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Reduction in the incidence of invasive infections caused by encapsulated bacteria after the onset of the COVID-19 pandemic
Reducción de la incidencia de infecciones invasivas por bacterias capsuladas luego del inicio de la Pandemia por COVID-19
Leda Guzzia,b,
Corresponding author
ledaguzzi@hotmail.com

Corresponding author.
, Juan Manuel Sambadea, Martin Diego Christina, Federico Rodriguez Cairolic, Alejandra Rodriguezd, Silvia Vicariod, Miriam Hinojosa Del Carpioa, Juan Molinosa, Pablo Dimitroffa
a Clínica Olivos, Swiss Medical Group, Vicente López, Argentina
b Sociedad Argentina de Infectología, Argentina
c Instituto de Efectividad Clínica y Sanitaria (IECS), Argentina
d Servicio de Microbiología Clínica, Swiss Medical Group, Ciudad Autónoma de Buenos Aires, Argentina
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Introduction</span><p id="par0025" class="elsevierStylePara elsevierViewall">Invasive bacterial infections such as bacteremic pneumonia&#44; empyema&#44; meningitis&#44; and sepsis are life threatening conditions&#46; Encapsulated bacteria&#44; namely <span class="elsevierStyleItalic">Streptococcus pneumoniae</span>&#44; <span class="elsevierStyleItalic">Haemophilus influenzae</span> and <span class="elsevierStyleItalic">Neisseria meningitidis</span> are among the most common pathogens&#44; causing a high burden of disease&#44; especially in children under 5 years of age&#44; adults over 65 years of age and in individuals with comorbidities&#46; Mortality rates reaching up to 36&#37; for invasive pneumococcal disease &#40;IPD&#41; in winter&#44; made prevention of invasive infections a priority for WHO&#44; leading to the development of effective vaccines<a class="elsevierStyleCrossRefs" href="#bib0185"><span class="elsevierStyleSup">9&#44;10&#44;12</span></a>&#46; Bacterial pathogens habitually colonize the respiratory tract&#44; particularly in children&#44; presenting a commensal relationship with the host unless local or systemic immune deficiencies facilitate invasion into sterile tissues<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">26</span></a>&#46; Although transmission mechanisms are still under investigation&#44; person-to-person spread through exposure to infectious secretions is widely accepted as the main source&#46; Recent animal models have shown airborne transmission also occurs between close contacts&#44; enhanced by coinfection with respiratory viruses<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">27</span></a>&#46; A paradigmatic example is synergism between influenza viruses and <span class="elsevierStyleItalic">S&#46; pneumoniae</span> contributing to pulmonary superinfection<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">25</span></a>&#46; Since December 2019&#44; emergence of a novel severe acute respiratory syndrome coronavirus 2 &#40;SARS-CoV-2&#41; causing coronavirus disease 2019 &#40;COVID-19&#41; has threatened global health&#46; On March 3&#44; 2020&#44; the first case was reported in Argentina and on March 11&#44; WHO declared COVID-19 a global pandemic&#46; To control spread of the virus&#44; compulsory containment measures were established in Argentina on March 20&#44; including discontinuation of non-essential services such as schools&#44; public or private social gatherings&#44; and restricted use of public transport&#46; Essential workers &#40;in healthcare&#44; security services&#44; among others&#41; were excluded<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">2&#44;7</span></a>&#46; Social distancing&#44; use of face masks and adequate ventilation of indoor spaces were recommended&#46; Individuals over the age 60 and&#47;or immunocompromised individuals were encouraged to stay at home<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">2&#44;23</span></a>&#46; Although adherence to these measures declined as the epidemic evolved&#44; use of face masks was sustained over time&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Large-scale application of containment measures&#44; as shown by various studies&#44; led to a significant reduction in incidence of other viral infections such as influenza&#44; Respiratory Syncytial Virus and Enterovirus<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">4&#44;6&#44;11&#44;14&#44;22&#44;28</span></a>&#46; Interaction between SARS-CoV-2 and encapsulated bacteria is still under investigation&#44; and frequency of coinfection has yet to be established&#46; Other questions of interest include&#44; whether health strategies for pandemic containment and mitigation influenced incidence of invasive infections due to encapsulated bacteria &#40;IIEB&#41;&#44; as occurs with other viral pathogens&#44; and whether coinfection increased case fatality rates&#46; The main objective of this study was to evaluate IIEB rates during the COVID-19 pandemic and compare incidence levels to the ones reported during the year prior to the pandemic&#46; As a secondary objective&#44; incidence of COVID-19&#47;IIEB coinfection and case fatality rate were also examined&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Methods</span><p id="par0035" class="elsevierStylePara elsevierViewall">A cross-sectional study was performed&#46; Data from a centralized microbiology laboratory serving a network of privately administered healthcare