Indirect impact of PCV10 children vaccination on the serotype distribution and antimicrobial resistance of <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> causing invasive disease in adults over 50 in Colombia, 2005–2019: Observational analysis | Enfermedades Infecciosas y Microbiología Clínica (English Edition)

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          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Percentages of <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> isolates by VT10&#44; AddVT23&#44; NVT&#44; VT&#44; and the pre-PCV10 &#40;2005&#8211;2009&#41;&#44; transition &#40;2010&#8211;2014&#41; and post-PCV10 &#40;2015&#8211;2019&#41; periods&#46; VT10&#58; serotypes included in PCV10 &#40;1&#44; 4&#44; 5&#44; 6B&#44; 7F&#44; 9V&#44; 14&#44; 18C&#44; 19F&#44; 23F&#41;&#44; AddVT23&#58; the 13 additional PPV23 &#40;2&#44; 3&#44; 8&#44; 9N&#44; 10A&#44; 11A&#44; 12F&#44; 5B&#44; 17F&#44; 19A&#44; 20&#44; 22F&#44; 33F&#41;&#44; NVT&#58; non-vaccine type&#44; NT&#58; non-typable&#44; NA&#58; not apply&#46; Black line represents the number of <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> isolates recovered per year of surveillance&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">The introduction of pneumococcal conjugate vaccines &#40;PCV&#41; has changed the epidemiology of invasive pneumococcal disease &#40;IPD&#41; and has significantly reduced the number of cases caused by the serotypes that are included in the vaccine serotypes &#40;VT&#41; both in children by direct impact and in adults due to indirect protection&#46; However&#44; an increase in IPD caused by <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> non-vaccine serotypes &#40;NVT&#41; has been reported&#46;<a class="elsevierStyleCrossRefs" href="#bib0155"><span class="elsevierStyleSup">1&#8211;3</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">The pneumococcal 7-valent conjugate vaccine &#40;PCV7&#41; was introduced in Bogot&#225; &#40;Colombia&#41; in 2009 and since January 2012&#44; it was replaced by the pneumococcal 10-valent conjugate vaccine &#40;PCV10&#41; which was introduced universally in Colombia to populations born on or after November 1&#44; 2011&#44; in a 2<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>1 schedule at 2&#44; 4&#44; and 12 months of age&#46; This vaccine is currently administered with a 94&#46;5&#37; coverage rate&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">4</span></a> Since 2008&#44; the pneumococcal polysaccharide vaccine &#40;PPV23&#41; has been recommended in Colombia for disease prevention in adults older than 60 years&#46; However&#44; only partial data are known on the impact of this vaccine on IPD in adults in the city of Bogot&#225;&#46;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">5</span></a> The aim of this study was to estimate the changes in serotype distribution and antimicrobial susceptibility of <span class="elsevierStyleItalic">S&#46; pneumoniae</span> isolates recovered from adult IPD and to evaluate the indirect effect of immunization with PCV10 based on laboratory records by analyzing the period from 2005 to 2019 including six years before and eight years after the universal PCV10 administration to Colombian children&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Pneumococcal isolates</span><p id="par0015" class="elsevierStylePara elsevierViewall">A total of 2204 <span class="elsevierStyleItalic">S&#46; pneumoniae</span> isolates from normally sterile body sites of adults &#40;&#8805;50 years old&#41; with IPD from 2005 to 2019 were recovered from hospital laboratories and confirmed by the National Reference Laboratory &#40;NRL&#41; in Colombia&#44; as part of the passive laboratory-based surveillance SIREVA II<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">6</span></a> network that was established in 1993 in the Latin American and Caribbean countries&#44; which was encouraged by the Pan American Health Organization &#40;PAHO&#41;&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Microbiological confirmation&#44; serotyping and antibiotic susceptibility testing</span><p id="par0020" class="elsevierStylePara elsevierViewall">The serotypes were determined by the Quellung reaction &#40;Statens Serum Institut-Copenhagen&#44; Denmark&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">7</span></a> Antimicrobial susceptibility tests were performed by the broth microdilution method to penicillin &#40;PEN&#41;&#44; ceftriaxone &#40;CRO&#41;&#44; trimethoprim&#8211;sulfamethoxazole &#40;SXT&#41;&#44; chloramphenicol &#40;CHL&#41;&#44; tetracycline &#40;TET&#41;&#44; erythromycin &#40;ERY&#41;&#44; and vancomycin &#40;VAN&#41;&#46; The results were interpreted using CLSI guidelines&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">8</span></a> Multi-drug resistance &#40;MDR&#41; was defined as resistance to three or more antibiotic families&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Statistical analysis</span><p id="par0025" class="elsevierStylePara elsevierViewall">The serotypes were also categorized in accordance with those included in PCV10&#58; VT10 &#40;1&#44; 4&#44; 5&#44; 6B&#44; 7F&#44; 9V&#44; 14&#44; 18C&#44; 19F&#44; and 23F&#41;&#59; thirteen additional included in PPV23&#58; AddVT23 &#40;2&#44; 3&#44; 8&#44; 9N&#44; 10A&#44; 11A&#44; 12F&#44; 5B&#44; 17F&#44; 19A&#44; 20&#44; 22F&#44; 