Respiratory Viruses Dynamics and Interactions: Ten Years of Surveillance in Central Europe

Abstract Background: Lower respiratory tract infections are among the main causes of death. Although there are many respiratory viruses, diagnostic efforts are focused mainly on influenza. The Respiratory Viruses Network (RespVir) collects infection data, primarily from German university hospitals, for a high diversity of infections by respiratory pathogens. In this study, we computationally analysed a subset of the RespVir database, covering 217,150 samples tested for 17 different viral pathogens in the time span from 2010 to 2019. Methods: We calculated the prevalence of 17 respiratory viruses, analysed their seasonality patterns using information-theoretic measures and agglomerative clustering, and analysed their propensity for dual infection using a new metric dubbed average coinfection exclusion score (ACES). Results: After initial data pre-processing, we retained 206,814 samples, corresponding to 1,408,657 performed tests. We found that Influenza viruses were reported for less than half of all infections and that they exhibited the highest degree of seasonality Coinfections of viruses are frequent, the most prevalent coinfection was rhinovirus/bocavirus and most of the virus pairs had a positive ACES indicating a tendency to exclude each other regarding infection. Conclusions: The analysis of respiratory viruses dynamics in monoinfection and coinfection contributes to the prevention, diagnostic, treatment, and development of new therapeutics. Data obtained from multiplex testing is fundamental for this analysis and should be prioritized over single pathogen testing.

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Circulation of Respiratory Viruses in Hospitalized Adults before and during the COVID-19 Pandemic in Brescia, Italy: A Retrospective Study

International Journal of Environmental Research and Public Health ◽

10.3390/ijerph18189525 ◽

2021 ◽

Vol 18 (18) ◽

pp. 9525

Author(s):

Maria Antonia De Francesco ◽

Caterina Pollara ◽

Franco Gargiulo ◽

Mauro Giacomelli ◽

Arnaldo Caruso

Keyword(s):

Respiratory Syncytial Virus ◽

Influenza A ◽

Statistical Significance ◽

Respiratory Viruses ◽

Influenza Viruses ◽

Contact Tracing ◽

Nucleic Acid Detection ◽

Respiratory Pathogens ◽

Syncytial Virus ◽

Human Coronaviruses

Different preventive public health measures were adopted globally to limit the spread of SARS-CoV-2, such as hand hygiene and the use of masks, travel restrictions, social distance actions such as the closure of schools and workplaces, case and contact tracing, quarantine and lockdown. These measures, in particular physical distancing and the use of masks, might have contributed to containing the spread of other respiratory viruses that occurs principally by contact and droplet routes. The aim of this study was to evaluate the prevalence of different respiratory viruses (influenza viruses A and B, respiratory syncytial virus, parainfluenza viruses 1, 2, 3 and 4, rhinovirus, adenovirus, metapneumovirus and human coronaviruses) after one year of the pandemic. Furthermore, another aim was to evaluate the possible impact of these non-pharmaceutical measures on the circulation of seasonal respiratory viruses. This single center study was conducted between January 2017–February 2020 (pre-pandemic period) and March 2020–May 2021 (pandemic period). All adults >18 years with respiratory symptoms and tested for respiratory pathogens were included in the study. Nucleic acid detection of all respiratory viruses was performed by multiplex real time PCR. Our results show that the test positivity for influenza A and B, metapneumovirus, parainfluenza virus, respiratory syncytial virus and human coronaviruses decreased with statistical significance during the pandemic. Contrary to this, for adenovirus the decrease was not statistically significant. Conversely, a statistically significant increase was detected for rhinovirus. Coinfections between different respiratory viruses were observed during the pre-pandemic period, while the only coinfection detected during pandemic was between SARS-CoV-2 and rhinovirus. To understand how the preventive strategies against SARS-CoV-2 might alter the transmission dynamics and epidemic patterns of respiratory viruses is fundamental to guide future preventive recommendations.