institutions in Buenos Aires City &#40;CABA&#41; and the greater Buenos Aires Metropolitan Area &#40;BAMA&#41; were collected&#46; The network includes 713 inpatient beds for children and adults&#44; which were expanded by 20&#37; during the pandemic&#46; Three periods were evaluated&#58; &#40;1&#41; pre-pandemic&#58; March 1&#44; 2019&#8211;February 29&#44; 2020&#59; &#40;2&#41; pandemic year 1&#58; March 1&#44; 2020&#8211;February 28&#44; 2021&#59; and &#40;3&#41; pandemic year 2&#58; March 1&#44; 2021&#8211;July 31&#44; 2021&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Biological samples collected from sterile sites &#40;blood&#44; cerebrospinal fluid&#44; pleural fluid&#44; synovial fluid&#44; etc&#46;&#41; of patients attending the emergency departments&#44; general wards and intensive care units of the network centers were analyzed&#46; Samples positive for <span class="elsevierStyleItalic">S&#46; pneumoniae</span>&#44; <span class="elsevierStyleItalic">H&#46; influenzae</span>&#44; and <span class="elsevierStyleItalic">N&#46; meningitidis</span> were identified&#44; and clinical characteristics&#44; laboratory results&#44; and outcome of patients with IIEB collected from medical records&#46; During the second and third period&#44; occurrence of COVID-19 &#40;confirmed by positive RT-PCR&#41; and IIEB coinfection was investigated and considered primary &#40;when simultaneous to IIEB&#41; or secondary &#40;diagnosed at least 3 days after hospital admission&#41;&#46; In-hospital case fatality rate of IIEB was determined&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Descriptive statistical analysis was conducted&#46; Categorical variables were expressed as absolute and relative frequencies&#46; Continuous variables were characterized with measures of central tendency &#40;mean and median&#41; and measures of dispersion &#40;ranges&#41;&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">The study was approved by the Institutional Review Board&#46; Sensitive patient data were protected by confidentiality and coding&#46; Only investigators directly related to the research and competent authorities had access to the information&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Results</span><p id="par0055" class="elsevierStylePara elsevierViewall">Between March 1&#44; 2019 and July 31&#44; 2021&#44; a total of 56<span class="elsevierStyleHsp" style=""></span>502 biological samples belonging to 27<span class="elsevierStyleHsp" style=""></span>224 patients were assessed&#59; 54<span class="elsevierStyleHsp" style=""></span>403 &#40;96&#37;&#41; were blood cultures and 2099 &#40;4&#37;&#41; from other sterile sites&#46; Fifty-four samples from 54 subjects were positive for encapsulated bacteria&#44; of which 50 were <span class="elsevierStyleItalic">S&#46; pneumoniae</span> and 4 <span class="elsevierStyleItalic">H&#46; influenzae</span>&#46; <span class="elsevierStyleItalic">N&#46; meningitidis</span> was not found during the study period &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0060" class="elsevierStylePara elsevierViewall">Demographics of the study population and risk factors for IIEB are shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0065" class="elsevierStylePara elsevierViewall">The most common causes for hospitalization were&#58; pneumonia &#40;28 cases&#41; and diarrhea &#40;2&#41; during period 1&#59; suspected SARS-CoV-2 infection &#40;3&#41;&#44; pneumonia &#40;1&#41;&#44; acute-on-chronic kidney disease &#40;1&#41; and febrile neutropenia and abdominal pain &#40;1&#41; during period 2&#59; and SARS-CoV-2 infection &#40;4&#41; in period 3&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Global cumulative incidence of IIEB was 95&#46;57 per 100<span class="elsevierStyleHsp" style=""></span>000 samples&#46; Comparative analysis showed incidence varied by period &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a> and <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0015"></elsevierMultimedia><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">Between the first and second period&#44; cumulative incidence of <span class="elsevierStyleItalic">S&#46; pneumoniae</span> infections decreased by 136&#46;21 cases per 100<span class="elsevierStyleHsp" style=""></span>000 samples &#40;relative decrease 0&#46;15&#41;&#46; However&#44; between the second and third&#44; 27&#46;19 more cases per 100<span class="elsevierStyleHsp" style=""></span>000 samples &#40;relative increase 2&#46;17&#41; were observed&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">Cumulative incidence of <span class="elsevierStyleItalic">H&#46; influenzae</span> infections between periods 1 and 2 showed an increase of 1&#46;33 cases per 100<span class="elsevierStyleHsp" style=""></span>000 samples &#40;relative increase 1&#46;17&#41;&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">During periods 2 and 3&#44; total number of COVID-19 hospitalizations was 12<span class="elsevierStyleHsp" style=""></span>328&#59; 12 IIEB occurred&#44; of which 10 were due to <span class="elsevierStyleItalic">S&#46; pneumoniae</span> and 2 to <span class="elsevierStyleItalic">H&#46; influenzae</span>&#46; Seven cases of SARS-CoV-2&#47;<span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfection were identified&#44; 2 primary and 5 secondary&#46; Coinfection rate was 0&#46;056&#37; in