33F&#41;&#44; NVT &#40;non-PCV10 and non-PP23&#41;&#44; and non-typable isolates &#40;NT&#41;&#59; AddVT23&#44; serotypes 3 and 19A were analyzed separately&#46; The annual reported rates &#40;ARRs&#41; were expressed as the number of isolates serotyped per 100&#44;000 population using population denominator projections from the National Statistics Institute &#40;DANE acronym in Spanish&#41; for those years included in the analysis as proxy of IPD occurrence&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">9</span></a> The World Health Organization &#40;WHO&#41; 2000 standard population was used as the reference population for age and sex standardization&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">10</span></a> The annual average ARRs were estimated to compare the two epidemiological periods&#44; pre- and post-PCV10&#46; Data statistical analyses and visualization were carried out in R software&#44; version 4&#46;0&#46;2 &#40;R Foundation Statistical Computing&#44; Austria&#46; URL&#58; <a href="https://www.r-project.org/">https&#58;&#47;&#47;www&#46;R-project&#46;org&#47;</a>&#41;&#46; The annual serotype percentages were compared using the <span class="elsevierStyleItalic">&#967;</span><span class="elsevierStyleSup">2</span> test for percentage trends with a 95&#37; CI or Fisher&#39;s exact test when small samples &#40;category of analysis with <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>5&#41; were excluded using the <span class="elsevierStyleItalic">&#967;</span><span class="elsevierStyleSup">2</span> test&#46; The serotype temporal trend <span class="elsevierStyleItalic">p</span> values were interpreted as trend variations of the percentages and absolute numbers during the 2005&#8211;2019 study period&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">11</span></a></p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Percentage changes in the proportions and variations of population rates</span><p id="par0030" class="elsevierStylePara elsevierViewall">Two impact analyses were performed&#46; First&#44; the percentage of change was determined using the proportion &#40;prevalence&#41; of each individual serotype or groups divided by the annual total isolates in a national aggregation&#44; a trend analysis &#40;<span class="elsevierStyleItalic">p</span>-value of trend&#41; was performed to identify whether the proportion variations in the observed period were statistically significant&#46; Second&#44; the variations in the ARRs of IPD were estimated with confidence intervals&#46; For both analyses&#44; a confidence level of 95&#37; &#40;alpha<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; was defined for the interpretations&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">12</span></a></p></span></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Results</span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Pneumococcal isolate distributions and annual reported rates &#40;ARRs&#41;</span><p id="par0035" class="elsevierStylePara elsevierViewall">The analysis was performed with 2155 isolates from 16&#47;32 departments &#40;50&#37;&#41;&#44; 49 isolates from 9 departments were excluded because there were fewer than 10 isolates over the period of the study &#40;2005&#8211;2019&#41;&#46; The distributions by department&#44; period and year of surveillance are shown in <a class="elsevierStyleCrossRef" href="#sec0080">Tables 1S and 2S</a>&#46; The data show an increase in the surveillance in recent years&#44; with an increase from 314 isolates from 2005 to 2009 &#40;pre-PCV10&#41; to 1190 from 2015 to 2019 &#40;post-PCV10&#41;&#46; <a class="elsevierStyleCrossRef" href="#sec0080">Fig&#46; 1S</a> shows the departments where <span class="elsevierStyleItalic">S&#46; pneumoniae</span> isolates were recovered&#44; the most populated regions of the country&#44; being Bogot&#225;&#44; Antioquia and Valle also the greatest contributors&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">The number of isolates and the ARRs per 100&#44;000 adults &#8805;50 years by department showed increases when comparing the pre-PCV10 and post-PCV10 periods&#58; mainly in Bogot&#225; with 136 &#40;43&#46;3&#37;&#41; isolates to 358 &#40;30&#46;1&#37;&#41; and ARRs from 1636 to 4540 isolates per 100&#44;000&#59; Antioquia with 89 &#40;28&#46;3&#37;&#41; to 329 &#40;27&#46;6&#37;&#41; isolates and ARRs from 1625 to 4227 isolates&#59; and Valle with 46 &#40;14&#46;6&#37;&#41; to 222 &#40;18&#46;7&#37;&#41; and ARRs from 2077 to 5848 isolates &#40;<a class="elsevierStyleCrossRef" href="#sec0080">Tables 1S&#8211;3S</a> and <a class="elsevierStyleCrossRef" href="#sec0080">Fig&#46; 2S</a>&#41;&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Among 2155 isolates&#44; 1165 &#40;54&#46;1&#37;&#41; were from male patients&#44; 946 &#40;43&#46;9&#37;&#41; were from patients &#8805;70 years old&#44; and 420 &#40;19&#46;5&#37;&#41; were from patients &#8805;80 years old&#46; <a class="elsevierStyleCrossRef" href="#sec0080">Table 4S</a> shows the distribution of isolates by age group and period&#46; The isolates were recovered from 1810 blood samples &#40;84&#46;0&#37;&#41;&#44; 269 cerebrospinal fluid samples &#40;12&#46;5&#37;&#41;&#44; 53 pleural fluid samples &#40;2&#46;5&#37;&#41;&#44; and 23 from other samples &#40;1&#46;1&#37;&#41;&#46; Sepsis was the most frequent clinical diagnosis for 1204 &#40;55&#46;9&#37;&#41; of the isolates and was followed by pneumonia 603 &#40;28&#46;0&#37;&#41;&#44; meningitis 323 &#40;15&#46;0&#37;&#41;&#44; and other IPDs 25 &#40;1&#46;2&#37;&#41; &#40;<a class="elsevierStyleCrossRef" href="#sec0080">Tables 5S and 6S</a>&#41;&#46; The pneumococcal vaccination status in adults was unknown&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Serotype distribution</span><p id="par0050" class="elsevierStylePara elsevierViewall">A total of sixty-three serotypes were identified&#46; The proportion of VT10 isolates was 26&#46;3&#37; &#40;568&#41;&#59; the proportion of AddVT23 was 40&#46;3&#37; &#40;868&#41;&#44; which consisted mainly of serotypes 3 &#40;286&#59; 13&#46;3&#37;&#41; and 19A &#40;217&#59; 10&#46;1&#37;&#41;&#59; the proportion of NVT with 41 different serotypes corresponded to 33&#46;1&#37; &#40;713&#41; of total isolates&#59; while only 0&#46;3&#37; &#40;6 isolates&#41; were NT&#46; Serotype 2 included in VT23 was not recovered&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">The differences in the serotype proportions in the three periods are shown in <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#44; and in <a class="elsevierStyleCrossRef" href="#sec0080">Table 7S</a>&#46; We observed that the trend for VT10 isolates significantly decreased from 50&#37; in 2005&#8211;2009 &#40;pre-PCV10&#41; &#40;p&#60;0&#46;0001&#41; to 16&#37; in 2015&#8211;2019 &#40;post-PCV10&#41; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;0001&#41;&#44; especially for serotypes 1 &#40;9&#46;9&#8211;0&#46;8&#37;&#41;&#44; 14 &#40;10&#46;5&#8211;2&#46;6&#37;&#41;&#44; 6B &#40;4&#46;5&#8211;0&#46;7&#37;&#41;&#44; and 23F &#40;5&#46;7&#8211;1&#46;3&#37;&#41;&#46; The increasing trend of AddVT23 was not statistically significant &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;71&#41;&#44; but serotype 19A increased significantly from 1&#46;6&#37; in the pre-PCV10 period to 14&#46;8&#37; in the post-PCV10 period &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;0001&#41;&#46; The NVT trend &#40;from 21&#46;4&#37; to 38&#46;4&#37;&#41; was mainly due to serotypes 6C &#40;1&#46;3&#8211;6&#46;3&#37;&#41;&#44; 15A &#40;2&#46;2&#8211;4&#46;2&#37;&#41;&#44; 23A &#40;1&#8211;5&#37;&#41;&#44; 23B &#40;0&#46;6&#8211;3&#37;&#41;&#44; and 35B &#40;0&#46;6&#8211;2&#46;6&#37;&#41;&#44; which represented 54&#46;3&#37; of all isolates &#40;248&#47;457&#41; in the post-PCV10 period&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Percentage of change in the proportions and variations of population rates</span><p id="par0060" class="elsevierStylePara elsevierViewall">Changes in percentages between the pre- and post-PCV10 periods were &#8722;68&#46;1&#37; for VT10 and &#43;60&#46;4&#37; for AddVT23&#46; We highlight the changes in percentages of serotypes 14 &#40;&#8722;75&#46;2&#37;&#41;&#44; 19A &#40;&#43;828&#46;8&#37;&#41;&#44; 3 &#40;&#43;37&#46;5&#37;&#41; and NVT &#40;&#43;77&#46;3&#37;&#41;&#46; Due to the low number of isolates&#44; the percentage changes were only calculated for the categories mentioned in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46; The ARR variations were significant for serotypes 3 &#40;276&#46;6&#44; 95&#37; CI&#58; 66&#46;9&#8211;749&#46;7&#41;&#59; 19A &#40;2496&#44; 95&#37; CI&#58; 238&#46;7&#8211;19804&#46;7&#41; and NVT &#40;376&#46;7&#44; 95&#37; CI&#58; 172&#46;3&#8211;734&#46;3&#41; and for the total of isolates received during the surveillance period &#40;170&#46;1&#44; 95&#37; CI&#58; 105&#46;3&#8211;255&#46;3&#41;&#46; The average adjusted ARRs of the <span class="elsevierStyleItalic">S&#46; pneumoniae</span> serotypes are shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#46; Eighty-five percent &#40;1832&#47;2155&#41; of the isolates were recovered from patients with a clinical diagnosis of non-meningitis&#44; and the most frequent serotypes were 3&#44; 19A&#44; 14 and 6C&#46; For meningitis the most frequent serotypes were 19A&#44; 19F and 3&#46; <a class="elsevierStyleCrossRef" href="#sec0080">Table 8S</a> shows the serotype distributions by diagnosis and type of vaccine&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Antimicrobial resistance</span><p id="par0065" class="elsevierStylePara elsevierViewall">Interestingly&#44; a total of 1216&#47;2155 &#40;56&#46;4&#37;&#41; isolates were susceptible to all antibiotics&#46; The proportions of VT10 susceptible isolates were 44&#46;6&#37; &#40;41&#47;92&#41; and 47&#46;1&#37; &#40;224&#47;476&#41; in meningitis and non-meningitis&#44; respectively&#46; All isolates were susceptible to vancomycin&#46; In general&#44; the isolates showed resistance to cotrimoxazole &#40;SXT&#41; &#40;27&#46;2&#37;&#41;&#44; tetracycline &#40;TET&#41; &#40;24&#46;3&#37;&#41;&#44; erythromycin &#40;ERY&#41; &#40;19&#46;4&#37;&#41; and chloramphenicol &#40;CHL&#41; &#40;2&#46;5&#37;&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#46; The number of isolates that were non-susceptible to penicillin &#40;PEN&#41; plus ERY were 20&#46;7&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>323&#41; for meningitis and 6&#46;6&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1832&#41; for non-meningitis&#46; The main serotypes resistant for meningitis were 19A &#40;82&#46;1&#37;&#59; 23&#47;28&#41;&#44; 6C &#40;66&#46;7&#37;&#59; 6&#47;15&#41;&#44; and 23A &#40;38&#46;9&#37;&#59; 7&#47;18&#41; and for