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Epidemiology of Respiratory Pathogens among Elderly Nursing Home Residents with Acute Respiratory Infections in Corsica, France, 2013–2017

BioMed Research International ◽

10.1155/2017/1423718 ◽

2017 ◽

Vol 2017 ◽

pp. 1-7 ◽

Cited By ~ 4

Author(s):

Shirley Masse ◽

Lisandru Capai ◽

Alessandra Falchi

Keyword(s):

Nursing Home ◽

Influenza A ◽

Respiratory Infections ◽

Nursing Home Residents ◽

Respiratory Viruses ◽

Sudden Onset ◽

Influenza Viruses ◽

Influenza B ◽

Acute Respiratory Infections ◽

Respiratory Pathogens

Background. The current study aims to describe the demographical and clinical characteristics of elderly nursing home (NH) residents with acute respiratory infections (ARIs) during four winter seasons (2013/2014–2016/2017), as well as the microbiological etiology of these infections. Methods. Seventeen NHs with at least one ARI resident in Corsica, France, were included. An ARI resident was defined as a resident developing a sudden onset of any constitutional symptoms in addition to any respiratory signs. Nasopharyngeal swabs from ARI residents were screened for the presence of 21 respiratory agents, including seasonal influenza viruses. Results. Of the 107 ARI residents enrolled from NHs, 61 (57%) were positive for at least one of the 21 respiratory pathogens. Forty-one (38.3%) of the 107 ARI residents had influenza: 38 (92%) were positive for influenza A (100% A(H3N2)) and three (8%) for influenza B/Victoria. Axillary fever (≥38°C) was significantly more common among patients infected with influenza A(H3N2). Conclusion. The circulation of seasonal respiratory viruses other than influenza A(H3N2) seems to be sporadic among elderly NH residents. Investigating the circulation of respiratory viruses in nonwinter seasons seems to be important in order to understand better the dynamic of their year-round circulation in NHs.

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Viral Infections of the Upper Airway in the Setting of COVID-19: A Primer for Rhinologists

American Journal of Rhinology and Allergy ◽

10.1177/1945892420947929 ◽

2020 ◽

Vol 35 (1) ◽

pp. 122-131

Author(s):

Erick Yuen ◽

David A. Gudis ◽

Nicholas R. Rowan ◽

Shaun A. Nguyen ◽

Rodney J. Schlosser

Keyword(s):

Severe Acute Respiratory Syndrome ◽

Viral Infections ◽

Current Knowledge ◽

Middle Eastern ◽

Upper Airway ◽

Respiratory Viruses ◽

Respiratory Pathogens ◽

Infectious Agents ◽

Tract Infections ◽

Viral Respiratory

Background Viral respiratory tract infections are associated with a significant burden of disease and represent one of the leading causes of mortality worldwide. The current Coronavirus Disease 2019 (COVID-19) pandemic highlights the devastating toll that respiratory viruses have on humanity and the desperate need to understand the biological characteristics that define them in order to develop efficacious treatments and vaccines. To date, Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has infected nearly 600 times more people and resulted in 200 times more deaths relative to Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV) and Middle Eastern Respiratory Syndrome Coronavirus (MERS-CoV) combined. Objective Through this review, we aim to summarize the key characteristics of respiratory viruses that hold global significance, with a focus on SARS-CoV-2. Our goal is to disseminate our current knowledge of these infectious agents to otolaryngologists, in particular rhinologists, practicing in the COVID-19 era. Methods The general and clinical characteristics of selected respiratory viruses along with available viral treatments and vaccines are reviewed. Results There has been significant progress in our understanding of the epidemiology and pathogenesis of various respiratory viruses. However, despite the advancement in knowledge, efficacious vaccines and antiviral treatments remain elusive for most respiratory viruses. The dire need for these scientific discoveries is highlighted by the recent COVID-19 pandemic, which has prompted investigators worldwide to conduct clinical trials at an accelerated timeline in an effort to reduce the morbidity and mortality associated with SARS-CoV-2 infection. Rhinologists will continue to remain on the front-lines of pandemics associated with respiratory viruses. Conclusion In light of these unprecedented times, the need to understand the nuances of these viral respiratory pathogens, especially SARS-CoV-2, cannot be overemphasized. This knowledge base is of particular importance to otolaryngologists, whose expertise in the upper airway coincides with the anatomic tropism of these infectious agents.

