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Review article
An immune system fighting against pneumococcus
Un sistema inmune en guardia frente al neumococo
C. Ruiz-Ruiza,
Corresponding author
cristina.ruiz@pfizer.com

Corresponding author.
, E. Redondo Margüellob
a Equipo Médico Vacunas Pfizer, Madrid, Spain
b Vacunación y Salud Internacional, Madrid Salud, Ayuntamiento de Madrid, Madrid, Spain
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="s0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0025">Introduction</span><p id="p0005" class="elsevierStylePara elsevierViewall">Respiratory infections are a major public health challenge and&#44; despite most being immune-preventable&#44; they are among the most frequent causes of death in Spain&#46; Pneumonia in particular is the most notable respiratory disease in terms of number of deaths in Spain &#40;with the exception of deaths due to COVID-19&#41;&#44; having increased by 28&#46;6&#37; in the last year&#46;<a class="elsevierStyleCrossRef" href="#bb0005"><span class="elsevierStyleSup">1</span></a></p><p id="p0010" class="elsevierStylePara elsevierViewall">The main pathogen causing community-acquired pneumonia is <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> &#40;<span class="elsevierStyleItalic">S&#46; pneumoniae</span>&#41;&#44; also called pneumococcus&#46;<a class="elsevierStyleCrossRef" href="#bb0010"><span class="elsevierStyleSup">2</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0015"><span class="elsevierStyleSup">3</span></a> This bacterium is naturally present&#44; without causing disease&#44; in the nasopharynx of children and adults&#46;<a class="elsevierStyleCrossRef" href="#bb0020"><span class="elsevierStyleSup">4</span></a> However&#44; to understand the mechanisms that trigger non-invasive clinical forms such as pneumonia or otitis&#44; or invasive forms of pneumococcal disease &#40;bacteraemic pneumonia&#44; meningitis&#44; sepsis&#44; etc&#46;&#41;&#44; it is important to understand the pathogenesis of the bacterium and the immune response generated after infection naturally or after vaccination&#46;</p></span><span id="s0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0030">Development of the topic</span><span id="s0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0035">Pneumococcus as a coloniser</span><p id="p0015" class="elsevierStylePara elsevierViewall">Nasopharyngeal colonisation is the main means of pneumococcal transmission&#44; and its gateway to invasive infection&#46; During the colonisation process&#44; pneumococcus must contend with the host&#39;s defences &#40;physical and immunological&#41; and compete with other colonising organisms&#46;<a class="elsevierStyleCrossRef" href="#bb0025"><span class="elsevierStyleSup">5</span></a> As part of the physical barriers&#44; the first line of defence encountered by pneumococcus is the interaction with mucus&#44; which contains antimicrobial peptides and immunoglobulins&#46; Pneumococcus manages to overcome this barrier&#44; thanks to its capsular polysaccharide which&#44; being negatively charged&#44; repels the mucopolysaccharides present in the mucus&#46; In addition&#44; using a combination of virulence factors such as metalloproteinase enzymes&#44; it is able to eliminate the IgA immunoglobulins present in the mucus and prevent activation of the complement system&#46;<a class="elsevierStyleCrossRef" href="#bb0025"><span class="elsevierStyleSup">5</span></a></p><p id="p0020" class="elsevierStylePara elsevierViewall">Thus&#44; <span class="elsevierStyleItalic">S&#46; pneumoniae</span> can gain access to the second physical barrier&#59; the epithelial cells of the mucosa where it establishes itself as a coloniser&#46; Pneumococcus binds to mucosal cells with various mucosal surface components&#44; the expression of which increases in response to proinflammatory stimuli from the host&#46;<a class="elsevierStyleCrossRef" href="#bb0030"><span class="elsevierStyleSup">6</span></a> This bacterium can also alter its phenotype through a process called phase shift&#44; in which it changes from an &#8216;opaque&#8217; phenotype with high expression of capsular polysaccharide to a &#8216;transparent&#8217; phenotype&#44; with reduced expression of the capsule&#44; which facilitates colonisation of the nasopharynx&#46;<a class="elsevierStyleCrossRefs" href="#bb0030"><span class="elsevierStyleSup">6&#8211;8</span></a> However&#44; the presence of previous viral infections favours a proinflammatory environment in the nasopharynx and thus facilitates colonisation by pneumococcus&#46; In this regard&#44; several studies have shown that the interaction of pneumococcus in the nasopharynx with different viruses favours both viral infection and pneumococcal colonisation and invasive infection&#46;<a class="elsevierStyleCrossRefs" href="#bb0045"><span class="elsevierStyleSup">9&#8211;14</span></a> Dagan et al&#46; recently observed a relationship between respiratory syncytial virus infection and subsequent pneumococcal disease&#44;<a class="elsevierStyleCrossRef" href="#bb0045"><span class="elsevierStyleSup">9</span></a> a