The role of pneumonia and secondary bacterial infection in fatal and serious outcomes of pandemic influenza a(H1N1)pdm09

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pneumonia 42 Title: BMC Infectious DiseasesThe role of pneumonia and secondary bacterial infection in fatal and serious outcomes of pandemic influenza a(H1N1)pdm09Chandini
pneumonia 434 12/2018Publication date (collection): /2018AbstractBackgroundThe aim of this study was to estimate the prevalence of pneumonia and secondary bacterial infections during the pandemic of influenza A(H1N1)pdm09.MethodsA systematic
pneumonia 1050 were reported in 11 studies, in which any co-infection was identified in 23% of cases (Streptococcus pneumonia e 29%). Eleven studies reported bacterial co-infection among hospitalised cases of A(H1N1)2009pdm with
pneumonia 1172 Eleven studies reported bacterial co-infection among hospitalised cases of A(H1N1)2009pdm with confirmed pneumonia , with a mean of 19% positive for bacteria (Streptococcus pneumoniae 54%). Of 16 studies of intensive
pneumonia 1239 of A(H1N1)2009pdm with confirmed pneumonia, with a mean of 19% positive for bacteria (Streptococcus pneumonia e 54%). Of 16 studies of intensive care unit (ICU) patients, bacterial co-infection identified in a mean
pneumonia 1384 care unit (ICU) patients, bacterial co-infection identified in a mean of 19% of cases (Streptococcus pneumonia e 26%). The mean prevalence of bacterial co-infection was 12% in studies of hospitalised patients not
pneumonia 1524 bacterial co-infection was 12% in studies of hospitalised patients not requiring ICU (Streptococcus pneumonia e 33%) and 16% in studies of paediatric patients hospitalised in general or pediatric intensive care
pneumonia 1667 paediatric patients hospitalised in general or pediatric intensive care unit (PICU) wards (Streptococcus pneumonia e 16%).ConclusionWe found that few studies of the 2009 influenza pandemic reported on bacterial complications
pneumonia 1932 this, secondary bacterial infection was identified in almost one in four patients, with Streptococcus pneumonia e the most common bacteria identified. Bacterial complications were associated with serious outcomes
pneumonia 3026 may also predispose to influenza and other viral infection [[9]]. During the 1918 pandemic, bacterial pneumonia was a major cause of morbidity and mortality, as shown by studies at the time as well as retrospective
pneumonia 3454 secondary bacterial sepsis. The most important bacterial co-infections during an influenza pandemic S. pneumonia e, H. influenzae, S. aureus, and group A Streptococcus (1, 4). However, two early reviews of severe cases
pneumonia 3637 two early reviews of severe cases of 2009 pandemic influenza A (H1N1) showed no evidence of bacterial pneumonia among 30 hospitalized patients with laboratory-confirmed cases in California (5) and 10 intensive-care
pneumonia 3976 no role in pandemic influenza deaths in 2009.The aim of this study was to estimate the prevalence of pneumonia and secondary bacterial infections during the 2009 pandemic of influenza A(H1N1)pdm09.MethodsSearch
pneumonia 5378 bacterial infections OR text words bacteria*, streptococcus, pneumococcus or staphylococcus adjacent to pneumonia , secondary, infection or evidence. The second search strategy included the influenza search terms and
pneumonia 7634 tested, including those reporting negative findings. We excluded studies reporting suspected bacterial pneumonia on the basis of clinical findings alone and studies which tested specimens for presence of co-infection
pneumonia 8017 were excluded if no data on other results were reported. We present the number of cases of reported pneumonia and those requiring mechanical ventilation as per the investigators definition.Data extraction and assessmentFive
pneumonia 8687 diagnostic data and treatment. Clinical outcomes included the diagnosis of bacterial co-infection, pneumonia , and death. Treatment included mechanical ventilation and use of antibiotics. Diagnostic data included
