Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections
Open accessAbstract
Context: In March 2009, a novel swine-origin influenza A/H1N1 virus was identified. After global spread, the World Health Organization in June declared the first influenza pandemic in 41 years. Objective: To describe the clinicopathologic characteristics of 34 people who died following confirmed A/H1N1 infection with emphasis on the pulmonary pathology findings. Design: We reviewed medical records, autopsy reports, microbiologic studies, and microscopic slides of 34 people who died between May 15 and July 9, 2009, and were investigated either by the New York City Office of Chief Medical Examiner (32 deaths) or through the consultation service of a coauthor (2 deaths). Results: Most of the 34 decedents (62%) were between 25 and 49 years old (median, 41.5 years). Tracheitis, bronchiolitis, and diffuse alveolar damage were noted in most cases. Influenza viral antigen was observed most commonly in the epithelium of the tracheobronchial tree but also in alveolar epithelial cells and macrophages. Most cases were reverse transcription–polymerase chain reaction positive for influenza. Histologic and microbiologic autopsy evidence of bacterial pneumonia was detected in 55% of cases. Underlying medical conditions including cardiorespiratory diseases and immunosuppression were present in 91% of cases. Obesity (body mass index, >30) was noted in 72% of adult and adolescent cases. Conclusions: The pulmonary pathologic findings in fatal disease caused by the novel pandemic influenza virus are similar to findings identified in past pandemics. Superimposed bacterial infections of the respiratory tract were common. Preexisting obesity, cardiorespiratory diseases, and other comorbidities also were prominent findings among the decedents.
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Written from the paper’s full text.
TL;DR
In 34 fatal 2009 pandemic A/H1N1 cases, pulmonary pathology showed tracheitis/bronchitis in all and diffuse alveolar damage in 25 of 34, with viral antigen mainly in tracheobronchial epithelium and macrophages. Bacterial pneumonia was found in 55%, and 91% of adult/adolescent decedents had underlying risk factors, including obesity in 72%.
Key findings
- Among 34 decedents, 62% were 25 to 49 years old (median, 41.5 years); there were 2 previously healthy infants aged 2 and 4 months and 1 person older than 60 years.
- Tracheitis and bronchitis were observed in all cases; bronchiolitis in 18 of 34; diffuse alveolar damage in 25 of 34; acute pulmonary hemorrhage in 8 of 34; and thrombotic changes in 9 of 34.
- Novel A/H1N1 virus was detected antemortem or at autopsy in all 34 decedents: 28 (82%) by real-time RT-PCR on postmortem nasopharyngeal and/or tracheal swabs and 23 of 34 (68%) by RT-PCR on FFPE lung and/or tracheal tissues.
- Autopsy evidence of acute pneumonia was seen in 19 of 34 cases (56%); tissue Gram stain showed bacterial pneumonia in 18 of 33 (55%), and 29 of 32 adult decedents (91%) had underlying risk factors, with obesity (BMI ≥30) in 72% of adult and adolescent decedents.
Methods
- Retrospective case series of 34 people who died between May 15 and July 9, 2009, with confirmed novel A/H1N1 infection: 32 investigated by the New York City Office of Chief Medical Examiner and 2 seen in consultation from Washington State and Long Island, New York.
- Reviewed medical records, autopsy reports, microbiologic studies, and microscopic slides; histologic examination used hematoxylin-eosin, Gomori methenamine silver, and Brown and Hopps tissue Gram stains.
- Viral studies included real-time RT-PCR on nasopharyngeal/tracheal swabs and FFPE autopsy tissue, plus immunohistochemistry for influenza A viral antigen; CT imaging was available for 4 patients.
Limitations
- Stated in the paper: there is insufficient clinical information about the natural history of severe influenza disease to fully inform optimal prophylaxis and treatment approaches.
- Stated in the paper: bacterial detection may be limited by inadequate sampling, collection from unaffected lung portions, or prolonged illness/treatment; it is also unknown whether CT abnormalities or pulmonary pathologic changes occur in milder or self-limited infections.
- Evident from the text: this is a small, retrospective autopsy/consultation case series without a control group, drawn from deaths investigated by a medical examiner’s office and selected consultations, so findings may not generalize to all A/H1N1 infections.
