Elevated Carbon Monoxide in the Exhaled Breath of Mice during a Systemic Bacterial Infection
Publication Date
July 31, 2013
Journal
PLOS ONE
Authors
Alan G. Barbour, Charlotte M. Hirsch, Arash Ghalyanchi Langeroudi, Simone Meinardi, et al
Volume
8
Issue
7
Pages
e69802
DOI
https://dx.plos.org/10.1371/journal.pone.0069802
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0069802
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23936104
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3729689
Europe PMC
http://europepmc.org/abstract/MED/23936104
Web of Science
000322633700044
Scopus
84881120437
Mendeley
http://www.mendeley.com/research/elevated-carbon-monoxide-exhaled-breath-mice-during-systemic-bacterial-infection
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Mendeley | Further Information

{"title"=>"Elevated Carbon Monoxide in the Exhaled Breath of Mice during a Systemic Bacterial Infection", "type"=>"journal", "authors"=>[{"first_name"=>"Alan G.", "last_name"=>"Barbour", "scopus_author_id"=>"7103410979"}, {"first_name"=>"Charlotte M.", "last_name"=>"Hirsch", "scopus_author_id"=>"55813510400"}, {"first_name"=>"Arash", "last_name"=>"Ghalyanchi Langeroudi", "scopus_author_id"=>"54994186700"}, {"first_name"=>"Simone", "last_name"=>"Meinardi", "scopus_author_id"=>"6603775815"}, {"first_name"=>"Eric R.G.", "last_name"=>"Lewis", "scopus_author_id"=>"55812996900"}, {"first_name"=>"Azadeh Shojaee", "last_name"=>"Estabragh", "scopus_author_id"=>"56119040600"}, {"first_name"=>"Donald R.", "last_name"=>"Blake", "scopus_author_id"=>"8359591200"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"23936104", "isbn"=>"1932-6203", "doi"=>"10.1371/journal.pone.0069802", "issn"=>"19326203", "scopus"=>"2-s2.0-84881120437", "pui"=>"369507639", "sgr"=>"84881120437"}, "id"=>"9cde2231-bc7f-3a72-99fb-74cf728745cb", "abstract"=>"Blood is the specimen of choice for most laboratory tests for diagnosis and disease monitoring. Sampling exhaled breath is a noninvasive alternative to phlebotomy and has the potential for real-time monitoring at the bedside. Improved instrumentation has advanced breath analysis for several gaseous compounds from humans. However, application to small animal models of diseases and physiology has been limited. To extend breath analysis to mice, we crafted a means for collecting nose-only breath samples from groups and individual animals who were awake. Samples were subjected to gas chromatography and mass spectrometry procedures developed for highly sensitive analysis of trace volatile organic compounds (VOCs) in the atmosphere. We evaluated the system with experimental systemic infections of severe combined immunodeficiency Mus musculus with the bacterium Borrelia hermsii. Infected mice developed bacterial densities of ∼10(7) per ml of blood by day 4 or 5 and in comparison to uninfected controls had hepatosplenomegaly and elevations of both inflammatory and anti-inflammatory cytokines. While 12 samples from individual infected mice on days 4 and 5 and 6 samples from uninfected mice did not significantly differ for 72 different VOCs, carbon monoxide (CO) was elevated in samples from infected mice, with a mean (95% confidence limits) effect size of 4.2 (2.8-5.6), when differences in CO2 in the breath were taken into account. Normalized CO values declined to the uninfected range after one day of treatment with the antibiotic ceftriaxone. Strongly correlated with CO in the breath were levels of heme oxygenase-1 protein in serum and HMOX1 transcripts in whole blood. These results (i) provide further evidence of the informativeness of CO concentration in the exhaled breath during systemic infection and inflammation, and (ii) encourage evaluation of this noninvasive analytic approach in other various other rodent models of infection and for utility in clinical management.", "link"=>"http://www.mendeley.com/research/elevated-carbon-monoxide-exhaled-breath-mice-during-systemic-bacterial-infection", "reader_count"=>20, "reader_count_by_academic_status"=>{"Student > Doctoral Student"=>3, "Researcher"=>7, "Student > Ph. D. Student"=>5, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>1, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_user_role"=>{"Student > Doctoral Student"=>3, "Researcher"=>7, "Student > Ph. D. Student"=>5, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>1, "Lecturer > Senior Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>5, "Medicine and Dentistry"=>4, "Philosophy"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>3, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Chemistry"=>{"Chemistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Philosophy"=>{"Philosophy"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United States"=>1, "India"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1138580"], "description"=>"<p>Selected components of the apparatus are indicated.