non-meningitis were 19A &#40;56&#46;1&#37;&#59; 106&#47;189&#41; and 19F &#40;12&#46;2&#37;&#59; 5&#47;41&#41; &#40;<a class="elsevierStyleCrossRef" href="#sec0080">Table 9S</a>&#41;&#46; The overall MDR rate for meningitis was 18&#46;6&#37; &#40;60&#47;323&#41; and for non-meningitis 6&#46;7&#37; &#40;122&#47;1832&#41;&#46; The most common serotype with MDR and resistance patterns to PEN&#44; SXT&#44; ERY&#44; and TET in meningitis and non-meningitis was 19A &#40;<a class="elsevierStyleCrossRef" href="#sec0080">Table 10S</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0015"></elsevierMultimedia></span></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Discussion</span><p id="par0070" class="elsevierStylePara elsevierViewall">This study describes the indirect impact of the vaccination with PCV10 in children on Colombian adult IPD by measuring the changes in <span class="elsevierStyleItalic">S&#46; pneumoniae</span> VT10 distributions and antimicrobial susceptibility of isolates recovered between the pre- and post-PCV10 periods&#46; It is important to mention that SIREVA II<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">6</span></a> surveillance was extended to adults and improved over the last years mainly due to the introduction of PCV10 in children&#46; The strengthening of surveillance in adults may be interpreted as a bias&#44; as it is an unexpected result&#44; and the awareness and understanding of the importance of pneumococcal surveillance may have increased among the reporting institutions&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">We presented evidence of a herd effect due to PCV10 introduction in children over the non-targeted age groups&#44; particularly for older adults&#44; which was evaluated through aetiological confirmation and identification of <span class="elsevierStyleItalic">S&#46; pneumoniae</span> serotypes&#46; The percentage change between the pre- and post-PCV10 periods in the elderly &#40;&#8805;50 years old&#41; for VT10 was &#8722;68&#46;1&#37;&#44; and we highlight the percentage change of serotype 14 &#40;&#8722;75&#46;2&#37;&#41; however&#44; the improvements in the surveillance system potentially include information bias in the analysis of annual population rate comparisons&#46; Similar studies using methods that were included in this analysis to approximate the herd effect are also available&#58; &#40;1&#41; the variations in VT proportions &#40;prevalence&#41; and &#40;2&#41; comparisons of population rate before and after the introduction of PCV&#46; These studies also reported limitations suggesting the herd effect and changes in the surveillance system&#46; Many studies have also evaluated the impact of pneumococcal 13-valent conjugate vaccine &#40;PCV13&#41; implementation&#59; for example&#44; in Ireland&#44; an analysis of incidence rate ratios in populations over 65 years old that was based on mandatory notification systems also showed a change in the distribution of VT serotypes but indicated no changes in population rates&#46;<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">13</span></a> In Germany&#44; after PCV13 introduction&#44; a study using similar methods to ours &#40;proportions by serotypes and population rates&#41; reported that the herd effect on IPD in adults had reached its limit&#44; with VT serotypes 4&#44; 19F&#44; and 19A persisting after the initial reductions and serotype 3 not showing any herd protection effect at all&#46; This study also reported changes in the surveillance system with potential reporting bias&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">14</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">In Iceland for PCV10<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">15</span></a> and France for PCV13&#44;<a class="elsevierStyleCrossRefs" href="#bib0165"><span class="elsevierStyleSup">3&#44;16</span></a> there were herd effects&#44; since the number of IPDs in adults was reduced by half&#46; In addition&#44; the USA and England and Wales showed that the IPD incidences among adults declined after PCV13 introduction in children&#46;<a class="elsevierStyleCrossRefs" href="#bib0235"><span class="elsevierStyleSup">17&#44;18</span></a> For Japan&#44; which was the only prospective study&#44; the proportions of vaccine-covered serotypes causing pneumococcal pneumonia in adults significantly decreased following PCV13 introduction&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">19</span></a> A multicentre European study that estimated the indirect effects of the childhood PCV10&#47;13 vaccine programme in adults aged<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>65 years determined that IPD caused by VT7 &#40;serotypes included in PCV7&#41; and VT10 declined by more than 70&#37; after five years compared with the pre-vaccine period&#46;<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">20</span></a></p><p id="par0085" class="elsevierStylePara elsevierViewall">Analysis of population data &#40;ARRs&#41; did not demonstrate a statistically significant impact on VT10 incidence &#40;variation in ARR &#8722;12&#46;6&#37;&#44; IC95&#37; &#8722;45&#46;1 to 39&#46;1&#37;&#41;&#44; which was likely due to the improvement in the surveillance system &#40;a significant increase in the overall pneumococcal ARR variations&#58; 170&#46;1&#37;&#44; IC95&#37; 105&#46;3&#8211;255&#46;3&#37;&#41;&#46; As a