patients hospitalized for COVID-19&#44; corresponding to an incidence of 5&#46;68 per 10<span class="elsevierStyleHsp" style=""></span>000 hospitalizations for COVID-19&#46; However&#44; in a subanalysis of patients hospitalized with IPD&#44; we found that 7 of 10 subjects were co-infected with SARS-COV-2&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Overall case fatality in IIEB patients was 33&#37;&#44; &#40;31&#37;&#44; 29&#37;&#44; and 60&#37; for periods 1&#44; 2 and 3 respectively&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0020">Table 4</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0020"></elsevierMultimedia><p id="par0095" class="elsevierStylePara elsevierViewall">All deaths occurred in patients with <span class="elsevierStyleItalic">S&#46; pneumoniae</span> infections&#44; except for 1 patient with <span class="elsevierStyleItalic">H&#46; influenzae</span> in period 1&#46; Case fatality of SARS-C0V-2&#47;<span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfection reached 43&#37; &#40;3 of 7 subjects&#41;&#44; whereas case fatality of IPD cases without COVID-19 coinfection was 32&#46;5&#37;&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Overall&#44; all-cause in-hospital mortality in COVID-19 patients between March 1&#44; 2020&#44; and July 31&#44; 2021&#44; was 4&#37; &#40;492 deaths&#41;&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Discussion</span><p id="par0105" class="elsevierStylePara elsevierViewall">A significant reduction in incidence of IPD was observed during the period 2020&#8211;2021&#44; coinciding with the implementation of large-scale containment measures to mitigate the spread of the COVID-19 pandemic&#46; This reduction was more pronounced during the first year of the pandemic &#40;period 2&#41;&#44; probably because more stringent restrictions were enforced&#46; Only 4 cases of invasive <span class="elsevierStyleItalic">H&#46; influenzae</span> infections occurred over the whole study period&#44; with no differences observed between periods&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">From March to July 2021&#44; a small increase in the incidence of IPD was observed compared to the first pandemic year&#44; coinciding with relaxing of restrictions&#46; Median age of hospitalized patients with IIEB was younger &#40;43 years&#41; during period 3 than during periods 2 &#40;70 years&#41; and 1 &#40;64 years&#41;&#44; in line with the decrease in average age of COVID-19 hospitalized patients in 2021&#44; during the second disease wave in Argentina&#44; and the launch of a vaccination program for healthcare workers and adults over 60 years of age&#44; which began in the first quarter of 2021&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">During the study period we observed a reduction in the incidence of IPD&#46; Our findings coincide with those of Brueggemann et al&#46;&#44; who conducted a large prospective laboratory surveillance study&#44; in 26 countries and territories on 6 continents&#44; finding a significant and sustained reduction in invasive <span class="elsevierStyleItalic">S&#46; pneumoniae</span> infections&#44; that reached 68&#37; in the first 4 weeks&#44; and 82&#37; in the following 8 weeks after introduction of restrictions on human mobility &#40;measured using Google COVID-19 Community Mobility Reports digital tool&#41;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">5</span></a>&#46; The authors suggested interruption of person-to-person transmission of <span class="elsevierStyleItalic">S&#46; pneumoniae</span> as the most plausible explanation for this reduction&#44; in the context of pandemic-related confinement measures&#46; Since the nasopharynx of children is the natural ecological niche of <span class="elsevierStyleItalic">S&#46; pneumoniae</span>&#44; school closures&#44; in addition to strict protection measures in older adults&#44; were the most probable reasons for the fall in IPDs observed&#46; In Tuscany&#44; Italy&#44; Lastrucci et al&#46; reported a significant reduction in the incidence of hospitalizations for community-acquired pneumonia in the elderly&#44; during the first wave of COVID-19&#44; compared to the previous 3 years&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">19</span></a> Less use of antimicrobials in the community was also observed during this period&#44; suggesting patients with pneumonia had not been treated in the outpatient setting&#46; The authors therefore attributed the fall in community acquired pneumonia to the indirect impact of the lockdown&#46; In Japan&#44; Hiroyuki et al&#46; also reported a significant reduction in the number of patients hospitalized for community pneumonia&#44; between August&#44; 2019 and July&#44; 2020&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">21</span></a></p><p id="par0120" class="elsevierStylePara elsevierViewall">Similar observations were made in younger populations&#46; Friedrich et al&#46; analyzed causes for hospital admission in children under 14 years of age in Brazil&#44; finding a significant decrease in hospitalizations for pneumonia in 2020 compared to the period 2015 to 2019&#44; for all age groups&#44; but especially in children under 9 years of age&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">13</span></a> This reduction coincided with the implementation of non-pharmacological