Model-written summary. Check it against the paper before relying on it.
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Claims the paper makes
0 of 24 cited sources checked · 0 supported · 0 flagged
- Findingown data
Among the 25 DAD cases, 7 showed acute and organizing DAD (average time in hospital, 11.7 days).
“Seven of 25 cases showed acute and organizing DAD (average time in hospital, 11.7 days).”
Quote in the paperNot a substantial claim - Findingown data
Influenza viral pneumonia with focal to extensive diffuse alveolar damage (DAD) was seen in 25 of 34 cases.
“Influenza viral pneumonia with focal to extensive diffuse alveolar damage (DAD) was seen in 25 of 34 cases (Figure 1, I), often associated with marked hyaline membrane formation, pulmonary edema, and, in 8 of 34 cases, acute pulmonary hemorrhage.”
Quote in the paperSubstantial claim - Findingown data
Real-time RT-PCR on FFPE lung and/or tracheal tissues detected novel A/H1N1 virus in 23 of 34 cases (68%).
“and by real-time reverse-transcription polymerase chain reaction on FFPE lung and/or tracheal tissues in 23 of 34 cases (68%; Table 2).”
Quote in the paperNot a substantial claim - Findingown data
Thrombotic changes similar to those observed in 1918 were seen in 9 of 34 cases.
“Thrombotic changes similar to changes observed in 191820 were seen in 9 of 34 cases.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [20] LeCount ER Disseminated necrosis of the pulmonary capillaries in influenzal pneumonia JAMA 1919 72 21 1519 1520
Not checked in the free run.
- Findingown data
Real-time RT-PCR on postmortem nasopharyngeal and/or tracheal swab samples detected novel A/H1N1 virus in 28 of 34 cases (82%).
“including by real-time reverse transcription–polymerase chain reaction on postmortem nasopharyngeal and/or tracheal swab samples in 28 (82%)”
Quote in the paperNot a substantial claim
- Findingown data
Autopsy evidence of acute pneumonias was observed in 19 of 34 cases, usually in association with bacteria.
“Autopsy evidence of acute pneumonias, ranging from focal to extensive in distribution, were observed in 19 of 34 cases (Figure 1, F), usually in association with bacteria (Figure 1, G; see Autopsy evidence of acute bacterial pneumonia and detection of bacteria).”
Quote in the paperNot a substantial claim - Findingown data
Novel A/H1N1 virus was detected antemortem or at autopsy in all 34 decedents.
“Novel A/H1N1 virus was detected antemortem or at autopsy in all 34 decedents, including by real-time reverse transcription–polymerase chain reaction on postmortem nasopharyngeal and/or tracheal swab samples in 28 (82%) and by real-time reverse-transcription polymerase chain reaction on FFPE lung and/or tracheal tissues in 23 of 34 cases (68%; Table 2).”
Quote in the paperSubstantial claim - Findingown data
Most of the 34 decedents were between 25 and 49 years old (62%; median, 41.5 years).
“Most of the 34 decedents (62%) were between 25 and 49 years old (median, 41.5 years).”
Quote in the paperNot a substantial claim - Findingown data
Among the 25 DAD cases, 16 showed only acute DAD (average time in hospital, 3.4 days).
“Sixteen of these 25 DAD cases showed only acute DAD (average time in hospital, 3.4 days).”
Quote in the paperNot a substantial claim - Findingown data
Among the 25 DAD cases, 2 had fibrosing and organizing DAD (average time in hospital, 31.5 days).
“Two of 25 cases had fibrosing and organizing DAD (average time in hospital, 31.5 days).”
Quote in the paperNot a substantial claim - Findingown data
Focal mild to moderate bronchiolitis was observed in 18 of 34 cases.
“Focal mild to moderate bronchiolitis (Figure 1, J) was observed in 18 of 34 cases, sometimes associated with squamous metaplasia.”
Quote in the paperNot a substantial claim - Findingown data
Immunohistochemistry for influenza viral antigen revealed prominent staining in the pseudostratified columnar epithelium of the tracheobronchial tree and its associated submucosal glands.
“Immunohistochemistry for influenza viral antigen revealed prominent staining in the pseudostratified columnar epithelium of the tracheobronchial tree (Figure 1, B and H) and its associated submucosal glands (Figure 1, D and E).”