consequence of this information bias&#44; an increase in ARRs was found for an additional 12 serotypes that were included in PPV23 &#40;168&#46;7&#37;&#44; IC95&#37; 35&#46;6&#8211;432&#46;5&#37;&#41; and NVT &#40;376&#46;7&#37;&#44; IC95&#37; 172&#46;3&#8211;734&#46;3&#37;&#41;&#59; although this was confirmed by the proportion analysis&#44; it could be overestimated&#46; However&#44; when we considered the variations in the distribution of IPD-causing serotypes&#44; a statistically significant decreasing trend was present for VT10&#44; and an increasing trend was detected for AddVT23 and NVT&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">In this study&#44; the most important reduction was observed for serotype 14&#46; In Colombia&#44; between 1994 and 2004&#44; it was the predominant serotype causing IPD&#44; with 29&#46;7&#37; of cases occurring among children<span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>6 years old and 13&#46;6&#37; in adults<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>50 years old and was associated with a wide distribution of penicillin-resistant Spain9V-ST156 clone&#46;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">21</span></a> In Bogot&#225;&#44; after PCV7 introduction&#44; a reduction in this serotype from 48&#37; &#40;2005&#8211;2009&#41; to 16&#46;7&#37; &#40;2010&#8211;2011&#41; was observed in children &#8804;2 years&#46;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">5</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">A Latin American study that was conducted in four countries that used PCV10&#44; including Colombia&#44; estimated the direct impact of PCV in children&#44; and showed an increase in serotypes 3&#44; 19A&#44; and NTV and a decrease in VT10<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">1</span></a>&#59; however&#44; ours&#44; is the first study evaluating the indirect impact of PCV10 vaccination in children on the serotype distribution of <span class="elsevierStyleItalic">S&#46; pneumoniae</span> causing IPD in Colombian adults&#46; Severiche-Bueno D&#46;F&#46; et al&#46; analyzed the results of <span class="elsevierStyleItalic">S&#46; pneumoniae</span>-serotypes surveillance from the SIREVA II project in Bogot&#225; &#40;2007&#8211;2017&#59; all serotype data from Bogot&#225; were included in our study&#41; and the IPD &#40;clinical data&#41; in all age groups&#46; The study determined that no herd effect was observed in adults due to an increased incidence of IPD in people over 50 years of age&#44; however they did not study the changes in serotype prevalence in that age group&#46; Conversely&#44; in the general population a significant decrease in VT10 was observed especially for serotypes 1&#44; 14 and 6B&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">22</span></a></p><p id="par0100" class="elsevierStylePara elsevierViewall">In 2010&#44; PCV10 was introduced in Brazil&#44; and a study that was conducted between 2013 and 2015 showed a predominance of NVT serotypes among IPD in the elderly population&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">23</span></a> In Mexico&#44; in adult patients with community-acquired pneumonia or IPD from three tertiary care hospitals over a 15-year period &#40;2000&#8211;2015&#41;&#44; after the introduction of PCV7&#44; the prevalence of the included serotypes declined significantly&#59; no such changes were found after introduction of the PCV13 vaccine&#44; including the prevalence of serotype 19A&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">24</span></a> In Uruguay&#44; the incidence rates of PCV7 showed a non-significant increase in the total number of isolates among adults<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>60 years of age after PCV7 introduction due to changes in diagnostic criteria or compliance with surveillance&#44; which showed an increase in the number of isolates between the pre- and post-vaccine periods for older patients &#40;from 94 to 290&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">25</span></a> similar to the results found in our study&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">In addition&#44; our results revealed a significant increase in the prevalence and variation of the ARRs of serotypes 3 and 19A in the post-PCV10 period&#59; this is concordant with the findings of other studies that have documented serotype 3 prevalence in older adults&#44; even in countries that have introduced PCV13&#46;<a class="elsevierStyleCrossRefs" href="#bib0225"><span class="elsevierStyleSup">15&#44;26</span></a></p><p id="par0110" class="elsevierStylePara elsevierViewall">In Colombia&#44; the increase in serotype 19A was not only a result of universal immunization but was also due to other factors that may have contributed to the reported increases in 19A&#44; including antibiotic pressure or the spread of multi-resistant 19A clones &#40;ST320&#44; ST276&#44; and ST1118&#41;&#44; among others&#46;<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">27</span></a> A remarkable finding concerns the relatively high MDR rates of serotype 19A&#44; and similar findings were reported in Latin America&#44; Mexico and Argentina&#44; where PCV13 was implemented in 2011 and 2012&#46;<a class="elsevierStyleCrossRefs" href="#bib0270"><span class="elsevierStyleSup">24&#44;28</span></a></p><p id="par0115" class="elsevierStylePara