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Addressing the unmet need in respiratory viruses: an interdisciplinary analysis of product development pipeline in Asia

International Journal of Clinical Trials ◽

10.18203/2349-3259.ijct20184397 ◽

2018 ◽

Vol 5 (4) ◽

pp. 151

Author(s):

Jelle J. Feddema ◽

Eric Claassen

Keyword(s):

Product Development ◽

Respiratory Infections ◽

Unmet Need ◽

Respiratory Viruses ◽

Influenza Viruses ◽

Non Profit ◽

Significant Burden ◽

Development Pipeline ◽

Tract Infections ◽

Global Initiatives

Background: Respiratory tract infections (RTIs) pose a significant burden on health systems worldwide. Progress has been booked in reducing RTI disease burden through development of diagnostics, therapeutics and vaccines, though most efforts often fail to address the contribution of non-influenza viruses. Increasing awareness and the prevailing unmet need has resulted in the establishment of initiatives that aim to explore ways in which to extend innovation efforts for influenza to the broad range of respiratory viruses. This study will provide a detailed description of the state of the RTI market in Asia.Methods: By developing a dataset containing data from patent documents and clinical trials (CTs) we aimed to provide a detailed description of the RTI market in Asia.Results: We found a downward patent filing trend in respiratory diagnostics but a high number of phase 3 studies. A strong preference for the development of therapeutics and vaccines targeting bacterial pneumonia and influenza became apparent, whereas less attention is given towards product development targeting non-influenza viruses.Conclusions: The findings indicate a mature respiratory diagnostics market with minor industrial interest but at the same time an evolving RTI CT market with a strong late-stage pipeline. Asia represents only a handful of studies related to non-influenza viruses, mostly conducted by non-profit organisations. The business segment appears to focus upon product development for more profitable respiratory infections thereby suggesting that involvement and engagement of the industry within global initiatives and efforts to increase innovation for non-influenza viruses is not optimal.

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Broad respiratory testing to identify SARS-CoV-2 viral co-circulation and inform diagnostic stewardship in the COVID-19 pandemic

10.21203/rs.3.rs-119566/v1 ◽

2020 ◽

Author(s):

Natalie C. Marshall ◽

Ruwandi M. Kariyawasam ◽

Nathan Zelyas ◽

Mathew A. Diggle

Keyword(s):

Public Health ◽

Respiratory Viruses ◽

Cross Reactivity ◽

Respiratory Pathogen ◽

Health Concern ◽

Respiratory Pathogens ◽

Public Health Importance ◽

Clinical Laboratories ◽

Pathogen Testing ◽

Virus Testing

Abstract Background: SARS-CoV-2 infection can present with a broad clinical differential that includes many other respiratory viruses; therefore, accurate tests are crucial to distinguish true COVID-19 cases from pathogens that do not require urgent public health interventions. Co-circulation of other respiratory viruses is largely unknown during the COVID-19 pandemic but would inform strategies to rapidly and accurately test patients with respiratory symptoms.Methods: This study retrospectively examined 298,415 respiratory specimens collected from symptomatic patients for SARS-CoV-2 testing in the three months since COVID-19 was initially documented in the province of Alberta, Canada. By focusing on 52,285 specimens that were also tested with the Luminex Respiratory Pathogen Panel for 17 other pathogens, this study examines the prevalence of 18 potentially co-circulating pathogens and their relative rates in prior years versus since COVID-19 emerged, including four endemic coronaviruses. Results: SARS-CoV-2 was identified in 2.2% of specimens. Parallel broad multiplex testing detected additional pathogens in only 3.4% of these specimens: significantly less than in SARS-CoV-2-negative specimens (p < 0.0001), suggesting very low rates of SARS-CoV-2 co-infection. Furthermore, the overall co-infection rate was significantly lower among specimens with SARS-CoV-2 detected (p < 0.0001). Finally, less than 0.005% of all specimens tested positive for both SARS-CoV-2 and any of the four endemic coronaviruses tested, strongly suggesting neither co-infection nor cross-reactivity between these coronaviruses. Conclusions: Broad respiratory pathogen testing rarely detected additional pathogens in SARS-CoV-2-positive specimens. While helpful to understand co-circulation of respiratory viruses causing similar symptoms as COVID-19, ultimately these broad tests were resource-intensive and inflexible in a time when clinical laboratories face unprecedented demand for respiratory virus testing, with further increases expected during influenza season. A transition from broad, multiplex tests toward streamlined diagnostic algorithms targeting respiratory pathogens of public health concern could simultaneously reduce the overall burden on clinical laboratories while prioritizing testing of pathogens of public health importance. This is particularly valuable with ongoing strains on testing resources, exacerbated during influenza seasons.