Quote in the paperNot a substantial claim - Findingown data
H1N1 RNA was subsequently detected by RT-PCR from FFPE lung in the sixth decedent.
“H1N1 RNA was subsequently detected by real-time reverse transcription-polymerase chain reaction from FFPE lung in the sixth decedent.”
Quote in the paperNot a substantial claim - Findingown data
Of the 13 decedents who died without having been hospitalized, 8 (62%) had evidence of bacterial pneumonia.
“Of the 13 decedents who died without having been hospitalized, 8 (62%) had evidence of bacterial pneumonia (Table 2), suggesting that community acquired bacterial pneumonia may play a significant role in the current pandemic.”
Quote in the paperSubstantial claim - Findingown data
Overall, 29 of 32 adult decedents (91%) had underlying risk factors.
“Overall, 29 of 32 adult decedents (91%) had underlying risk factors (Table 2 and Table 4).”
Quote in the paperNot a substantial claim - Findingown data
One CT case also showed areas of denser consolidation obscuring underlying parenchymal architecture and bronchovascular margins, consistent with a secondary bacterial pneumonia identified at autopsy.
“One case (Figure 2, D) also showed areas of denser consolidation obscuring underlying parenchymal architecture and bronchovascular margins, consistent with a secondary bacterial pneumonia identified at autopsy.”
Quote in the paperNot a substantial claim - Findingown data
Of the 20 New York City deaths following hospital admission, 12 presented in advanced respiratory distress requiring mechanical ventilation on admission.
“Twelve of these 20 patients presented in advanced respiratory distress requiring mechanical ventilation on admission.”
Quote in the paperNot a substantial claim - Findingown data
Gastrointestinal symptoms were described in the medical records of 11 of 28 decedents.
“Gastrointestinal symptoms, including nausea, vomiting, diarrhea, and/or abdominal pain, were described in the medical records of 11 of 28 decedents.”
Quote in the paperNot a substantial claim - Findingown data
The remaining 3 bacterial-positive cases had acute and organizing DAD with chronic inflammatory cells and bronchiolitis.
“The remaining 3 had acute and organizing DAD with chronic inflammatory cells and bronchiolitis.”
Quote in the paperNot a substantial claim - Findingown data
Of the 13 decedents who died without hospitalization, 8 also had DAD.
“In addition, 8 of these 13 decedents also had DAD, confirming that these changes are not just secondary to prolonged mechanical respirator support but a component of the viral disease process as described in the 1918 and 1957 pandemics.”
Quote in the paperSubstantial claim - Findingcitation
Seventy-two percent of the adult and adolescent decedents were obese (BMI ≥30).
“Seventy-two percent of the adult and adolescent decedents were obese (body mass index [BMI] ≥30)26 (Table 4).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [26] Yanovski SZ Yanovski JA Obesity N Engl J Med 2002 346 8 591 602 11856799
Not checked in the free run.
- Findingown data
Viral antigen was often detected both in the cytoplasm and in the nuclei of alveolar macrophages.
“Viral antigen was often detected both in the cytoplasm and in the nuclei of alveolar macrophages, suggesting viral replication in macrophages.”
Quote in the paperNot a substantial claim - Findingown data
Superimposed bacterial infections of the respiratory tract were common in fatal 2009 pandemic influenza.
“Superimposed bacterial infections of the respiratory tract were common.”
Quote in the paperSubstantial claim- Rests on an assumption: The 34 investigated deaths are representative of fatal 2009 pandemic influenza A/H1N1 infections.
- Rests on an assumption: Autopsy histologic and microbiologic findings accurately reflect the pulmonary disease process that caused death.
- Findingown data
One of the 2 infant deaths also had bacterial pneumonia.
“One of the 2 infant deaths (case 3) also had bacterial pneumonia.”
Quote in the paperNot a substantial claim - Findingown data
Focal viral antigen positivity in bronchiolar epithelium was seen.
“Focal viral antigen positivity in bronchiolar epithelium was seen (Figure 1, J).”
Quote in the paperNot a substantial claim - Findingown data
Most bacterial-positive cases (15 of 18; 83%) also had histologic evidence of acute pneumonia.