measures to contain the pandemic&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall">Another relevant finding of our study was the low frequency of SARS-CoV-2&#47;<span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfection&#59; the observed incidence was 5&#46;68 per 10<span class="elsevierStyleHsp" style=""></span>000 hospitalizations for COVID-19&#46; It should be clarified that only invasive <span class="elsevierStyleItalic">S&#46; pneumoniae</span> infections were considered since samples were from sterile sites&#46; Conversely&#44; in patients hospitalized for IPD during the pandemic&#44; SARS-CoV-2 coinfection rate was 70&#37;&#46; The low rate of bacterial coinfections in patients hospitalized for COVID-19 argues in favor of avoiding unnecessary early use of antimicrobial agents&#44; which predisposes to spread of multidrug-resistant gram negative bacteria both in the hospital and in the community&#46;<a class="elsevierStyleCrossRefs" href="#bib0145"><span class="elsevierStyleSup">1&#44;8&#44;15&#44;20</span></a> Lansbury et al&#46; performed a meta-analysis of 30 studies and found&#44; of a total of 3834 patients hospitalized for COVID-19&#44; 7&#37; had bacterial coinfections&#44; increasing to 14&#37; for patients admitted to the ICU&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">18</span></a> The most frequent pathogens were <span class="elsevierStyleItalic">Mycoplasma pneumoniae</span> &#40;47&#37;&#41;&#44; <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span> &#40;12&#37;&#41;&#44; and <span class="elsevierStyleItalic">H&#46; influenzae</span> &#40;12&#37;&#41;&#46; Another meta-analysis carried out by Langford et al&#46; estimated 3&#46;5&#37; of patients with COVID-19 had a primary bacterial coinfection and 14&#46;3&#37; developed secondary bacterial infections during hospitalization&#46;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">17</span></a> A retrospective study performed by Hughes et al&#46; included 836 patients hospitalized for COVID-19&#44; 27 &#40;3&#46;2&#37;&#41; presented bacterial coinfection early&#44; within 5 days of admission&#44; increasing to 51 &#40;6&#46;1&#37;&#41; during the remaining hospital stay&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">16</span></a> No <span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfections were found&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">With respect to SARS-CoV-2 and <span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfections&#44; the largest study to date was conducted in England by Amin-Chowdhury et al&#46;&#44; between February and June&#44; 2020&#44; monitoring incidence of IPD and COVID-19 during lockdown&#46; The authors reported 30&#37; reduction in the incidence of IPD cases&#44; even after adjusting for age&#44; gender&#44; and bacterial serotype&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">3</span></a> The rate of coinfection was 0&#46;025&#37; for patients diagnosed with COVID-19&#44; and 3&#46;5&#37; in those hospitalized for IPD&#46; Risk of coinfection increased with age&#44; and high blood pressure and dementia were the most common comorbidities&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">In our study&#44; case fatality rate of SARS-COV-2&#47;<span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfection was high &#40;43&#37;&#41;&#44; greater than for isolated IPD cases &#40;32&#46;5&#37;&#41;&#44; and for in-hospital COVID-19 cases &#40;4&#37;&#41;&#46; These findings are similar to the Lansbury meta-analysis&#44; which reported a 5&#46;82-fold increase in the risk of dying in coinfected patients&#46;<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">18</span></a> Rodriguez-Nava et al&#46;&#44; who analyzed 11 episodes of SARS-CoV-2 and <span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfection&#44; also found high mortality rate &#40;64&#37;&#41; during hospitalization&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">24</span></a> In the surveillance study conducted by Amin-Chowdhury&#44; 30-day mortality was 3&#46;88 times higher in patients who developed COVID-19 after IPD and 7&#46;75 times higher in those with primary coinfection&#44; compared to those with IPD alone&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">3</span></a></p><p id="par0140" class="elsevierStylePara elsevierViewall">Limitations to our study include the fact that patients originated from the Buenos Aires metropolitan area &#40;CABA and BAMA&#41; exclusively&#44; with access to private healthcare or social security&#46; Although this region has one of the highest incidences of COVID-19 in the country&#44; no patients from the public health system were included&#46; Furthermore&#44; information on pneumococcal vaccination status of patients was not available&#44; and the third study period was shorter than the first two&#46; Finally&#44; because of its observational nature&#44; statistical results presented are descriptive only&#46; Lack of data precluded further analysis since univariate analysis without adjusting for other variables could have led to incorrect conclusions&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusions</span><p id="par0145" class="elsevierStylePara elsevierViewall">This study is the first in Argentina to assess the incidence of IIEB&#44; particularly due to <span