Severity and properties of cardiac damage caused by  Streptococcus pneumoniae  are strain dependent

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Abstract

Streptococcus pneumoniae is an opportunistic Gram-positive pathogen that can cause invasive disease. Recent studies have shown that S. pneumoniae is able to invade the myocardium and kill cardiomyocytes, with one-in-five adults hospitalized for pneumococcal pneumonia having a pneumonia-associated adverse cardiac event. Furthermore, clinical reports have shown up to a 10-year increased risk of adverse cardiac events in patients formerly hospitalized for pneumococcal bacteremia. In this study, we investigated the ability of nine S. pneumoniae clinical isolates, representing eight unique serotypes, to cause cardiac damage in a mouse model of invasive disease. Following intraperitoneal challenge of C57BL/6 mice, four of these strains (D39, WU2, TIGR4, and 6A-10) caused high-grade bacteremia, while CDC7F:2617–97 and AMQ16 caused mid- and low-grade bacteremia, respectively. Three strains did not cause any discernible disease. Of note, only the strains capable of high-grade bacteremia caused cardiac damage, as inferred by serum levels of cardiac troponin-I. This link between bacteremia and heart damage was further corroborated by Hematoxylin & Eosin and Trichrome staining which showed cardiac cytotoxicity only in D39, WU2, TIGR4, and 6A-10 infected mice. Finally, hearts infected with these strains showed varying histopathological characteristics, such as differential lesion formation and myocytolysis, suggesting that the mechanism of heart damage varied between strains.

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Most cited references 30

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Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6.

Joel A Lanie, Wai-Leung Ng, Krystyna Kazmierczak … (2007)

Streptococcus pneumoniae (pneumococcus) is a leading human respiratory pathogen that causes a variety of serious mucosal and invasive diseases. D39 is an historically important serotype 2 strain that was used in experiments by Avery and coworkers to demonstrate that DNA is the genetic material. Although isolated nearly a century ago, D39 remains extremely virulent in murine infection models and is perhaps the strain used most frequently in current studies of pneumococcal pathogenesis. To date, the complete genome sequences have been reported for only two S. pneumoniae strains: TIGR4, a recent serotype 4 clinical isolate, and laboratory strain R6, an avirulent, unencapsulated derivative of strain D39. We report here the genome sequences and new annotation of two different isolates of strain D39 and the corrected sequence of strain R6. Comparisons of these three related sequences allowed deduction of the likely sequence of the D39 progenitor and mutations that arose in each isolate. Despite its numerous repeated sequences and IS elements, the serotype 2 genome has remained remarkably stable during cultivation, and one of the D39 isolates contains only five relatively minor mutations compared to the deduced D39 progenitor. In contrast, laboratory strain R6 contains 71 single-base-pair changes, six deletions, and four insertions and has lost the cryptic pDP1 plasmid compared to the D39 progenitor strain. Many of these mutations are in or affect the expression of genes that play important roles in regulation, metabolism, and virulence. The nature of the mutations that arose spontaneously in these three strains, the relative global transcription patterns determined by microarray analyses, and the implications of the D39 genome sequences to studies of pneumococcal physiology and pathogenesis are presented and discussed.

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Cardiac complications in patients with community-acquired pneumonia: incidence, timing, risk factors, and association with short-term mortality.

Julio A. Chirinos, F Corrales, Gary G. Wells … (2012)

Community-acquired pneumonia (CAP) affects >5 million adults each year in the United States. Although incident cardiac complications occur in patients with community-acquired pneumonia, their incidence, timing, risk factors, and associations with short-term mortality are not well understood. A total of 1343 inpatients and 944 outpatients with community-acquired pneumonia were followed up prospectively for 30 days after presentation. Incident cardiac complications (new or worsening heart failure, new or worsening arrhythmias, or myocardial infarction) were diagnosed in 358 inpatients (26.7%) and 20 outpatients (2.1%). Although most events (89.1% in inpatients, 75% in outpatients) were diagnosed within the first week, more than half of them were recognized in the first 24 hours. Factors associated with their diagnosis included older age (odds ratio [OR]=1.03; 95% confidence interval [CI], 1.02-1.04), nursing home residence (OR, 1.8; 95% CI, 1.2-2.9), history of heart failure (OR, 4.3; 95% CI, 3.0-6.3), prior cardiac arrhythmias (OR, 1.8; 95% CI, 1.2-2.7), previously diagnosed coronary artery disease (OR, 1.5; 95% CI, 1.04-2.0), arterial hypertension (OR, 1.5; 95% CI, 1.1-2.1), respiratory rate ≥30 breaths per minute (OR, 1.6; 95% CI, 1.1-2.3), blood pH <7.35 (OR, 3.2; 95% CI, 1.8-5.7), blood urea nitrogen ≥30 mg/dL (OR, 1.5; 95% CI, 1.1-2.2), serum sodium <130 mmol/L (OR, 1.8; 95% CI, 1.02-3.1), hematocrit <30% (OR, 2.0; 95% CI, 1.3-3.2), pleural effusion on presenting chest x-ray (OR, 1.6; 95% CI, 1.1-2.4), and inpatient care (OR, 4.8; 95% CI, 2.8-8.3). Incident cardiac complications were associated with increased risk of death at 30 days after adjustment for baseline Pneumonia Severity Index score (OR, 1.6; 95% CI, 1.04-2.5). Incident cardiac complications are common in patients with community-acquired pneumonia and are associated with increased short-term mortality. Older age, nursing home residence, preexisting cardiovascular disease, and pneumonia severity are associated with their occurrence. Further studies are required to test risk stratification and prevention and treatment strategies for cardiac complications in this population.