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Broad respiratory testing to identify SARS-CoV-2 viral co-circulation and inform diagnostic stewardship in the COVID-19 pandemic

Virology Journal ◽

10.1186/s12985-021-01545-9 ◽

2021 ◽

Vol 18 (1) ◽

Author(s):

Natalie C. Marshall ◽

Ruwandi M. Kariyawasam ◽

Nathan Zelyas ◽

Jamil N. Kanji ◽

Mathew A. Diggle

Keyword(s):

Public Health ◽

Respiratory Viruses ◽

Cross Reactivity ◽

Respiratory Pathogen ◽

Health Concern ◽

Respiratory Pathogens ◽

Public Health Importance ◽

Clinical Laboratories ◽

Pathogen Testing ◽

Virus Testing

Abstract Background SARS-CoV-2 infection can present with a broad clinical differential that includes many other respiratory viruses; therefore, accurate tests are crucial to distinguish true COVID-19 cases from pathogens that do not require urgent public health interventions. Co-circulation of other respiratory viruses is largely unknown during the COVID-19 pandemic but would inform strategies to rapidly and accurately test patients with respiratory symptoms. Methods This study retrospectively examined 298,415 respiratory specimens collected from symptomatic patients for SARS-CoV-2 testing in the three months since COVID-19 was initially documented in the province of Alberta, Canada (March-May, 2020). By focusing on 52,285 specimens that were also tested with the Luminex Respiratory Pathogen Panel for 17 other pathogens, this study examines the prevalence of 18 potentially co-circulating pathogens and their relative rates in prior years versus since COVID-19 emerged, including four endemic coronaviruses. Results SARS-CoV-2 was identified in 2.2% of all specimens. Parallel broad multiplex testing detected additional pathogens in only 3.4% of these SARS-CoV-2-positive specimens: significantly less than in SARS-CoV-2-negative specimens (p < 0.0001), suggesting very low rates of SARS-CoV-2 co-infection. Furthermore, the overall co-infection rate was significantly lower among specimens with SARS-CoV-2 detected (p < 0.0001). Finally, less than 0.005% of all specimens tested positive for both SARS-CoV-2 and any of the four endemic coronaviruses tested, strongly suggesting neither co-infection nor cross-reactivity between these coronaviruses. Conclusions Broad respiratory pathogen testing rarely detected additional pathogens in SARS-CoV-2-positive specimens. While helpful to understand co-circulation of respiratory viruses causing similar symptoms as COVID-19, ultimately these broad tests were resource-intensive and inflexible in a time when clinical laboratories face unprecedented demand for respiratory virus testing, with further increases expected during influenza season. A transition from broad, multiplex tests toward streamlined diagnostic algorithms targeting respiratory pathogens of public health concern could simultaneously reduce the overall burden on clinical laboratories while prioritizing testing of pathogens of public health importance. This is particularly valuable with ongoing strains on testing resources, exacerbated during influenza seasons.

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Influenza and Other Respiratory Viruses Involved in Severe Acute Respiratory Disease in Northern Italy during the Pandemic and Postpandemic Period (2009–2011)

BioMed Research International ◽

10.1155/2014/241298 ◽

2014 ◽

Vol 2014 ◽

pp. 1-5 ◽

Cited By ~ 6

Author(s):

Elena Pariani ◽

Marianna Martinelli ◽

Marta Canuti ◽

Seyed Mohammad Jazaeri Farsani ◽

Bas B. Oude Munnink ◽

...

Keyword(s):