pneumonia 8817 Treatment included mechanical ventilation and use of antibiotics. Diagnostic data included determination of pneumonia and bacterial testing. We also extracted methodological details of the relevant studies including study
pneumonia 9747 interpretation provided. We present results separately for fatal cases, hospitalised cases with confirmed pneumonia , cases admitted to intensive care units (ICU) and hospitalised cases admitted to general wards including
pneumonia 10731 bacterial findings varied widely in the included published studies. It was not clear in many studies if pneumonia was community or hospital acquired. The studies also varied in their methodologies and proportion of
pneumonia 12999 support during their hospitalisation and 25–94% of patients with clinical and/or autopsy evidence of pneumonia (viral or bacterial). From chart reviews, positive bacterial growth ranged from 2 to 38% (mean bacterial
pneumonia 13200 (mean bacterial 23%) [[9]] of autopsied cases. Of the total coinfection cases, 29% were Streptococcus pneumonia e. The overall rate of bacterial infection was significantly higher in fatal cases compared to nonfatal
pneumonia 13889 48 hAntibioticsbn/N (%) pre n/N (%) onn/N (%) during admissionPositive bacterial growthN (%) bacterial pneumonia N (%) with S.pneumoniaeSite of isolationICUMechanical VentilationFajardo-Dolci (2009) [[14]]Mexico16/3/09–16/5/09Medical
pneumonia 13911 pre n/N (%) onn/N (%) during admissionPositive bacterial growthN (%) bacterial pneumoniaN (%) with S. pneumonia eSite of isolationICUMechanical VentilationFajardo-Dolci (2009) [[14]]Mexico16/3/09–16/5/09Medical
pneumonia 14211 (100)NR84/100 (84.0)56/100 (56)NR94/100 (94)2/100 (2%)(Site not mentioned)77/82 (94.0)CXR suggestive of pneumonia .NRLee (2010) [[1]]USA4/09–7/09Enhanced surveillance/confirmed cases in New York City.N = 4731/47
pneumonia 16155 co-infection positive through PCR and histopathology on lung tissue38/64 (59) radiological diagnosis of pneumonia 10/100 (10)Lung tissue through PCRCDC (2009) [[16]]USA5/09–8/09Case series (US CDC), multiple (8)
pneumonia 17026 blood or sputum culture34/115 (29.6) positive on blood or sputum culture97/113 (85.8)CXR suggestive of pneumonia 3/115 (2.6) bronchoalveolar lavage (BAL)Streptococcus was also isolated from blood of one caseNakajima
pneumonia 17944 “On” = started on admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia , viral pneumonia and ARDSNo diff Did not differentiate between aetiology of abnormal chest imagingaNumber
pneumonia 17961 admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia, viral pneumonia and ARDSNo diff Did not differentiate between aetiology of abnormal chest imagingaNumber (percentage)
pneumonia 18403 reported in the first 100 confirmed deaths in Mexico [[14]] where 94% of patients had multiple foci of pneumonia (based on imaging) and 84% required mechanical ventilation, and only 2 cases had positive bacterial
pneumonia 19894 bacteria tested for.Bacterial co-infection among hospitalised cases of A(H1N1)2009pdm with confirmed pneumonia Eleven studies reported on influenza A(H1N1)pdm09 among hospitalised cases with evidence of pneumonia
pneumonia 19995 pneumoniaEleven studies reported on influenza A(H1N1)pdm09 among hospitalised cases with evidence of pneumonia and are summarised in Table 2. Pneumonia was largely defined based on radiological findings in these
pneumonia 20257 reported in 9/11 studies and positive bacterial growth was ranged from 0 to 47% (mean 19%). Streptococcus pneumonia e was the most commonly isolated pathogen (54%). In these 9 studies, Acinobacter baumanii was the next most
pneumonia 20446 Acinobacter baumanii was the next most commonly identified bacteria (5–21%), followed by MRSA (3–6%), S. pneumonia e (2–4%) and K. Pneumonia in (1–8%). Of the 11 studies, 2 reported no evidence of bacterial co-infection