“Most of these bacterial-positive cases (15 of 18; 83%) also had histologic evidence of acute pneumonia, consistent with the high percentage of secondary bacterial pneumonia described in fatal cases from earlier pandemics.”
Quote in the paperNot a substantial claim - Findingown data
On CT, the lungs of all 4 patients displayed patchy ground-glass opacities in a predominantly peripheral and peribronchial distribution, consistent with DAD.
“On CT, the lungs of all 4 patients displayed patchy ground-glass opacities, in which underlying parenchymal architecture remained visible with discernible bronchovascular margins in a predominantly peripheral and peribronchial distribution, consistent with DAD.”
Quote in the paperNot a substantial claim - Findingown data
Among the 11 adults who were dead on arrival, the median BMI was 47 (range, 25-62).
“Among the 11 adults who were dead on arrival (and therefore received no fluid resuscitation), the median BMI was 47 (range, 25–62).”
Quote in the paperNot a substantial claim - Findingown data
Viral antigen was seen commonly in alveolar macrophages but less frequently in alveolar type I and type II cells.
“Viral antigen was seen commonly in alveolar macrophages but was seen less frequently in alveolar type I and type II cells (Figure 1, K through M).”
Quote in the paperNot a substantial claim - Findingown data
CT imaging provided detailed information on antemortem pathologic changes in the lungs of 4 patients in this case series.
“A potentially important diagnostic modality in the new influenza pandemic is CT imaging, which provided detailed information on antemortem pathologic changes in the lungs of 4 patients in this case series.”
Quote in the paperSubstantial claim - Findingown data
Nearly half of the patients in this case series had a BMI greater than 40.
“Nearly half of the patients in this case series had a BMI greater than 40.”
Quote in the paperSubstantial claim - Interpretationcitation
The pulmonary pathologic abnormalities observed in the 2009 fatalities do not differ significantly from those reported by pathologists during the 1918 and 1957 pandemics.
“The pulmonary pathologic abnormalities observed in the 2009 fatalities reported here do not differ significantly from those reported by pathologists who performed meticulous autopsies during the 1918 and 1957 pandemics (reviewed in references 23 and 25).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [23] Mulder J Hers JFP Influenza 1972 Groningen, the Netherlands Wolters-Noordhoff Publishing 287
Not checked in the free run.
- cites [25] Taubenberger JK Morens DM The pathology of influenza virus infections Annu Rev Pathol 2008 3 499 522 18039138 PMC2504709
Not checked in the free run.
- Rests on an assumption: The 34 investigated deaths are representative of fatal 2009 pandemic influenza A/H1N1 infections.
- Rests on an assumption: Autopsy histologic and microbiologic findings accurately reflect the pulmonary disease process that caused death.
- Interpretationown data
The DAD changes in these decedents are not just secondary to prolonged mechanical respirator support but a component of the viral disease process as described in the 1918 and 1957 pandemics.
“In addition, 8 of these 13 decedents also had DAD, confirming that these changes are not just secondary to prolonged mechanical respirator support but a component of the viral disease process as described in the 1918 and 1957 pandemics.”
Quote in the paperSubstantial claim - Interpretationreasoning
The presence of viral antigen in both the cytoplasm and nuclei of alveolar macrophages suggests viral replication in macrophages.
“Viral antigen was often detected both in the cytoplasm and in the nuclei of alveolar macrophages, suggesting viral replication in macrophages.”
Quote in the paperNot a substantial claim - Interpretationcitation
The pulmonary pathologic findings in fatal disease caused by the novel pandemic influenza virus are similar to findings identified in past pandemics.
“The pulmonary pathologic findings in fatal disease caused by the novel pandemic influenza virus are similar to findings identified in past pandemics.”
- Also stated in: § COMMENT · boosted
“These pathologic findings are strikingly similar to those of published autopsy studies from the 1918 and 1957 pandemics and to a more limited extent from publications investigating seasonal influenza.23,25,27,28”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [23] Mulder J Hers JFP Influenza 1972 Groningen, the Netherlands Wolters-Noordhoff Publishing 287
Not checked in the free run.
- cites [25] Taubenberger JK Morens DM The pathology of influenza virus infections Annu Rev Pathol 2008 3 499 522 18039138 PMC2504709
Not checked in the free run.