elsevierViewall">The Pneumococcal Serotype Replacement and Distribution Estimation &#40;PSERENADE&#41; project found that the main serotypes that caused meningitis in children<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>5 years in the countries using PCV13&#44; after 5&#8211;7 years postvaccination were 3&#44; 8&#44; 12F&#44; 23B and 23A&#44; and in Brazil were 3&#44; 19A&#44; 6C&#44; 23A and 23B following the introduction of PCV10&#46;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">29</span></a></p><p id="par0120" class="elsevierStylePara elsevierViewall">The diversity of emerging non-vaccine serotypes may be due to differences in the genetic background within the same serotype that could induce variations in disease potential or the existence of different serotypes of a single clonal lineage&#44; which could explain why the frequencies of some NVTs is increasing in some countries but not in others&#46;<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">30</span></a> Continued surveillance of serotype distributions and genetic lineages will provide knowledge for predicting future serotype trends and the development of new vaccines&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall">This study evaluated the indirect effect of immunization with PCV10 based on laboratory records&#44; but our principal limitations are associated with the unknown pneumococcal vaccination status and mortality in adults&#59; these data should be included in future studies&#46; The lack of comparison of IPD incidence rates over the same years of the study and a sub-registration of information &#40;i&#46;e&#46;&#44; using ARR as proxy of incidence rates&#41; was due to the fact that laboratory surveillance is only mandatory for meningitis and passive &#40;voluntary&#41; for other IPD&#44; however&#44; an improvement in the surveillance system is associated with the immunization of children&#44; as noted by the increased ARRs over the period of analysis&#46; Despite the limitations&#44; retrospective analysis of serotype distributions in IPD cases plays an important role in informing future vaccination strategies&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">In our study&#44; the indirect effect of PCV10 in adults was evidenced&#44; and the increased prevalence of NVT and variations in ARRs in the post-PCV10 period were significant&#44; which may indicate replacement of serotypes&#46; A decrease in IPD caused by PCV10 serotypes was observed in adults<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>50 years&#44; but an increase in NVT did not allow us to observe an overall decrease in IPD cases in this population&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">To determine if changes in the distribution of IPD-causing serotypes and antimicrobial resistance in both children and adults is due to vaccination&#44; it is necessary to maintain and improve <span class="elsevierStyleItalic">S&#46;</span><span class="elsevierStyleItalic">pneumonia</span>e surveillance&#44; including other antibiotics as quinolones&#46; Data collected by the SIREVA II surveillance can guide the introduction of new PCVs in the Latin America and Caribbean region&#44; however the addition of new serotypes to conjugated vaccines should be carefully considered&#46; With the information available to date&#44; it is difficult to predict a group of common serotypes for the region&#44; as there is clear country diversity&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Ethical issues</span><p id="par0140" class="elsevierStylePara elsevierViewall">The data was obtained from laboratory-based surveillance performed by Instituto Nacional de Salud &#8211; Colombia&#44; for this reason&#44; ethical approval was not required&#46; Collection of the isolates and information was considered as surveillance activity and was obtained with the approval of each participating hospital&#46; The data and isolates could not be traced back to the source&#46;</p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">Conflict of interests</span><p id="par0145" class="elsevierStylePara elsevierViewall">All authors declare no competing interests&#46;</p></span></span>"
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              "titulo" => "Introducci&#243;n"
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              "identificador" => "sec0055"
              "titulo" => "Antimicrobial resistance"
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          "titulo" => "Discussion"
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        8 => array:2 [
          "identificador" => "sec0065"
          "titulo" => "Ethical issues"
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          "identificador" => "sec0070"
          "titulo" => "Conflict of interests"
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          "identificador" => "xack700806"
          "titulo" => "Acknowledgments"
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          "titulo" => "References"
        ]
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    "pdfFichero" => "main.pdf"
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    "fechaRecibido" => "2023-02-14"
    "fechaAceptado" => "2023-07-09"
    "PalabrasClave" => array:2 [
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        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Keywords"