class="elsevierStyleItalic">S&#46; pneumoniae</span>&#44; in the context of the COVID-19 pandemic&#46; Significant reduction compared to the pre-pandemic year was observed&#44; coinciding with implementation of public health strategies for pandemic containment and mitigation&#46; The potential impact of these measures on other health conditions beyond COVID-19&#44; such as IPD&#44; is remarkable&#46; Based on these findings&#44; we believe that people with risk factors for IPD would strongly benefit from continued use of face masks and social distancing&#44; beyond the pandemic&#44; in particular during winter&#46; We also observed low rates of SARS-CoV-2 and invasive <span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfection&#44; supporting the concept that early antimicrobial treatment in COVID-19 patients is unnecessary&#46; Finally&#44; case fatality was higher in coinfected patients than in those presenting IPD&#44; or in-hospital COVID-19 alone&#44; suggesting a potential adverse synergistic interaction between pathogens&#44; although further studies will be needed to confirm this hypothesis&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Funding</span><p id="par0150" class="elsevierStylePara elsevierViewall">None declared&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Conflicts of interest</span><p id="par0155" class="elsevierStylePara elsevierViewall">The authors declare that there are no conflicts of interest&#46;</p></span></span>"
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    "highlights" => array:2 [
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      "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">&#8226;</span><p id="par0005" class="elsevierStylePara elsevierViewall">IIEB incidence dropped dramatically during the COVID-19 pandemic&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">&#8226;</span><p id="par0010" class="elsevierStylePara elsevierViewall">Reduction coincided with public health measures to contain the pandemic&#46;</p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">&#8226;</span><p id="par0015" class="elsevierStylePara elsevierViewall">We observed low rates of SARS-COV2 and invasive <span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfection&#46;</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">&#8226;</span><p id="par0020" class="elsevierStylePara elsevierViewall">Case fatality was higher in coinfected patients than in those presenting IPD&#46;</p></li></ul></p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Interaction between severe acute respiratory coronavirus 2 &#40;SARS-CoV-2&#41; and IIEB remains under investigation&#46; Objective&#58; to compare IIEB incidence before and during COVID-19 pandemic&#44; and assess incidence of coinfection with COVID-19 and case fatality&#46; A cross-sectional study was performed on data from a centralized microbiology laboratory serving a network of healthcare centers comprising 713 pediatric and adult inpatient beds&#44; expanded by 20&#37; during the pandemic&#46; Three periods were evaluated&#58; &#40;1&#41; pre-pandemic&#58; March 1&#44; 2019&#8211;February 29&#44; 2020&#59; &#40;2&#41; pandemic year 1&#58; March 1&#44; 2020&#8211;February 28&#44; 2021&#59; &#40;3&#41; pandemic year 2&#58; March 1&#44; 2021&#8211;July 31&#44; 2021&#46; Descriptive statistical analysis was performed&#46; 56 502 samples &#40;96&#37; blood cultures&#41; from 27<span class="elsevierStyleHsp" style=""></span>224 patients were analyzed&#46; Of these&#44; 54 samples &#40;from 54 patients&#41; were positive for encapsulated bacteria&#46; IIEB incidence was&#58; 167&#46;4&#44; 32&#46;6&#44; and 50&#46;4 per 100<span class="elsevierStyleHsp" style=""></span>000 samples for periods 1&#44; 2&#44; and 3&#44; respectively&#46; Twelve IIEB episodes occurred during the pandemic period&#58; 10 <span class="elsevierStyleItalic">Streptococcus pneumoniae</span>&#44; and 2 <span class="elsevierStyleItalic">Haemophilus influenzae</span>&#44; of which 7 were SARS-CoV-2&#47;<span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfections&#44; with an incidence of 5&#46;68 per 10<span class="elsevierStyleHsp" style=""></span>000 COVID-19-related hospitalizations &#40;0&#46;056&#37;&#41;&#46; IIEB case fatality was 31&#37;&#44; 29&#37;&#44; and 60&#37; for each period&#44; respectively&#44; 3&#47;7 patients with coinfection died &#40;43&#37;&#41;&#46; Case fatality for invasive pneumococcal disease &#40;IPD&#41; in patients without COVID-19&#44; was 32&#46;5&#37;&#46; Significant reduction in IIEB incidence was observed during the pandemic&#44; coinciding with implementation of containment measures&#46; The incidence of SARS-CoV-2&#47;<span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfection was low&#44; with higher case fatality than IPD patients without COVID-19&#46;</p></span>"