relationship also observed previously in the case of influenza&#46;<a class="elsevierStyleCrossRef" href="#bb0060"><span class="elsevierStyleSup">12</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0065"><span class="elsevierStyleSup">13</span></a> Conversely&#44; pneumococcal infection has also been associated with a decreased immune response to different viruses&#44; such as SARS-CoV-2<a class="elsevierStyleCrossRef" href="#bb0050"><span class="elsevierStyleSup">10</span></a> or the influenza virus&#46;<a class="elsevierStyleCrossRef" href="#bb0055"><span class="elsevierStyleSup">11</span></a> Thus&#44; virus-bacteria co-infection could explain the spike in cases of invasive pneumococcal disease observed in Spain after the COVID-19 pandemic&#44; coinciding with the increased circulation of respiratory viruses&#46;<a class="elsevierStyleCrossRefs" href="#bb0075"><span class="elsevierStyleSup">15&#8211;17</span></a></p><p id="p0025" class="elsevierStylePara elsevierViewall">The host immune system is activated to prevent colonisation by recruiting numerous components of the innate and adaptive immune system&#46; In particular&#44; Th17 lymphocytes appear to be particularly involved in the control of <span class="elsevierStyleItalic">S&#46; pneumoniae</span> colonisation&#44; as they mediate the recruitment of neutrophils&#44; an important defence mechanism against extracellular bacteria&#44; stimulating the phagocytic capacity of macrophages and the production of antimicrobial substances&#46;<a class="elsevierStyleCrossRefs" href="#bb0090"><span class="elsevierStyleSup">18&#8211;20</span></a></p><p id="p0030" class="elsevierStylePara elsevierViewall">The introduction of pneumococcal conjugate vaccines &#40;PCVs&#41; in the childhood immunisation schedule has been associated with a significant decrease in pneumococcal disease in all age groups in the Spanish population&#44; showing herd protection&#46;<a class="elsevierStyleCrossRef" href="#bb0105"><span class="elsevierStyleSup">21</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0110"><span class="elsevierStyleSup">22</span></a> This protection is largely due to the effect of PCV on nasopharyngeal colonisation&#44; which decreases transmission of the bacteria&#46; These vaccines stimulate the production of memory B cells&#44; which after differentiation into plasma cells produce IgG immunoglobulins in the mucosa that favour opsonophagocytosis of the bacteria&#59; both elements are related to protection against colonisation&#46;<a class="elsevierStyleCrossRef" href="#bb0115"><span class="elsevierStyleSup">23</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0120"><span class="elsevierStyleSup">24</span></a> IgA levels after PCV vaccination have not shown a clear correlation with the decrease in nasopharyngeal colonisation&#44; probably due to the enzymatic degradation of this immunoglobulin by pneumococcus&#44; as mentioned above&#46;<a class="elsevierStyleCrossRef" href="#bb0030"><span class="elsevierStyleSup">6</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0120"><span class="elsevierStyleSup">24</span></a></p></span><span id="s0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0040">Pneumococcus as a pathogen</span><p id="p0035" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Streptococcus pneumoniae</span> is a natural coloniser of the human nasopharynx&#46; However&#44; different factors may favour its localised penetration into different host organs to cause non-invasive disease such as otitis or pneumonia&#44; as well as progression to invasive disease such as bacteraemic pneumonia&#44; meningitis&#44; or sepsis&#46; The proinflammatory environment and damage to the respiratory epithelium caused by previous viral infections that increase colonisation density are some of the factors favouring pneumococcal invasiveness&#46;<a class="elsevierStyleCrossRef" href="#bb0025"><span class="elsevierStyleSup">5</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0030"><span class="elsevierStyleSup">6</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0070"><span class="elsevierStyleSup">14</span></a> In addition&#44; the capsular polysaccharide surrounding the bacterium plays a key role in its ability to cause disease&#46; It has been shown that pneumococcus is able to increase the expression levels of its polysaccharide capsule to generate a more virulent phenotype &#40;&#8216;opaque&#8217; phenotype&#41;&#44; in which it hides the bacterial surface from immune system components such as antibodies or the complement system&#44; making opsonophagocytosis by phagocytes more difficult&#46;<a class="elsevierStyleCrossRef" href="#bb0025"><span class="elsevierStyleSup">5</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0030"><span class="elsevierStyleSup">6</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0125"><span class="elsevierStyleSup">25</span></a></p><p id="p0040" class="elsevierStylePara elsevierViewall">The defence mechanisms of the immune system vary according to the site of disease caused by pneumococcus&#44; and involve numerous components of the innate and adaptive