          "identificador" => "xpalclavsec1718034"
          "palabras" => array:6 [
            0 => "<span class="elsevierStyleItalic">Streptococcus pneumoniae</span>"
            1 => "Adults"
            2 => "Vaccination"
            3 => "Pneumococcal vaccines"
            4 => "Serotypes"
            5 => "Colombia"
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          "palabras" => array:5 [
            0 => "<span class="elsevierStyleItalic">Streptococcus pneumoniae</span>"
            1 => "Adultos"
            2 => "Vacunaci&#243;n"
            3 => "Vacunas antineumoc&#243;cicas&#44; Serotipos"
            4 => "Colombia"
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    "resumen" => array:2 [
      "en" => array:3 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The introduction of pneumococcal conjugate vaccine &#40;PCV&#41; into childhood vaccination programmes has reduced the prevalence of vaccine serotypes &#40;VTs&#41; that cause invasive pneumococcal disease &#40;IPD&#41; in children&#46; In the elderly population&#44; an impact has also been seen through indirect protection &#40;herd effect&#41;&#46; The aim of this study was to estimate the changes in serotype distribution and antimicrobial susceptibility of <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> isolates recovered from adult IPD and to evaluate the indirect effect of immunization with PCV10 based on laboratory records by analyzing the period from 2005 to 2019 for six years before and eight years after the universal PCV10 administration to Colombian children&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A total of 2204 <span class="elsevierStyleItalic">S&#46; pneumoniae</span> isolates from adults &#40;&#8805;50 years&#41; with IPD were analyzed&#46; The analysis examined the percentage changes in proportions &#40;prevalence&#41; and percentage variations in population rates &#40;annual reported rates &#8211; ARR&#41; of VTs between the pre-PCV10 &#40;2005&#8211;2009&#41; and post-PCV10 &#40;2015&#8211;2019&#41; periods&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">The findings were &#40;1&#41; evidence of a significant percentage decrease of pneumococcal VT10 causing IPD in adults &#40;50&#37; pre-PCV10 and 16&#37; post-PCV10&#41;&#59; &#40;2&#41; significant increase of serotype 19A &#40;from 1&#46;6&#37; to 14&#46;8&#37;&#41; and less important increase of serotype 3 &#40;from 10&#46;5&#37; to 14&#46;5&#37;&#41; and non-vaccine serotypes &#40;NVT&#41; &#40;from 21&#46;4&#37; to 38&#46;4&#37;&#41; non-significant&#59; and &#40;3&#41; meningitis and non-meningitis multidrug resistant isolates associated with serotype 19A&#46; An improvement in the surveillance system is associated with the immunization of children&#44; as noted by the increased ARRs across the analysis period&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Our results show the indirect impact of PCV10 vaccination in children on the VT10 distribution and antimicrobial resistance of <span class="elsevierStyleItalic">S&#46; pneumoniae</span> causing IPD in Colombian adults over 50 when comparing the pre-PCV10 &#40;2005&#8211;2009&#41; and post-PCV10 &#40;2015&#8211;2019&#41; periods&#46;</p></span>"
        "secciones" => array:4 [
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            "identificador" => "abst0005"
            "titulo" => "Introduction"
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            "titulo" => "Methods"
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            "titulo" => "Results"
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            "titulo" => "Conclusions"
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        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducci&#243;n</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">La introducci&#243;n de las vacunas neumoc&#243;cicas conjugadas &#40;<span class="elsevierStyleItalic">pneumococcal conjugate vaccines</span> &#91;PCV&#93;&#41; en los programas de vacunaci&#243;n infantil ha reducido la prevalencia de los serotipos vacunales &#40;<span class="elsevierStyleItalic">vaccine serotypes</span> &#91;VT&#93;&#41; que causan la enfermedad neumoc&#243;cica invasiva &#40;ENI&#41; en los ni&#241;os&#46; En la poblaci&#243;n adulta tambi&#233;n se ha visto un impacto a trav&#233;s de la protecci&#243;n indirecta &#40;efecto reba&#241;o&#41;&#46; El objetivo de este estudio fue estimar los cambios en la distribuci&#243;n de serotipos y la susceptibilidad antimicrobiana de aislamientos de <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> recuperados de ENI de adultos y evaluar el efecto indirecto de la inmunizaci&#243;n con PCV10 con base en registros de laboratorio mediante el an&#225;lisis del per&#237;odo de 2005 a 2019&#44; seis a&#241;os antes y ocho a&#241;os despu&#233;s de la administraci&#243;n universal de PCV10 a ni&#241;os colombianos&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se analizaron un total de 2&#46;204 aislamientos de <span class="elsevierStyleItalic">S&#46; pneumoniae</span> de adultos &#40;&#8805;50<span class="elsevierStyleHsp" style=""></span>a&#241;os&#41; con ENI&#46; Se examinaron los cambios porcentuales en las proporciones &#40;prevalencia&#41; y las variaciones porcentuales en las tasas poblacionales &#40;tasas anuales informadas &#91;<span class="elsevierStyleItalic">annual