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        "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">La interacci&#243;n entre SARS-CoV-2 e infecciones invasivas por bacterias capsuladas &#40;IIBC&#41; contin&#250;a bajo estudio&#46; Objetivos&#58; comparar la incidencia de IIBC antes y durante la pandemia por COVID-19&#44; evaluar la incidencia de coinfecci&#243;n con COVID-19 y la letalidad&#46; Estudio transversal de registros de un laboratorio centralizado de Microbiolog&#237;a&#44; que asiste a una red de centros asistenciales con 713 camas de internaci&#243;n para adultos y pedi&#225;tricos&#44; expandida 20&#37; durante la pandemia&#46; Tres periodos evaluados&#58; 1&#41; Pre-pandemia&#58; 1-Marzo-2019 al 29-Febrero-2020&#59; 2&#41; Primer a&#241;o de Pandemia&#58; 1-Marzo-2020 al 28-Febrero-2021&#59; 3&#41; Pandemia 2021&#58; 1-Marzo-2021 al 31-Julio-2021&#46; An&#225;lisis estad&#237;stico descriptivo&#58; Se analizaron 56&#46;502 muestras &#40;96&#37; hemocultivos&#41; correspondientes a 27&#46;224 pacientes&#46; De estas&#44; 54 muestras &#40;de 54 pacientes&#41; fueron positivas para bacterias capsuladas&#46; La incidencia de IIBC fue 167&#44;4&#44; 32&#44;6 y 50&#44;4 por cada 100&#46;000 muestras para los periodos 1&#44; 2 y 3&#44; respectivamente&#46; Doce IIBC ocurrieron durante la pandemia&#58; 10 <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> y dos <span class="elsevierStyleItalic">Haemophilus influenzae</span>&#44; siete de ellos corresponden a coinfecci&#243;n SARS-CoV-2&#47;<span class="elsevierStyleItalic">S&#46; pneumoniae</span>&#44; con una incidencia de 5&#44;68 por cada 10&#46;000 internaciones por COVID 19 &#40;0&#44;056&#37;&#41;&#46; La letalidad de las IIBC fue de 31&#44; 29 y 60&#37; para los tres periodos&#44; respectivamente&#44; 3&#47;7 coinfectados fallecieron &#40;43&#37;&#41;&#46; La letalidad por enfermedad neumoc&#243;cica invasiva &#40;ENI&#41;&#44; sin COVID fue de 32&#44;5&#37;&#46; Se evidenci&#243; una reducci&#243;n significativa de la incidencia de IIBC luego del comienzo de la pandemia&#44; coincidente con la implementaci&#243;n de las medidas sanitarias de contenci&#243;n de la pandemia&#46; La incidencia de coinfecci&#243;n de SARS-CoV-2&#47;<span class="elsevierStyleItalic">S&#46; pneumoniae</span> fue baja y present&#243; mayor letalidad que las ENI sin COVID-19&#46;</p></span>"
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                  \t\t\t\t">9&#46;3&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 ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>&#8226; Age&#58; mean&#47;median&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">57&#46;5&#47;64&#46;5&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">41&#46;4&#47;43&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">56&#46;5&#47;63&#46;3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>&#8226; Minimum age&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">6 years&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10 years&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">28 years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>&#8226; Maximum age&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">85 years&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">64 years&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">94 years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>&#8226; Male&#47;female ratio&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">0&#46;83&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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;33&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="left" valign="\n
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                  \t\t\t\t">0&#46;25&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="left" valign="\n
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                  \t\t\t\t">0&#46;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="5" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="\n
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                  \t\t\t\t  " colspan="5" align="left" valign="\n
                  \t\t\t\t\ttop\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>&#8226; Older than 64 years of age&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">21&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="left" valign="\n
                  \t\t\t\t\ttop\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>&#8226; Chronic obstructive pulmonary disease&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">1&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">16&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>&#8226; Cancer&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">12&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</td></tr><tr title="table-row"><td class="td-with-role" title="\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Period 3March&#8211;July 2021&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">S&#46; pneumoniae</span>&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">159&#46;46&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">23&#46;25&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">50&#46;44&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">H&#46; influenzae</span>&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">7&#46;97&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9&#46;3&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="4" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Total&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">167&#46;4&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">32&#46;6&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">50&#46;44&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
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                0 => "xTab3488995.png"