- cites [27] Guarner J Paddock CD Shieh WJ Histopathologic and immunohistochemical features of fatal influenza virus infection in children during the 2003–2004 season Clin Infect Dis 2006 43 2 132 140 16779738
Not checked in the free run.
- Rests on an assumption: The 34 investigated deaths are representative of fatal 2009 pandemic influenza A/H1N1 infections.
- Rests on an assumption: Autopsy histologic and microbiologic findings accurately reflect the pulmonary disease process that caused death.
- Also stated in: § COMMENT · boosted
- Interpretationcitation
Severe disease is associated with the development of influenza viral pneumonia, with or without secondary bacterial pneumonia.
“The findings in this and other studies24 suggest that severe disease is associated with the development of influenza viral pneumonia,23,25,30 with or without secondary bacterial pneumonia.24,31,32”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [24] Morens DM Taubenberger JK Fauci AS Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness J Infect Dis 2008 198 7 962 970 18710327 PMC2599911
Not checked in the free run.
- cites [23] Mulder J Hers JFP Influenza 1972 Groningen, the Netherlands Wolters-Noordhoff Publishing 287
Not checked in the free run.
- cites [25] Taubenberger JK Morens DM The pathology of influenza virus infections Annu Rev Pathol 2008 3 499 522 18039138 PMC2504709
Not checked in the free run.
- Interpretationcitation
The observation that viral antigen in alveolar cells often did not colocalize with foci of DAD and alveolar hyaline membrane formation likely reflects the rapid asynchronous kinetics of influenza viral replication and clearance.
“Our observation that viral antigen in alveolar cells often did not colocalize with foci of DAD and alveolar hyaline membrane formation likely reflects the rapid asynchronous kinetics of influenza viral replication and clearance.25”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [25] Taubenberger JK Morens DM The pathology of influenza virus infections Annu Rev Pathol 2008 3 499 522 18039138 PMC2504709
Not checked in the free run.
- Interpretationown data
Community-acquired bacterial pneumonia may play a significant role in the current pandemic.
“Of the 13 decedents who died without having been hospitalized, 8 (62%) had evidence of bacterial pneumonia (Table 2), suggesting that community acquired bacterial pneumonia may play a significant role in the current pandemic.”
Quote in the paperSubstantial claim - Interpretationown data
Even in an era of widespread and early antibiotic use, bacterial pneumonia remains an important factor in severe/fatal influenza.
“Regardless, these findings suggest that, even in an era of widespread and early antibiotic use, bacterial pneumonia remains an important factor in severe/fatal influenza.”
Quote in the paperSubstantial claim- Rests on an assumption: The 34 investigated deaths are representative of fatal 2009 pandemic influenza A/H1N1 infections.
- Rests on an assumption: Autopsy histologic and microbiologic findings accurately reflect the pulmonary disease process that caused death.
- Premisecitation
In a subset of fatal cases for which medical records were available, 91% had preexisting underlying medical conditions, notably cardiac and respiratory diseases, immunosuppression, pregnancy, and obesity.
“In a subset of fatal cases for which medical records were available, 91% had preexisting underlying medical conditions, notably cardiac and respiratory diseases, immunosuppression, pregnancy, and obesity, the latter being an unexpected finding based on evidence from prior pandemics.13”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [13] Vaillant L La Ruche G Tarantola A Barboza P Epidemiology of fatal cases associated with pandemic H1N1 influenza 2009 Euro Surveill 2009 14 33 1 6 19712643
Not checked in the free run.
- Premisecitation
The 2009 pandemic has predominantly affected the young, with a median age between 12 and 22 years.
“Whereas in seasonal influenza most deaths occur in persons older than 65 years,9 the 2009 pandemic has predominantly affected the young, with a median age between 12 and 22 years.10–12”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [10] Centers for Disease Control and Prevention 2009 pandemic influenza A (H1N1) virus infections—Chicago, Illinois, April–July 2009 MMWR Morb Mortal Wkly Rep 2009 58 33 913 918 19713879
Not checked in the free run.