pneumonia 21006 identified.Table 2Bacterial co-infection among hospitalised cases of A(H1N1)2009pdm with confirmed pneumonia (n = 11)Author and yearStudy typeStudy populationCase severityAntivirals*n/N (%) anyn/N (%) 48 hAntibiotics†n/N
pneumonia 21215 48 hAntibiotics†n/N (%) pren/N (%) onn/N (%) during admissionAny positive bacterial growthn/N (%) S. pneumonia e[Site of isolation]N (%)pneumoniaMethodDiff/no diffICUMechanical VentilationDeathsPerez-Padilla (2009)
pneumonia 21249 onn/N (%) during admissionAny positive bacterial growthn/N (%) S.pneumoniae[Site of isolation]N (%) pneumonia MethodDiff/no diffICUMechanical VentilationDeathsPerez-Padilla (2009) [[23]]Mexico3/09–4/09Single-centre
pneumonia 21454 [[23]]Mexico3/09–4/09Single-centre case series (retrospective medical record review) of patients admitted to hospital with pneumonia and A(H1N1)pdm09 (N = 18)N = 1812/18 (66.7)12/18 (66.7)7/18 (38.9)14/18 (77.7)12/18 pre (66.7)17/18
pneumonia 21656 pre (66.7)17/18 post (94.4)0/6 (0) BC0/2 (0) BA0/1 (0) pleural fluid4/18 (22.2) Ventilator Associated pneumonia 0/18 [NR]NP swab and bronchial aspirates18 (100)CXRNo diffChien (2010) [[3]]Taiwan07/09–8/09Nation-wide
pneumonia 21866 [[3]]Taiwan07/09–8/09Nation-wide notified cases (retrospective medical record review)New pulmonary infiltrates consistent with pneumonia , compatible clinical presentations.Identification of clinicalyl significant bacteria in respiratory
pneumonia 22774 case series (retrospective medical record review) of patients admitted to a tertiary hospital with pneumonia and H1N1(N = 68)Blood cultures (BC) - Any patient with high fever > 38.0 °C for ≥3 days
pneumonia 24451 and/or a positive urinary antigen test26/210 (12.4)All CXR positivePiacentini [[57]]Compares H1N1 with pneumonia in ICU and community acquiredN = 1010/10 (100)5/10 (50)0/10 (0)10/10 (100)10/10 (100)2/10 (20.0)Pre-treatment
pneumonia 24605 (100)5/10 (50)0/10 (0)10/10 (100)10/10 (100)2/10 (20.0)Pre-treatment BC, SC, and urinary Ag for S. pneumonia e and Legionella sp.2/10 (20)Specimen type NRCXR positive (multilobar infiltrates) all except 2 (single
pneumonia 24825 infiltrates)Mulrennan [[58]]New pulmonary infiltrates on imaging + clinical symptomsCompared with non- pneumonia H1N1N = 3511/35 (31.4)10/35 (28.6)2/35 (5.7)35/35 (100)NR5/35 (14.3)NP, lower resp. tarctNR35/35
pneumonia 25539 diffBusi [[4]]N = 40NRNR1/40 (2.5)NRNR0/40 (0) Specimen NR40/40 (100) 40 had findings consistent with pneumonia . These 28/40 (70 bilaterial) Non-DiffAntibiotics: time started – “Pre” = started prior admission,
pneumonia 25775 “On” = started on admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia , viral pneumonia and ARDS;No diff Did not differentiate between aetiology of abnormal chest imaging,
pneumonia 25792 admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia, viral pneumonia and ARDS;No diff Did not differentiate between aetiology of abnormal chest imaging, NR not reportedSix
pneumonia 26528 PCR assay for respiratory bacterial panels (for detection of Legionella pneumophila, Chlamydophila pneumonia e, and Mycoplasma pneumoniae) and Binax NOW, an in vitro immunochromatographic assay for Streptococcus
pneumonia 26555 bacterial panels (for detection of Legionella pneumophila, Chlamydophila pneumoniae, and Mycoplasma pneumonia e) and Binax NOW, an in vitro immunochromatographic assay for Streptococcus pneumonia. However, the mPCR
pneumonia 26640 and Mycoplasma pneumoniae) and Binax NOW, an in vitro immunochromatographic assay for Streptococcus pneumonia . However, the mPCR assay did not test for S. pneumoniae in one study and the authors could not report
pneumonia 26695 immunochromatographic assay for Streptococcus pneumonia. However, the mPCR assay did not test for S. pneumonia e in one study and the authors could not report the presence of this organism [[23]].Bacterial co-infection
pneumonia 27677 studies and bacterial co-infection was identified in 1–43% of cases (mean bacterial 19%, Streptococcus pneumonia e 26%). One study assessed differences in mortality outcomes based on secondary bacterial pneumonia.
