The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index; none of the 24 sources its claims cite is checked for support yet.
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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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.
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38 Own result · 15 Not checked yet · 6 Own interpretation
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In the paper
“Seven of 25 cases showed acute and organizing DAD (average time in hospital, 11.7 days).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Pulmonary Pathologic Findings
plainn = 25- Asserted: passes — The authors put it forward as true.
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In the paper
“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.”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Pulmonary Pathologic Findings
plainn = 34- Asserted: passes — The authors put it forward as true.
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In the paper
“and by real-time reverse-transcription polymerase chain reaction on FFPE lung and/or tracheal tissues in 23 of 34 cases (68%; Table 2).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Influenza Viral Detection
plainn = 34- Asserted: passes — The authors put it forward as true.
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In the paper
“Thrombotic changes similar to changes observed in 191820 were seen in 9 of 34 cases.”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Pulmonary Pathologic Findings
What the sources say
- Not checked yetcites [20] LeCount ER Disseminated necrosis of the pulmonary capillaries in influenzal pneumonia JAMA 1919 72 21 1519 1520
plainn = 34- Asserted: passes — The authors put it forward as true.
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In the paper
“including by real-time reverse transcription–polymerase chain reaction on postmortem nasopharyngeal and/or tracheal swab samples in 28 (82%)”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Influenza Viral Detection
plainn = 34- Asserted: passes — The authors put it forward as true.
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In the paper
“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).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Pulmonary Pathologic Findings
plaincorrelationaln = 34- Asserted: passes — The authors put it forward as true.
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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Influenza Viral Detection
plainn = 34- Asserted: passes — The authors put it forward as true.
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In the paper
“Most of the 34 decedents (62%) were between 25 and 49 years old (median, 41.5 years).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > Abstract > Results
plainn = 34- Asserted: passes — The authors put it forward as true.
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In the paper
“Sixteen of these 25 DAD cases showed only acute DAD (average time in hospital, 3.4 days).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Pulmonary Pathologic Findings
plainn = 25- Asserted: passes — The authors put it forward as true.
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In the paper
“Two of 25 cases had fibrosing and organizing DAD (average time in hospital, 31.5 days).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Pulmonary Pathologic Findings
plainn = 25- Asserted: passes — The authors put it forward as true.
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In the paper
“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.”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Influenza Viral Detection
plainn = 34- Asserted: passes — The authors put it forward as true.
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In the paper
“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.”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Influenza Viral Detection
plainn = 6- Asserted: passes — The authors put it forward as true.
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In the paper
“Tracheitis and bronchitis of focal or extensive nature were observed in all cases”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Pulmonary Pathologic Findings
plainn = 34- Asserted: passes — The authors put it forward as true.
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In the paper
“Autopsy evidence of acute pneumonia was seen in 19 of 34 cases (56%) and was necrotizing/extensive in 5 cases (15%).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Autopsy Evidence of Acute Bacterial Pneumonia and Detection of Bacteria
plainn = 34- Asserted: passes — The authors put it forward as true.
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In the paper
“Obesity, heart disease, and underlying pulmonary disease were most common.”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Risk Factors and Comorbidities
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Preexisting obesity, cardiorespiratory diseases, and other comorbidities also were prominent findings among the decedents.”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > Abstract > Conclusions
plain- Asserted: passes — The authors put it forward as true.
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- 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.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Antigen-positive alveolar macrophages containing visible cytoplasmic bacteria were also observed (Figure 1, K).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Influenza Viral Detection
plain- Asserted: passes — The authors put it forward as true.
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In the paper
“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.”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Autopsy Evidence of Acute Bacterial Pneumonia and Detection of Bacteria
plainn = 33- Asserted: passes — The authors put it forward as true.
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In the paper
“Nine decedents had pulmonary thrombi including 5 with focal infarcts.”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > COMMENT
plainn = 9- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“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).”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > RESULTS > Autopsy Evidence of Acute Bacterial Pneumonia and Detection of Bacteria
What the sources say
- Not checked yetcites [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 yetcites [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
plainn = 30- Asserted: passes — The authors put it forward as true.
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In the paper
“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”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > COMMENT
What the sources say
- Not checked yetcites [23] Mulder J Hers JFP Influenza 1972 Groningen, the Netherlands Wolters-Noordhoff Publishing 287
plain- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“The virus was a novel genetic reassortant derived from 2 preexisting swine influenza virus lineages. 6”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > Abstract > Conclusions
What the sources say
- Not checked yetcites [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
plaindirect- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Thrombi are common with DAD and have been described with influenza infection since 1918.20,35”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > COMMENT
What the sources say
- Not checked yetcites [20] LeCount ER Disseminated necrosis of the pulmonary capillaries in influenzal pneumonia JAMA 1919 72 21 1519 1520
- Not checked yetcites [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
plaincorrelational- Asserted: passes — The authors put it forward as true.
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Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > COMMENT
hedgedcorrelationaln = 4- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
In the paper
“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”
§ Pulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections > COMMENT
What the sources say
- Not checked yetcites [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
hedgedconditionalSingle case- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
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.”
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“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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Metadata
- 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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