immune system&#46;<a class="elsevierStyleCrossRef" href="#bb0025"><span class="elsevierStyleSup">5</span></a> In the case of invasive disease&#44; immunoglobulins or antibodies to bacterial membrane proteins and to capsular polysaccharide are particularly important due to the rapid progression of these forms of disease following infection&#46;<a class="elsevierStyleCrossRef" href="#bb0130"><span class="elsevierStyleSup">26</span></a> The mechanisms involved in bacterial clearance are numerous and include bacterial neutralisation&#44; stimulation of opsonophagocytosis of the pneumococcus by phagocytes&#44; as well as bacterial clearance by natural killer cells and activation of the complement system&#46;<a class="elsevierStyleCrossRef" href="#bb0100"><span class="elsevierStyleSup">20</span></a> In the case of non-invasive diseases&#44; such as otitis or pneumonia&#44; which occur in mixed areas with a mucosal and systemic component&#44; both antibodies and Th17 lymphocytes have been shown to play an important role in their prevention&#44; similar to their role in the nasopharynx in preventing colonisation&#46;<a class="elsevierStyleCrossRef" href="#bb0090"><span class="elsevierStyleSup">18</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0095"><span class="elsevierStyleSup">19</span></a></p><p id="p0045" class="elsevierStylePara elsevierViewall">The implementation of childhood pneumococcal conjugate vaccination programmes has had a major impact on both invasive and non-invasive forms of the disease&#46;<a class="elsevierStyleCrossRef" href="#bb0135"><span class="elsevierStyleSup">27</span></a> This is due to the immune response that PCVs trigger in vaccinated individuals&#59; these vaccines stimulate both humoral and cellular immune responses&#46;<a class="elsevierStyleCrossRef" href="#bb0140"><span class="elsevierStyleSup">28</span></a> In terms of the humoral response&#44; conjugate vaccines generate IgG antibodies to a greater extent&#44; which are particularly relevant for the prevention of pneumococcal disease&#46;<a class="elsevierStyleCrossRef" href="#bb0090"><span class="elsevierStyleSup">18</span></a> However&#44; when assessing the immunogenicity of PCVs&#44; the quantitative measurement of IgG production by ELISA &#40;enzyme-linked immunosorbent assay&#41; is not the only parameter to be taken into account&#44; but also the capacity of the antibodies produced to neutralise pneumococcus&#44; activate the complement system&#44; and stimulate opsonophagocytosis by phagocytes&#46;<a class="elsevierStyleCrossRef" href="#bb0130"><span class="elsevierStyleSup">26</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0145"><span class="elsevierStyleSup">29</span></a> In this regard&#44; several studies indicate that there is no direct correlation between IgG titres and prevention of pneumococcal disease&#46;<a class="elsevierStyleCrossRefs" href="#bb0145"><span class="elsevierStyleSup">29&#8211;31</span></a> However&#44; prevention does seem to be related to the production of opsonophagocytic antibodies&#46; These are measured by the opsonophagocytic assay technique&#44; which assesses antibody functionality in vitro by mimicking the mechanism of complement activation and opsonophagocytosis by phagocytes that occurs in vivo&#46;<a class="elsevierStyleCrossRef" href="#bb0145"><span class="elsevierStyleSup">29</span></a> An example of this correlation was seen during the approval of PCV13&#59; this vaccine had a lower IgG antibody response measured by ELISA than PCV7 for serotypes 6B and 9V&#44; but had a similar opsonophagocytic antibody response&#46; Despite having a lower IgG response&#44; PCV13 retained effectiveness against 6B and 9V&#44; demonstrating a stronger association with opsonophagocytic antibodies&#46;<a class="elsevierStyleCrossRef" href="#bb0145"><span class="elsevierStyleSup">29</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRefs" href="#bb0160"><span class="elsevierStyleSup">32&#8211;34</span></a></p><p id="p0050" class="elsevierStylePara elsevierViewall">Regarding the cellular response&#44; it has been observed that after vaccination with PCV&#44; effector T and B cells are activated&#44; as well as memory cells that will allow protection to be maintained over time&#46;<a class="elsevierStyleCrossRef" href="#bb0140"><span class="elsevierStyleSup">28</span></a> Although the quantification and characterisation of memory B and T cells is not an easily standardised technique and therefore not routinely studied at present for the approval of new PCVs&#44; there are indirect measurements of the memory response generated by these vaccines&#46; Some studies&#44; and even the World Health Organisation&#44; suggest that a possible indicator of the presence of a memory immune response is the observation of an increase in IgG and&#47;or opsonophagocytic antibody titres between the primary vaccination and the booster dose &#40;known as the booster effect&#41;&#44;<a class="elsevierStyleCrossRef" href="#bb0175"><span class="elsevierStyleSup">35</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0180"><span class="elsevierStyleSup">36</span></a> which