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            0 => array:3 [
              "identificador" => "tblfn0010"
              "etiqueta" => "&#42;"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0010">Expressed as cumulative incidence per 100<span class="elsevierStyleHsp" style=""></span>000 samples&#46;</p>"
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">IIEB incidence according to time period and pathogen&#46;</p>"
        ]
      ]
      4 => array:8 [
        "identificador" => "tbl0020"
        "etiqueta" => "Table 4"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at4"
            "detalle" => "Table "
            "rol" => "short"
          ]
        ]
        "tabla" => array:1 [
          "tablatextoimagen" => array:1 [
            0 => array:2 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Period 1&#40;pre pandemic&#41;&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Period 2&#40;pandemic year 1&#41;&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Period 3&#40;pandemic year 2&#41;&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Total&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Overall case fatality&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">31&#37; &#40;13&#47;42&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">29&#37; &#40;2&#47;7&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">60&#37; &#40;3&#47;5&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">18&#47;54 &#40;33&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Invasive <span class="elsevierStyleItalic">S&#46; pneumoniae</span> infections&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">30&#37; &#40;12&#47;40&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">20&#37; &#40;2&#47;5&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">60&#37; &#40;3&#47;5&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">34&#37; &#40;17&#47;50&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">SARS-CoV-2&#47;<span class="elsevierStyleItalic">S&#46; pneumoniae</span> coinfection&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#95;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">33&#37; &#40;1&#47;3&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">50&#37; &#40;2&#47;4&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">43&#37; &#40;3&#47;7&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">S&#46; pneumoniae</span> without COVID-19&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">30&#37; &#40;12&#47;40&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">50&#37; &#40;1&#47;2&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">100&#37; &#40;1&#47;1&#41;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t">32&#46;5&#37; &#40;14&#47;43&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
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        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Case fatality of IIEB according to pathogen and time period&#46;</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0015"
          "bibliografiaReferencia" => array:28 [
            0 => array:3 [
              "identificador" => "bib0145"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Low rate of bacterial co-infection in patients with COVID-19"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "H&#46; Adler"
                            1 => "R&#46; Ball"
                            2 => "M&#46; Fisher"
                            3 => "K&#46; Mortimer"
                            4 => "M&#46;S&#46; Vardhan"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/S2666-5247(20)30036-7"
                      "Revista" => array:5 [
                        "tituloSerie" => "Lancet Microbe"
                        "fecha" => "2020"
                        "volumen" => "1"
                        "paginaInicial" => "e62"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/32835331"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            1 => array:3 [
              "identificador" => "bib0150"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Boletin Oficial de la Rep&#250;blica Argentina&#46; Decreto 297&#47;2020&#46; DECNU-2020-297-APN-PTE &#8211; Disposiciones"
                      "autores" => array:1 [
                        0 => array:2 [
                          "colaboracion" => "Aislamiento Social Preventivo y Obligatorio"
                          "etal" => false
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Libro" => array:1 [
                        "fecha" => "2020"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            2 => array:3 [
              "identificador" => "bib0155"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Impact of the coronavirus disease 2019 &#40;COVID-19&#41; pandemic on invasive pneumococcal disease and risk of pneumococcal coinfection with severe acute respiratory syndrome coronavirus 2 &#40;SARS-CoV-2&#41;&#58; prospective national cohort study&#44; England"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:9 [
                            0 => "Z&#46; Amin-Chowdhury"
                            1 => "F&#46; Aiano"
                            2 => "A&#46; Mensah"
                            3 => "C&#46;L&#46; Sheppard"
                            4 => "D&#46; Litt"
                            5 => "N&#46;K&#46; Fry"