- cites [11] Kelly HA Grant KA Williams S Fielding J Smith D Epidemiological characteristics of pandemic influenza H1N1 2009 and seasonal influenza infection Med J Aust 2009 191 3 146 149 19645642
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- cites [12] Baker MG Wilson N Huang QS Pandemic influenza A(H1N1)v in New Zealand: the experience from April to August 2009 Euro Surveill 2009 14 34 1 6 19712648
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- Premisecitation
A recent CDC report described concurrent bacterial infection in 29% of referral specimens from influenza A/H1N1 fatalities.
“A recent report by the Centers for Disease Control and Prevention described concurrent bacterial infection in 29% of referral specimens from influenza A/H1N1 fatalities.21”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [21] Centers for Disease Control and Prevention Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1)—United States, May–August 2009 MMWR Morb Mortal Wkly Rep 2009 58 1 4 19798021
Not checked in the free run.
- Interpretationcitation
Enhanced susceptibility to fatal infection in obese persons might reflect associated independent risk factors such as compromised ventilatory function, hypertension, congestive heart failure, or diabetes mellitus.
“Enhanced susceptibility to fatal infection in obese persons might reflect associated independent risk factors such as compromised ventilatory function, hypertension, congestive heart failure, or diabetes mellitus.36”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [36] Haque AK Gadre S Taylor J Haque SA Freeman D Duarte A Pulmonary and cardiovascular complications of obesity: an autopsy study of 76 obese subjects Arch Pathol Lab Med 2008 132 9 1397 1404 18788850
Not checked in the free run.
- Interpretationown data
This case series emphasizes an association between underlying illnesses and mortality.
“In addition to demonstrating the characteristics and constancy of pulmonary abnormalities in fatal pandemic influenza, this case series emphasizes an association between underlying illnesses and mortality.”
Quote in the paperSubstantial claim- Rests on an assumption: The 34 investigated deaths are representative of fatal 2009 pandemic influenza A/H1N1 infections.
- Rests on an assumption: Autopsy histologic and microbiologic findings accurately reflect the pulmonary disease process that caused death.
- May combine two claims. 11
- The quote only partly states this claim. 2
- Classified as probably not a substantial claim. 4
May combine two claims.
Findingown dataThe longest interval in which viral RNA was detected after the onset of respiratory symptoms was 12 days for postmortem nasopharyngeal samples and 38 days for FFPE material.
“The longest interval in which viral RNA was detected after the onset of respiratory symptoms was 12 days for postmortem nasopharyngeal samples and 38 days for FFPE material.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe 6 decedents in whom viral RNA was not detected in nasopharyngeal samples had intervals between 17 and 44 days; all had received oseltamivir while hospitalized, and 5 of 6 had antemortem detection of H1N1 viral RNA.
“The 6 decedents in which viral RNA was not detected in nasopharyngeal samples had intervals between 17 and 44 days; all had received oseltamivir phosphate (Tamiflu) while hospitalized, and 5 of the 6 had antemortem detection of H1N1 viral RNA.”
Quote in the paperNot a substantial claimThe quote only partly states this claim.
Findingown dataTracheitis and bronchitis of focal or extensive nature were observed in all 34 cases.
“Tracheitis and bronchitis of focal or extensive nature were observed in all cases”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataAutopsy evidence of acute pneumonia was seen in 19 of 34 cases (56%) and was necrotizing/extensive in 5 cases (15%).
“Autopsy evidence of acute pneumonia was seen in 19 of 34 cases (56%) and was necrotizing/extensive in 5 cases (15%).”
Quote in the paperSubstantial claimMay combine two claims. The quote only partly states this claim.
Findingown dataObesity, heart disease, and underlying pulmonary disease were the most common causes of death, risk factors, and comorbidities.
“Obesity, heart disease, and underlying pulmonary disease were most common.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataPreexisting obesity, cardiorespiratory diseases, and other comorbidities were prominent findings among the decedents.
“Preexisting obesity, cardiorespiratory diseases, and other comorbidities also were prominent findings among the decedents.”
Quote in the paperSubstantial claim- Rests on an assumption: The 34 investigated deaths are representative of fatal 2009 pandemic influenza A/H1N1 infections.
- Rests on an assumption: Autopsy histologic and microbiologic findings accurately reflect the pulmonary disease process that caused death.
Probably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataAntigen-positive alveolar macrophages containing visible cytoplasmic bacteria were observed.