indirectly points to more extended protection over time and a decrease in nasopharyngeal colonisation&#46;<a class="elsevierStyleCrossRef" href="#bb0115"><span class="elsevierStyleSup">23</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bb0120"><span class="elsevierStyleSup">24</span></a></p></span></span><span id="s0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0045">Conclusion</span><p id="p0055" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Streptococcus pneumoniae</span> is a bacterium that causes complex disease in humans&#46; In response&#44; our immune system defends itself with a variety of elements&#44; the relevance of which varies depending on the site of bacterial infection in the body&#46; Pneumococcal conjugate vaccines&#44; developed more than 2 decades ago to prevent pneumococcal disease caused by prevalent and epidemiologically relevant serotypes&#44; have had a major impact in reducing the disease due to the complex immune response they trigger&#46; Although various components of the immune system such as IgG production or opsonophagocytic antibody production are evaluated in the approval of new pneumococcal conjugate vaccines&#44; only IgG production is considered in the primary targets of paediatric vaccine approval trials&#44; which simplifies and possibly underestimates the extent of the complex immune response generated by these vaccines&#46; Evaluation of other components such as opsonophagocytic antibodies &#40;used for licencing of adult vaccines&#41;&#44; related to the functional antibody response&#44; or the booster effect&#44; an indirect measure of the memory response&#44; could give a more complete picture of the extent of immunity and protection generated by these vaccines&#46;</p></span><span id="s0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="st0050">Funding</span><p id="p0060" class="elsevierStylePara elsevierViewall">The authors declare that they received no funding for this article&#46;</p></span></span>"
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        "resumen" => "<span id="as0005" class="elsevierStyleSection elsevierViewall"><p id="sp0005" class="elsevierStyleSimplePara elsevierViewall">Pneumococcus is a common coloniser of the human nasopharynx&#46; However&#44; it can also cause human diseases such as otitis or pneumonia&#44; which may progress into invasive forms such as bacteremic pneumonia&#44; meningitis&#44; or sepsis&#46; This bacterium reaches and establishes itself in the nasopharynx through different mechanisms&#44; which include evasion of the host immune system&#46; Moreover&#44; certain factors such as the coinfection with viruses favour colonisation&#44; as well as the ability of pneumococcus to cause diseases&#46; Our immune system responds to pneumococcal colonisation and infection through the innate and adaptive responses&#44; which can be stimulated by pneumococcal vaccines&#46; In the following article&#44; we will briefly review the mechanisms of pneumococcal infection and how our immune system responds to it&#59; as well as the immune response generated after vaccination and its impact on the prevention of pneumococcal disease&#46;</p></span>"
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        "resumen" => "<span id="as0010" class="elsevierStyleSection elsevierViewall"><p id="sp0010" class="elsevierStyleSimplePara elsevierViewall">El neumococo es un com&#250;n colonizador de la nasofaringe humana&#46; Sin embargo&#44; en ocasiones puede causar enfermedades no invasivas como otitis o neumon&#237;as&#44; que pueden progresar a formas invasivas de la enfermedad como neumon&#237;as bacteri&#233;micas&#44; meningitis o sepsis&#46; Esta bacteria es capaz de establecerse en la nasofaringe mediante diversos mecanismos&#44; que incluyen la evasi&#243;n del sistema inmune del hu&#233;sped&#46; Adem&#225;s&#44; ciertos factores como la coinfecci&#243;n con virus favorecen la colonizaci&#243;n&#44; as&#237; como la capacidad del neumococo para causar enfermedades&#46; Por otro lado&#44; nuestro sistema inmune responde a la colonizaci&#243;n y a la infecci&#243;n por neumococo por medio de las respuestas innata y adaptativa&#44; las cuales pueden ser estimuladas mediante vacunas antineumoc&#243;cicas&#46; En este art&#237;culo se revisan brevemente los mecanismos de infecci&#243;n del neumococo y la manera en la que nuestro sistema inmune se defiende de &#233;ste&#44; as&#237; como la respuesta que se produce tras la vacunaci&#243;n y su impacto en la prevenci&#243;n de la enfermedad neumoc&#243;cica&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="np4005">Please cite this article as&#58; Ruiz-Ruiz C&#44; Redondo Marg&#252;ello E&#46; An immune system fighting against pneumococcus&#46; Vacunas&#46; 2024&#46; <span class="elsevierStyleInterRef" id="ir3005" href="https://doi.org/10.1016/j.vacun.2024.06.003">https&#58;&#47;&#47;doi&#46;org&#47;10&#46;1016&#47;j&#46;vacun&#46;2024&#46;06&#46;003</span>&#46;</p>"
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ISSN: 24451460
Original language: English
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