                            6 => "N&#46; Andrews"
                            7 => "M&#46;E&#46; Ramsay"
                            8 => "S&#46;N&#46; Ladhani"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1093/cid/ciaa1728"
                      "Revista" => array:6 [
                        "tituloSerie" => "Clin Infect Dis"
                        "fecha" => "2021"
                        "volumen" => "72"
                        "paginaInicial" => "e65"
                        "paginaFinal" => "e75"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/33196783"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            3 => array:3 [
              "identificador" => "bib0160"
              "etiqueta" => "4"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Coronavirus disease 2019 pandemic&#58; impact caused by school closure and national lockdown on pediatric visits and admissions for viral and nonviral infections &#8211; a time series analysis"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:13 [
                            0 => "F&#46; Angoulvant"
                            1 => "N&#46; Ouldali"
                            2 => "D&#46;D&#46; Yang"
                            3 => "M&#46; Filser"
                            4 => "V&#46; Gajdos"
                            5 => "A&#46; Rybak"
                            6 => "R&#46; Guedj"
                            7 => "V&#46; Soussan-Banini"
                            8 => "R&#46; Basmaci"
                            9 => "A&#46; Lefevre-Utile"
                            10 => "D&#46; Brun-Ney"
                            11 => "L&#46; Beaujouan"
                            12 => "D&#46; Skurnik"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:5 [
                        "tituloSerie" => "Clin Infect Dis"
                        "fecha" => "2021"
                        "volumen" => "72"
                        "paginaInicial" => "319"
                        "paginaFinal" => "322"
                      ]
                    ]
                  ]
                ]
              ]
            ]
            4 => array:3 [
              "identificador" => "bib0165"
              "etiqueta" => "5"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Changes in the incidence of invasive disease due to <span class="elsevierStyleItalic">Streptococcus pneumoniae</span>&#44; <span class="elsevierStyleItalic">Haemophilus influenzae</span>&#44; and <span class="elsevierStyleItalic">Neisseria meningitidis</span> during the COVID-19 pandemic in 26 countries and territories in the Invasive Respiratory Infection Surveillance Initiative&#58; a prospective analysis of surveillance data"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:95 [
                            0 => "A&#46;B&#46; Brueggemann"
                            1 => "M&#46;J&#46; Jansen van Rensburg"
                            2 => "D&#46; Shaw"
                            3 => "N&#46;D&#46; McCarthy"
                            4 => "K&#46;A&#46; Jolley"
                            5 => "M&#46;C&#46;J&#46; Maiden"
                            6 => "M&#46;P&#46;G&#46; van der Linden"
                            7 => "Z&#46; Amin-Chowdhury"
                            8 => "D&#46;E&#46; Bennett"
                            9 => "R&#46; Borrow"
                            10 => "M&#46;C&#46; Brandileone"
                            11 => "K&#46; Broughton"
                            12 => "R&#46; Campbell"
                            13 => "B&#46; Cao"
                            14 => "C&#46; Casanova"
                            15 => "E&#46;H&#46; Choi"
                            16 => "Y&#46;W&#46; Chu"
                            17 => "S&#46;A&#46; Clark"
                            18 => "H&#46; Claus"
                            19 => "J&#46; Coelho"
                            20 => "M&#46; Corcoran"
                            21 => "S&#46; Cottrell"
                            22 => "R&#46;J&#46; Cunney"
                            23 => "T&#46; Dalby"
                            24 => "H&#46; Davies"
                            25 => "L&#46; de Gouveia"
                            26 => "A&#46;E&#46; Deghmane"
                            27 => "W&#46; Demczuk"
                            28 => "S&#46; Desmet"
                            29 => "R&#46;J&#46; Drew"
                            30 => "M&#46; du Plessis"
                            31 => "H&#46; Erlendsdottir"
                            32 => "N&#46;K&#46; Fry"
                            33 => "K&#46; Fuursted"
                            34 => "S&#46;J&#46; Gray"
                            35 => "B&#46; Henriques-Normark"
                            36 => "T&#46; Hale"
                            37 => "M&#46; Hilty"
                            38 => "S&#46; Hoffmann"
                            39 => "H&#46; Humphreys"
                            40 => "M&#46; Ip"
                            41 => "S&#46; Jacobsson"
                            42 => "J&#46; Johnston"
                            43 => "J&#46; Kozakova"
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ISSN: 03257541
Original language: English
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es en pt

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?

Você é um profissional de saúde habilitado a prescrever ou dispensar medicamentos