“Antigen-positive alveolar macrophages containing visible cytoplasmic bacteria were also observed (Figure 1, K).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataOf 33 cases examined by tissue Gram stain, 18 (55%) showed bacterial pneumonia, 16 morphologically compatible with streptococci and 2 with staphylococci.
“Thirty-three of 34 cases were examined for evidence of pulmonary bacterial infection by tissue Gram stain. Of these, 18 (55%) showed bacterial pneumonia, 16 being morphologically compatible with streptococci and 2 with staphylococci.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataNine decedents had pulmonary thrombi including 5 with focal infarcts.
“Nine decedents had pulmonary thrombi including 5 with focal infarcts.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataOf 30 cases evaluated by postmortem bacteriologic culture and immunohistochemistry, 10 had evidence of bacterial infection: 6 with Streptococcus pneumoniae, 2 with Streptococcus pyogenes, 1 with S pneumoniae and S pyogenes, and 1 with methicillin-resistant Staphylococcus aureus.
“Of the 30 cases evaluated by postmortem bacteriologic culture and immunohistochemistry, 10 (4 of whom had been hospitalized before death) had evidence of bacterial infection: 6 with Streptococcus pneumoniae, 2 with Streptococcus pyogenes, 1 with S pneumoniae and S pyogenes, and 1 with methicillin-resistant Staphylococcus aureus (Table 2 and Table 3).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [21] Centers for Disease Control and Prevention Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1)—United States, May–August 2009 MMWR Morb Mortal Wkly Rep 2009 58 1 4 19798021
Not checked in the free run.
- cites [22] Guarner J Packard MM Nolte KB Usefulness of immunohistochemical diagnosis of streptococcus pneumoniae in formalin-fixed, paraffin-embedded specimens compared with culture and gram stain techniques Am J Clin Pathol 2007 127 4 612 618 17369138
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationInfluenza viral antigen in the tracheobronchial epithelium, alveolar lining cells, and alveolar macrophages was first demonstrated by immunofluorescence in 1957 pandemic autopsy cases.
“For example, influenza viral antigen in the tracheobronchial epithelium, alveolar lining cells, and alveolar macrophages, as shown here by immunohistochemistry (Figure 1), was first demonstrated by immunofluorescence in 1957 pandemic autopsy cases.23”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [23] Mulder J Hers JFP Influenza 1972 Groningen, the Netherlands Wolters-Noordhoff Publishing 287
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe 2009 pandemic H1N1 virus was a novel genetic reassortant derived from 2 preexisting swine influenza virus lineages.
“The virus was a novel genetic reassortant derived from 2 preexisting swine influenza virus lineages. 6”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [6] Garten RJ Davis CT Russell CA Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans Science 2009 325 5937 197 201 19465683 PMC3250984
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationThrombi are common with DAD and have been described with influenza infection since 1918.
“Thrombi are common with DAD and have been described with influenza infection since 1918.20,35”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [20] LeCount ER Disseminated necrosis of the pulmonary capillaries in influenzal pneumonia JAMA 1919 72 21 1519 1520
Not checked in the free run.
- cites [35] Centers for Disease Control and Prevention Intensive-care patients with severe novel influenza A (H1N1) virus infection—Michigan, June 2009 MMWR Morb Mortal Wkly Rep 2009 58 27 749 752 19609249
Not checked in the free run.
May combine two claims.
Interpretationown dataCT can be a valuable tool in identifying patients who will require intensive medical support and to elucidate the pathogenesis of severe disease.
“Our findings suggest that CT can be a valuable tool in identifying patients who will require intensive medical support and to elucidate the pathogenesis of severe disease.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationcitationThe presence of only a single decedent older than 60 years is consistent with current reports that older individuals are less vulnerable to infection with the 2009 A/H1N1 virus than with seasonal influenza viruses, presumably because of immunologic protection induced by prior exposure to previously circulating human A/H1N1 viruses.
“The presence of only a single decedent older than 60 years is also consistent with current reports that older individuals are less vulnerable to infection with the 2009 A/H1N1 virus than with seasonal influenza viruses, presumably because of immunologic protection induced by prior exposure to previously circulating human A/H1N1 viruses.37”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [37] Centers for Disease Control and Prevention Serum cross-reactive antibody response to a novel influenza A (H1N1) virus after vaccination with seasonal influenza vaccine MMWR Morb Mortal Wkly Rep 2009 58 19 521 524 19478718
Not checked in the free run.