pneumonia 27776 pneumoniae 26%). One study assessed differences in mortality outcomes based on secondary bacterial pneumonia . In a large study involving admissions to 35 ICUs for ILI and ARF requiring mechanical ventilation in
pneumonia 27952 requiring mechanical ventilation in Argentina (n = 337), 24% of included patients had bacterial pneumonia on admission, 8% with S. pneumoniae [[5]]. S.pneumoniae co-infection was associated with higher mortality
pneumonia 27987 Argentina (n = 337), 24% of included patients had bacterial pneumonia on admission, 8% with S. pneumonia e [[5]]. S.pneumoniae co-infection was associated with higher mortality (OR 2.72 95% CI 1.05–7.06),
pneumonia 28007 (n = 337), 24% of included patients had bacterial pneumonia on admission, 8% with S. pneumoniae [[5]]. S. pneumonia e co-infection was associated with higher mortality (OR 2.72 95% CI 1.05–7.06), despite concurrent
pneumonia 28630 48 hAntibiotics†n/N (%) pren/N (%) onn/N (%) during admissionAny positive bacterial growthNumber (%) patients with S. pneumonia e and site of isolationNumber (%) with bacterial pneumonia- Method- Diff/no diffICU - ECMOMechanical VentilationDeathsMiller
pneumonia 28688 bacterial growthNumber (%) patients with S.pneumoniae and site of isolationNumber (%) with bacterial pneumonia - Method- Diff/no diffICU - ECMOMechanical VentilationDeathsMiller (2010) [[36]]Utah, USA5/09–6/09Adults(16+)Multicentre
pneumonia 33588 “On” = started on admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia , viral pneumonia and ARDSNo diff Did not differentiate between aetiology of abnormal chest imagingaH1N1
pneumonia 33605 admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia, viral pneumonia and ARDSNo diff Did not differentiate between aetiology of abnormal chest imagingaH1N1 testing = 53
pneumonia 34400 and any positive bacterial growth was reported in 1.6–76% cases (mean bacterial 12%, Streptococcus pneumonia e 33%). The number of patients with S.pneumoniae co-infection varied from 1 to 31% depending on site
pneumonia 34447 in 1.6–76% cases (mean bacterial 12%, Streptococcus pneumoniae 33%). The number of patients with S. pneumonia e co-infection varied from 1 to 31% depending on site of sample. Palacios et al. conducted a study in
pneumonia 34659 Argentina and bacteria was found in 76% of nasopharyngeal samples (152/199), of which Streptococcus pneumonia e was isolated in 31% (62/199) samples [[42]].Table 4Bacterial co-infection reported among hospitalised
pneumonia 35067 symptomsAntibiotics†n/N (%) pren/N (%) onn/N (%) during admissionAny positive bacterial growthNumber (%) patients with S. pneumonia e and site of isolationNumber (%) with bacterial pneumonia- Method- Diff/no diffICUNMV- typeDeathsCDC
pneumonia 35125 bacterial growthNumber (%) patients with S.pneumoniae and site of isolationNumber (%) with bacterial pneumonia - Method- Diff/no diffICUNMV- typeDeathsCDC (2009) [[59]]California, USA4/09–5/09State-wide passive
pneumonia 38686 IV = 21/631 (3.3)29/631 (4.6)474/631 (75.1)- NS366/631 (58)4/102 (3.9%) of cases with radiological pneumonia 1/102 (0.9) sputum culture0/102 (0) BC102/349 (29.2)- CXR- No diffSanta-Olalla Peralta [[72]] (2010)Spain4/09–12/09National
pneumonia 39434 (48.2)Bac culture pos3/29 (10.3), site NS14/29 (48.2) confirmed and 10/29 (34.5) probable bacterial pneumonia - NR- DiffJartti [[74]]Cases with severe cases and CXR finding available, I hospital in FinlandN = 13518/135
pneumonia 40539 “On” = started on admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia , viral pneumonia and ARDSNo diff Did not differentiate between aetiology of abnormal chest imagingBacterial
pneumonia 40556 admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia, viral pneumonia and ARDSNo diff Did not differentiate between aetiology of abnormal chest imagingBacterial co-infection
pneumonia 41469 to January 2010. Bacteria were isolated from nasopharyngeal swabs of 87% admitted cases (40/46)- S. pneumonia e 37.0%; S. pneumoniae and H. influenzae 23.9%, H. influenza, 26.1% and S. aureus 23.9%.Table 5Bacterial
pneumonia 41490 Bacteria were isolated from nasopharyngeal swabs of 87% admitted cases (40/46)- S. pneumoniae 37.0%; S. pneumonia e and H. influenzae 23.9%, H. influenza, 26.1% and S. aureus 23.9%.Table 5Bacterial co-infection reported
pneumonia 41834 influenza/ casesAntiviral agents- Number (%) started ≤48 h of symptomsNumber (%) patients with S. pneumonia e and site of isolationAny bacteria positiveNumber (%) with bacterial pneumonia- Method- Diff/no diffAntibiotics
pneumonia 41913 (%) patients with S.pneumoniae and site of isolationAny bacteria positiveNumber (%) with bacterial pneumonia - Method- Diff/no diffAntibiotics used (Pre, on, during)RequiredICU - ECMOMVDeathsHospitalisedLouie (2010)