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The association between pneumococcal pneumonia and acute cardiac events.

Oscar M Rueda, S Kaka, M Mapara … (2007)

Increased cardiac stress, hypoxemia, and inflammation may contribute to acute cardiac events, such as myocardial infarction (MI), arrhythmia, and/or congestive heart failure (CHF). We sought to determine the incidence of such events in patients who were hospitalized for community-acquired pneumococcal pneumonia. We studied the medical records of all patients who were admitted for pneumococcal pneumonia during a 5-year period (2001-2005) to identify those who had MI, atrial fibrillation or ventricular tachycardia, or new-onset or worsening CHF at the time of hospital admission. Of 170 patients, 33 (19.4%) had > or =1 of these major cardiac events. Twelve had MI, of whom 2 also had arrhythmia and 5 had new-onset or worsening CHF. Eight had new-onset atrial fibrillation or ventricular tachycardia; 6 of these also had new CHF. Thirteen had newly diagnosed or worsening CHF, without MI or new arrhythmias. Hypoxemia and anemia were prominent. Importantly, patients with concurrent pneumococcal pneumonia and cardiac events had a significantly higher mortality than those with pneumococcal pneumonia alone (P<.008). The coexistence of pulmonary and cardiac disease was often overlooked by admitting physicians who, seeking a unifying diagnosis, emphasized one diagnosis to the exclusion of the other. Patients with pneumococcal pneumonia are at substantial risk for a concurrent acute cardiac event, such as MI, serious arrhythmia, or new or worsening CHF. This concurrence significantly increases mortality due to pneumonia. Admitting physicians tend to seek a unifying diagnosis, but the frequent coexistence of pneumonia and cardiac events indicates the importance of considering multiple diagnoses.

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Author and article information

Contributors

Anukul T. Shenoy: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing

Sarah M. Beno: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing

Terry Brissac:

ORCID: http://orcid.org/0000-0002-2549-4479

Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – review & editing

Jeremiah W. Bell: Role: Data curationRole: Investigation

Lea Novak: Role: Data curationRole: Formal analysisRole: InvestigationRole: VisualizationRole: Writing – review & editing

Carlos J. Orihuela:

ORCID: http://orcid.org/0000-0002-8542-4069

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing

D. Ashley Robinson: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 14 September 2018

Publication date Collection: 2018

Volume: 13

Issue: 9

Electronic Location Identifier: e0204032

Affiliations

[1 ] Department of Microbiology, The University of Alabama at Birmingham, Birmingham, Alabama, United States of America

[2 ] Department of Pathology, The University of Alabama at Birmingham, Birmingham, Alabama, United States of America

University of Mississippi Medical Center, UNITED STATES

Author notes

Competing Interests: The authors have declared that no competing interests exist.

[¤]

Current address: Pulmonary Center–Boston University School of Medicine, Boston, Massachusetts, United States of America

* E-mail: corihuel@ 123456uab.edu

Author information

Terry Brissac http://orcid.org/0000-0002-2549-4479

Carlos J. Orihuela http://orcid.org/0000-0002-8542-4069

Article

Publisher ID: PONE-D-18-08052

DOI: 10.1371/journal.pone.0204032

PMC ID: 6138390

PubMed ID: 30216364

SO-VID: f7acc6de-672c-4dac-a1fd-21a3a5c4e03f

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 15 March 2018

Date accepted : 31 August 2018

Page count

Figures: 3, Tables: 1, Pages: 15

Funding

Funded by: funder-id http://dx.doi.org/10.13039/100000060, National Institute of Allergy and Infectious Diseases;

Award ID: R01 AI114800

Award Recipient :

ORCID: http://orcid.org/0000-0002-8542-4069

Carlos J. Orihuela

Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: 1 K12 GM 088010-09

Award Recipient : Sarah M. Beno

Funded by: American Heart Association (US)

Award ID: 16GRNT30230007

Award Recipient :

ORCID: http://orcid.org/0000-0002-8542-4069

Carlos J. Orihuela

This work was supported by National Institutes of Health ( http://grants.nih.gov/) grant AI114800 and American Heart Association ( http://research.americanheart.org) award 16GRNT30230007 awarded to CJO. SMB was supported by National Institutes of Health ( http://grants.nih.gov/) grant 1 K12 GM 088010-09. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Severity and properties of cardiac damage caused by Streptococcus pneumoniae are strain dependent

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Most cited references 30

Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6.

Cardiac complications in patients with community-acquired pneumonia: incidence, timing, risk factors, and association with short-term mortality.

The association between pneumococcal pneumonia and acute cardiac events.

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