approach to prevent or reduce pneumococcal colonization and disease... The World Health Organization (WHO) defines probiotics as live micro-organisms that confer a health benefit to the host and are generally regarded as safe in humans... In otitis media-prone children given antibiotics prior to oral treatment with a powdered S. salivarius K12 formula, 33% were newly colonized with K12 while two of 19 children were shown to expand the pre-existing S. salivarius population... No impact on clinical outcomes was reported in this study, and the small sample size used makes it difficult to draw meaningful conclusions... In contrast, when otitis-prone children (n = 155) were given a daily probiotic mix containing LGG, L. rhamnosus LC705, B. breve 99, and Propionibacterium freudenreichii JS for 24 weeks, no effect on nasopharyngeal carriage of otitis pathogens was observed... Furthermore, this probiotic formula did not prevent the occurrence of otitis media in these children, although there was a trend of reduced recurrent respiratory infections... To date, the effect of probiotics on the gastrointestinal microbiome have provided the best evidence for host–microbe interactions such as pathogen exclusion, enhanced mucus secretion, production of anti-bacterial factors, and modulation of host immunity... However, no change in diphtheria toxoid or tetanus toxoid IgG levels was observed, suggesting that the effects of probiotics may vary depending on the vaccine antigen used... Recently, Lactobacillus casei was reported to significantly enhance the pneumococcal protective protein A (PppA)-specific IgG and IgA response in the serum and mucosa following nasal vaccination with PppA and was associated with a significantly reduced pathogen load in the nasal lavage by day 42 post-immunization.

Show MeSH
Related in: MedlinePlus