pneumonia 42654 (25.0) empyema10 /121 (8)Blood culture25/251 (10.0) bacterial confirm- Among 92 CXR, 78% diagnosis was pneumonia -NonDiff186/251 (74.1)- On = 8247/251 (18.7)42/251 (16.7)13/251 (5.2)Okada [[43]] 2011Japan7/09–1/10Single-centre
pneumonia 42979 (n = unclear).PCR/4644/46 (95.6)- NR28/46 (60.9)NP40/46 (86.9)NP positive swab40/46 (86.9%)NP swabBac pneumonia 21/46 (45.6%) unilateral infiltrates- CXR- No diff32/46 (69.6)- NSNRNR0/46 (0)Kumar [[79]] (2010)Wisconsin,
pneumonia 45654 NR (before ICU admission =49)0/38 (0) BC15/274 (5.5) respiratory secretionsBC: 0274/838 (32.7) had pneumonia /other bacterial co-infectionFrom resp. secretions274/838 (32.7) had pneumonia/other bacterial co-infectionFrom
pneumonia 45732 secretionsBC: 0274/838 (32.7) had pneumonia/other bacterial co-infectionFrom resp. secretions274/838 (32.7) had pneumonia /other bacterial co-infectionFrom resp. secretionsNR838/838 (100)- 33 (3.9)546/838 (67.3)75/838 (8.9) Shin
pneumonia 46394 “On” = started on admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia , viral pneumonia and ARDSNo diff Did not differentiate between aetiology of abnormal chest imagingDiscussionSecondary
pneumonia 46411 admission, “During” = started during admissionDiff Differentiated between bacterial pneumonia, viral pneumonia and ARDSNo diff Did not differentiate between aetiology of abnormal chest imagingDiscussionSecondary
pneumonia 46875 mortality, with higher rates in adults, ICU patients and those with a fatal outcome. Streptococcus pneumonia e was the most common bacteria identified, and in ICU patients, ventilator associated pneumonia with
pneumonia 46970 Streptococcus pneumoniae was the most common bacteria identified, and in ICU patients, ventilator associated pneumonia with organisms such as Acinetobacter baumannii, Achromobacter xylosoxidans, methicillin-resistant Staphylococcus
pneumonia 49350 tissue samples collected during the 1918 influenza pandemic and histologic evidence of severe bacterial pneumonia was found in almost all samples [[10]]. The authors also did a literature search around autopsy case
pneumonia 49776 al. reviewed the studies that reported more than 10 sterile-site antemortem cultures from adults with pneumonia during 1918 pandemic [[48]]. Culture positivity rates among influenza cases without pneumonia was very
pneumonia 49870 with pneumonia during 1918 pandemic [[48]]. Culture positivity rates among influenza cases without pneumonia was very low (mean < 1%), compare to those with pneumonia (mean, 16%; range, 2 to 50) [[48]]. Bacterial
pneumonia 49932 positivity rates among influenza cases without pneumonia was very low (mean < 1%), compare to those with pneumonia (mean, 16%; range, 2 to 50) [[48]]. Bacterial co-infection rates among hospitalised cases with confirmed
pneumonia 50047 (mean, 16%; range, 2 to 50) [[48]]. Bacterial co-infection rates among hospitalised cases with confirmed pneumonia in this study was 19%, which is comparable to Chien et al.The rate of bacterial co-infection may be
pneumonia 50241 co-infection may be underestimated as many cases are not tested for bacterial infections, and bacterial pneumonia cannot always be differentiated from viral pneumonia on the basis of clinical presentation, radiology
pneumonia 50294 tested for bacterial infections, and bacterial pneumonia cannot always be differentiated from viral pneumonia on the basis of clinical presentation, radiology and routine blood tests. There is also a need to develop
pneumonia 50794 pneumococcal vaccines [[49]]. The CAPITA trial shows efficacy of conjugate pneumococcal vaccine against pneumonia [[50]], and the polysaccharide vaccine also has efficacy against invasive pneumococcal disease [[51]].
pneumonia 51061 influenza during the 2009 pandemic did comprise secondary bacterial causes, including streptococcus pneumonia e as a contributing factor. Vaccination against streptococcus pneumonia is often neglected in pandemic
pneumonia 51132 causes, including streptococcus pneumoniae as a contributing factor. Vaccination against streptococcus pneumonia is often neglected in pandemic planning [[52]], but could have a positive impact on morbidity and mortality.
pneumonia 51611 impact of a pandemic.To our knowledge, this is the first systematic review to estimate the prevalence of pneumonia and secondary bacterial infections during pandemic influenza A(H1N1)pdm09. We calculated bacterial co-infection
pneumonia 51801 calculated bacterial co-infection rates separately for fatal cases, hospitalised cases with confirmed pneumonia , hospitalised cases admitted to ICU, hospitalised cases admitted to general wards and paediatric hospitalised
pneumonia 52144 bacterial infection was an important complication of the 2009 influenza pandemic, with Streptococcus pneumonia e the most common bacteria identified. Bacterial infection appeared to be associated with morbidity and

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