Respiratory Disease ◽

Influenza A ◽

Case Fatality ◽

Respiratory Viruses ◽

Northern Italy ◽

Influenza Viruses ◽

Respiratory Pathogens ◽

Severe Acute Respiratory Infection ◽

Influenza A H1n1 ◽

The Impact

Since 2009 pandemic, international health authorities recommended monitoring severe and complicated cases of respiratory disease, that is, severe acute respiratory infection (SARI) and acute respiratory distress syndrome (ARDS). We evaluated the proportion of SARI/ARDS cases and deaths due to influenza A(H1N1)pdm09 infection and the impact of other respiratory viruses during pandemic and postpandemic period (2009–2011) in northern Italy; additionally we searched for unknown viruses in those cases for which diagnosis remained negative. 206 respiratory samples were collected from SARI/ARDS cases and analyzed by real-time RT-PCR/PCR to investigate influenza viruses and other common respiratory pathogens; also, a virus discovery technique (VIDISCA-454) was applied on those samples tested negative to all pathogens. Influenza A(H1N1)pdm09 virus was detected in 58.3% of specimens, with a case fatality rate of 11.3%. The impact of other respiratory viruses was 19.4%, and the most commonly detected viruses were human rhinovirus/enterovirus and influenza A(H3N2). VIDISCA-454 enabled the identification of one previously undiagnosed measles infection. Nearly 22% of SARI/ARDS cases did not obtain a definite diagnosis. In clinical practice, great efforts should be dedicated to improving the diagnosis of severe respiratory disease; the introduction of innovative molecular technologies, as VIDISCA-454, will certainly help in reducing such “diagnostic gap.”

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Multipathogen Detection in Patients with Respiratory Tract Infection: Identification of Non-respiratory Viruses Using Multiplex Real-time Polymerase Reaction

Jundishapur Journal of Microbiology ◽

10.5812/jjm.120553 ◽

2022 ◽

Vol 14 (11) ◽

Author(s):

Khosrow Agin ◽

Zahra Heydarifard ◽

Leila Ghalichi ◽

Mahmood Yaghoobi ◽

Hamidreza Hagh Ranjbar ◽

...

Keyword(s):

Respiratory Tract ◽

Real Time ◽

Herpes Virus ◽

Respiratory Viruses ◽

Respiratory Pathogens ◽

Human Herpes ◽

Human Herpes Virus ◽

Herpès Virus ◽

Tract Infections ◽

Respiratory Specimens

Background: Due to the overlapping clinical characteristics of respiratory tract infections (RTIs) and the unavailability of appropriate diagnostic techniques, the diagnosis of RTIs is controversial. Objectives: The study aimed to prompt the diagnosis of RTIs using commercial multiplex real-time PCR. Methods: The survey undertook for two years (2019 - 2020) on 144 flu-negative immunocompetent outpatients. Respiratory samples were examined by multiplex PCR assays. Results: Study population consisted of females (n = 77, 53.5%) and males (n = 67, 46.5%). The mean age was 42.8 ± 23.7 years. Thirty-one (21.5%) patients were infected with only one viral or bacterial infection. Eighty-two (57%) were infected with more than one pathogen. Ninety-five (37%) and 161 (62%) tests were positive for bacterial and viral pathogens, respectively. Community-acquired Pneumonia (CAP) and atypical CAP pathogens included 17% and 10% of respiratory specimens, respectively. The predominant pathogens consisted of Human Herpes Virus 7 (HHV-7) (n = 38, 15.5%), Epstein-Barr Virus (EBV) (n = 34, 13.8%), Mycoplasma pneumoniae (n = 24, 9.8%), and Human Herpes Virus 6 (HHV-6) (n = 21, 8.5%). There were associations between pathogen findings and special age categories. Fever, cough, dyspnea, and hemoptysis were associated with certain pathogens. There was no substantial difference between viral and bacterial Ct concerning gender, age group, and comorbidities. Conclusions: Multiplex diagnostic assays significantly increased the rate of appropriate diagnosis of respiratory pathogens. However, further investigation is needed to find non-respiratory viruses' significance in respiratory specimens of immunocompetent symptomatic patients.

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An algorithmic approach to the use of rapid molecular diagnostics for SARS-CoV-2, influenza viruses, and other respiratory pathogens during an unprecedented respiratory season

American Journal of Clinical Pathology ◽

10.1093/ajcp/aqab191.277 ◽

2021 ◽

Vol 156 (Supplement_1) ◽

pp. S130-S130

Author(s):

A S Maris ◽

L Tao ◽

C W Stratton ◽

R M Humphries ◽

J E Schmitz

Keyword(s):