The paper relies on this without support.
The 34 investigated deaths are representative of fatal 2009 pandemic influenza A/H1N1 infections.
“We investigated 34 deaths with confirmed novel A/H1N1 respiratory infection, reviewing available clinical, radiologic, pathologic, and microbiologic data.”
The paper relies on this without support.
Autopsy histologic and microbiologic findings accurately reflect the pulmonary disease process that caused death.
“The decision by the New York City Office of Chief Medical Examiner to investigate deaths associated with infection by the 2009 pandemic influenza virus provides an opportunity to examine the pathogenesis of fatal pandemic influenza.”
Claims other papers make about this one
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Evidence from seasonal influenza epidemics, past pandemics, pathology studies and animal models shows influenza predisposes to bacterial co-infection.
“Evidence of influenza predisposing to bacterial co-infection is seen in seasonal influenza epidemics, past pandemics, pathology studies and animal models [1–8].”
From The role of pneumonia and secondary bacterial infection in fatal and serious outcomes of pandemic influenza a(H1N1)pdm09. (2018) · cites this paper as [2]
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Garten, R. J., Davis, C. T., Russell, C. A., Shu, B., Lindstrom, S., Balish, A. L., Sessions, W. M., Xu, X., Skepner, E., Deyde, V., et al. (2009) · Science · doi:10.1126/science.1176225 · Cited by 2,499 · see citing works
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Comparative Pathology of Select Agent Influenza A Virus Infections
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Glycan Shielding of the Influenza Virus Hemagglutinin Contributes to Immunopathology in Mice
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Effects of Influenza on Alveolar Macrophage Viability Are Dependent on Mouse Genetic Strain
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Pandemic Swine-Origin H1N1 Influenza A Virus Isolates Show Heterogeneous Virulence in Macaques
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Invasive Aspergillosis as an Under-recognized Superinfection in COVID-19
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PPAR-γ Activation As an Anti-inflammatory Therapy for Respiratory Virus Infections
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A Centenary Tale of Two Pandemics: The 1918 Influenza Pandemic and COVID-19, Part I
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Self-citationPoly I:C Enhances Susceptibility to Secondary Pulmonary Infections by Gram-Positive Bacteria
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- Authors
- Gill, J. R., Sheng, Z.-M., Ely, S. F., Guinee, D. G., Beasley, M. B., Suh, J., Deshpande, C., Mollura, D. J., Morens, D. M., Bray, M., Travis, W. D., & Taubenberger, J. K.
- Affiliations
- Office of Chief Medical Examiner (US)
- National Institutes of Health (US)
- ORCID
- Venue
- Archives of Pathology & Laboratory Medicine
- Published
- 2010-02
- Volume
- 134
- Issue
- 2
- Pages
- 235-243
- ISSN
- 0003-9985 (ISSN-L)
- 1543-2165
- PMC
- PMC2819217
- OpenAlex
- W1852307476
- Cited by
- 426
- References
- 39
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 12 · 2023: 16 · 2022: 16 · 2021: 38 · 2020: 23 · 2019: 22 · 2018: 19 · 2017: 10 · 2016: 13 · 2015: 22 · 2014: 21 · 2013: 31 · 2012: 57
- FWCI
- 46.91
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Archives of Pathology & Laboratory Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (ZIAAI000986)
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
- Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
- Keywords
- 2009 H1N1 pandemic, H1N1 influenza, fatal influenza, lung pathology, secondary bacterial infection, bacterial pneumonia, tracheitis, bronchiolitis, diffuse alveolar damage, obesity, comorbidities, cardiopulmonary disease, immunosuppression, autopsy findings
- MeSH terms
- Adolescent, Adult, Aged, Child, Child, Preschool, Disease Outbreaks, Female, Humans, Infant, Infant, Newborn, Influenza, Human, Lung, Male, Middle Aged, Radiography, Time Factors, Comorbidity, Pneumonia, Bacterial, Influenza A Virus, H1N1 Subtype
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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