reported rates</span>&#44; ARR&#93;&#41; de VT entre los per&#237;odos anterior &#40;2005-2009&#41; y posterior a PCV10 &#40;2015-2019&#41;&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Los hallazgos fueron&#58; 1&#41; evidencia de una disminuci&#243;n porcentual significativa de los serotipos incluidos en la VT10 neumoc&#243;cica que causa ENI en adultos &#40;50&#37; pre-PCV10 y 16&#37; post-PCV10&#41;&#59; 2&#41; aumento significativo del serotipo 19A &#40;del 1&#44;6&#37; al 14&#44;8&#37;&#41; y aumento menos importante del serotipo 3 &#40;del 10&#44;5&#37; al 14&#44;5&#37;&#41; y de aislados no tipables &#40;NVT&#41; &#40;del 21&#44;4&#37; al 38&#44;4&#37;&#41; no significativo&#44; y 3&#41; aislamientos multirresistentes de meningitis y no-meningitis asociados con el serotipo 19A&#46; Se asoci&#243; una mejora en el sistema de vigilancia junto con la inmunizaci&#243;n de los ni&#241;os&#44; como se observa en el aumento de las ARR durante el periodo de an&#225;lisis&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Estos resultados demuestran el impacto indirecto de la vacunaci&#243;n con PCV10 en ni&#241;os en la distribuci&#243;n de serotipos VT10 y en la resistencia a antimicrobianos de <span class="elsevierStyleItalic">S&#46; pneumoniae</span> causante de ENI en adultos colombianos mayores de 50 a&#241;os&#44; cuando se compara el periodo pre-PCV10 &#40;2005-2009&#41; con el post-PCV10 &#40;2015-2019&#41;&#46;</p></span>"
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            "titulo" => "Resultados"
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            "apendice" => "<p id="par0160" class="elsevierStylePara elsevierViewall">The following are the supplementary data to this article&#58;<elsevierMultimedia ident="upi0005"></elsevierMultimedia></p>"
            "etiqueta" => "Appendix A"
            "titulo" => "Supplementary data"
            "identificador" => "sec0080"
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        ]
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      0 => array:7 [
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        "etiqueta" => "Fig&#46; 1"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
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        "descripcion" => array:1 [
          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Percentages of <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> isolates by VT10&#44; AddVT23&#44; NVT&#44; VT&#44; and the pre-PCV10 &#40;2005&#8211;2009&#41;&#44; transition &#40;2010&#8211;2014&#41; and post-PCV10 &#40;2015&#8211;2019&#41; periods&#46; VT10&#58; serotypes included in PCV10 &#40;1&#44; 4&#44; 5&#44; 6B&#44; 7F&#44; 9V&#44; 14&#44; 18C&#44; 19F&#44; 23F&#41;&#44; AddVT23&#58; the 13 additional PPV23 &#40;2&#44; 3&#44; 8&#44; 9N&#44; 10A&#44; 11A&#44; 12F&#44; 5B&#44; 17F&#44; 19A&#44; 20&#44; 22F&#44; 33F&#41;&#44; NVT&#58; non-vaccine type&#44; NT&#58; non-typable&#44; NA&#58; not apply&#46; Black line represents the number of <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> isolates recovered per year of surveillance&#46;</p>"
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          "leyenda" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">VT10&#58; serotypes included in PCV10 &#40;1&#44; 4&#44; 5&#44; 6B&#44; 7F&#44; 9V&#44; 14&#44; 18C&#44; 19F&#44; 23F&#41;&#44; AddVT23&#58; the 13 additional PPV23 &#40;2&#44; 3&#44; 8&#44; 9N&#44; 10A&#44; 11A&#44; 12F&#44; 5B&#44; 17F&#44; 19A&#44; 20&#44; 22F&#44; 33F&#41;&#44; NVT&#58; non-vaccine type&#44; NT&#58; non-typable&#44; NA&#58; not apply&#46;</p><p id="spar0080" class="elsevierStyleSimplePara elsevierViewall">&#42; Significant at p&#60;0&#46;05&#46;</p>"
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                  """
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        "descripcion" => array:1 [
          "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Distributions of <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> serotypes by VT10&#44; AddVT23&#44; NVT&#44; VT&#44; and periods&#46;</p>"
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          "leyenda" => "<p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">VT10&#58; serotypes included in PCV10 &#40;1&#44; 4&#44; 5&#44; 6B&#44; 7F&#44; 9V&#44; 14&#44; 18C&#44; 19F&#44; 23F&#41;&#44; AddVT23&#58; the 13 additional PPV23 &#40;2&#44; 3&#44; 8&#44; 9N&#44; 10A&#44; 11A&#44; 12F&#44; 5B&#44; 17F&#44; 19A&#44; 20&#44; 22F&#44; 33F&#41;&#44; NVT&#58; non-vaccine type&#44; NT&#58; non-typable&#44; NA&#58; not apply&#46;</p>"
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                  \t\t\t\t">All serotypes&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">10&#46;189&#46;188&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  """
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                  \t\t\t\t" scope="col">Antibiotic&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">n</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">n</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">n</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">PEN meningitis<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">33&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">31&#46;4&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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