Point Of Care ◽

Random Access ◽

Access Point ◽

Clinical Situation ◽

Influenza Viruses ◽

Respiratory Pathogen ◽

Respiratory Pathogens ◽

Test Volume ◽

Dumpster Diving ◽

Pathogen Testing

Abstract Introduction/Objective The COVID-19 pandemic exacerbated deficiencies of testing personnel, reagents, supplies and disposables, instruments, and automation in many clinical laboratories. Upon entering respiratory season, a strategy was warranted to optimize laboratory resources when supplies were already limited and expected respiratory season test volume was unknown. An algorithm was devised to prioritize test ordering and TAT based on patient clinical scenario. Methods/Case Report The institutional respiratory season SARS-CoV-2 algorithm was constructed by a multidisciplinary team including infectious disease, infection prevention, laboratory, and IT/LIS leadership. CDC guidance on influenza testing was incorporated. Antigen-based testing was discontinued; only molecular amplification- based platforms with FDA EUA were utilized. Platforms had a range of TAT (20 minutes to 8 hours) and included fully- automated high throughput, rapid random access, point-of-care, and CDC SARS-CoV-2 assays. Test bundles included SARS-CoV-2 (monoplex), or SARS-CoV-2 + fluA&B (triplex), or SARS-CoV-2 + respiratory pathogen panel (multiplex RPP; includes 22 targets, including flu A&B). Results (if a Case Study enter NA) Key factors in the algorithm included whether the patient was outpatient or inpatient, hospital employee or not, symptomatic or not, immunocompetent or immunocompromised, and whether a concurrent order for other respiratory pathogens was included or not. Clinician responses for these factors determined the type of swab collected (wet swab in VTM or dry swab) and how quickly the TAT was indicated for a given patient using a colored-dot sticker system. Priority TAT in decreasing order was symptomatic inpatients, asymptomatic pre- procedure patients, asymptomatic admissions, symptomatic employees, and symptomatic outpatients. Conclusion An algorithm for respiratory pathogen testing during an unprecedented respiratory season prioritizes result TAT to an individual patient’s clinical situation while maximizing laboratory stewardship by eliminating redundant influenza testing and requiring ‘all upfront’ orders to avoid add-on orders that require ‘dumpster diving’ for samples. Limitations include inherent differences in sensitivity, LOD, and specificity when multiple different platforms are utilized to detect the same analytes.

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Respiratory tract infections among French Hajj pilgrims from 2014 to 2017

Scientific Reports ◽

10.1038/s41598-019-54370-0 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 8

Author(s):

Van-Thuan Hoang ◽

Saliha Ali-Salem ◽

Khadidja Belhouchat ◽

Mohammed Meftah ◽

Doudou Sow ◽

...

Keyword(s):

Risk Factors ◽

Respiratory Tract ◽

Respiratory Symptoms ◽

Respiratory Tract Infections ◽

Influenza Viruses ◽

Respiratory Pathogen ◽

Respiratory Pathogens ◽

Increased Risk ◽

Human Coronaviruses ◽

Tract Infections

AbstractRespiratory tract infections (RTIs) are common among Hajj pilgrims, but risk factors for RTIs and respiratory pathogen acquisition during the Hajj are not clearly identified. Based on previous studies, most frequent pathogens acquired by Hajj pilgrims were investigated: rhinovirus, human coronaviruses, influenza viruses, Streptococcus pneumoniae, Staphylococcus aureus, Klebsiella pneumoniae and Haemophilus influenzae. 485 pilgrims were included. 82.1% presented with RTIs. Respiratory chronic diseases were associated with cough, Influenza-like illness (ILI) and the acquisition of H. influenzae. Vaccination against invasive pneumococcal diseases (IPD) and influenza was associated with a decrease in the acquisition of S. pneumoniae and prevalence of ILI (aRR = 0.53, 95%CI [0.39–0.73] and aRR = 0.69, 95%CI [0.52–0.92] respectively). Individuals carrying rhinovirus and H. influenzae-S. pneumoniae together were respectively twice and five times more likely to have respiratory symptoms. Individual with H. influenzae-K. pneumoniae carriage were twice (p = 0.04) as likely to develop a cough. The use of disposable handkerchiefs was associated with a decrease in the acquisition of S. aureus (aRR = 0.75, 95%CI [0.57–0.97]). Results could be used to identify pilgrims at increased risk of RTIs and acquisition of respiratory pathogens. Results also confirm the effectiveness of influenza and IPD vaccinations in reducing ILI symptoms and acquisition of S. pneumoniae carriage respectively.

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