</p>", "links"=>[], "tags"=>["microbiology", "immunity", "inflammation", "Bacterial pathogens", "Host-pathogen interaction", "Analytical chemistry", "Chemical analysis", "atmospheric chemistry", "chromatography", "Gas chromatography", "Anatomy and physiology", "Respiratory system", "Respiratory physiology", "Infectious diseases", "Bacterial diseases", "bloodstream infections", "Borrelia infection", "apparatus", "exhaled", "samples", "groups"], "article_id"=>760945, "categories"=>["Medicine", "Chemistry", "Biological Sciences"], "users"=>["Alan G. Barbour", "Charlotte M. Hirsch", "Arash Ghalyanchi Langeroudi", "Simone Meinardi", "Eric R. G. Lewis", "Azadeh Shojaee Estabragh", "Donald R. Blake"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0069802.g001", "stats"=>{"downloads"=>4, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Assembled_apparatus_for_collection_of_exhaled_breath_samples_from_groups_or_individual_mice_/760945", "title"=>"Assembled apparatus for collection of exhaled breath samples from groups or individual mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-31 02:22:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1138582"], "description"=>"<p>Samples were obtained when bacteremia reached its peak in infected mice; analyte concentrations in wt per ml were determined by immunoassay as described in text. The graphs are box-whisker plots of log<sub>10</sub>-transformed values. Each box indicates the first and third quartiles, and the line inside the box is the median. The 1.5× interquartile range is indicated by the vertical line (whiskers) bisecting the box, and values outside this range are indicated by asterisks. If the result for a biomarker was “undetected”, we report the lower limit of quantitation for that substance on the run as the concentration for that specimen. Abbreviations: IL, Interleukin; VCAM1, Vascular Cell Adhesion Molecule-1.</p>", "links"=>[], "tags"=>["microbiology", "immunity", "inflammation", "Bacterial pathogens", "Host-pathogen interaction", "Analytical chemistry", "Chemical analysis", "atmospheric chemistry", "chromatography", "Gas chromatography", "Anatomy and physiology", "Respiratory system", "Respiratory physiology", "Infectious diseases", "Bacterial diseases", "bloodstream infections", "Borrelia infection", "acute", "biomarkers", "plasma", "mice", "uninfected", "infected"], "article_id"=>760947, "categories"=>["Medicine", "Chemistry", "Biological Sciences"], "users"=>["Alan G. Barbour", "Charlotte M. Hirsch", "Arash Ghalyanchi Langeroudi", "Simone Meinardi", "Eric R. G. Lewis", "Azadeh Shojaee Estabragh", "Donald R. Blake"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0069802.g002", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Selected_acute_phase_reactants_cytokines_and_other_inflammation_biomarkers_in_the_plasma_of_BALB_c_scid_mice_that_were_uninfected_n_6_or_infected_n_12_with_Borrelia_hermsii_/760947", "title"=>"Selected acute phase reactants, cytokines, and other inflammation biomarkers in the plasma of BALB/c<i>-scid</i> mice that were uninfected (n = 6) or infected (n = 12) with <i>Borrelia hermsii</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-31 02:22:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1138583"], "description"=>"<p>Coefficients of determination (<i>R<sup>2</sup></i>) for each group are shown in the figures. Upper panel: Eight groups of 3 BALB/c-<i>scid</i> male and female mice sampled on days −4, −2, and 0 (uninfected; total of 24 determinations) and injected with <i>B. hermsii</i> on day 0 after sampling. Mice were sampled again in the same groups on days 3 and 5. The plot shows the day 5 values for 8 groups of mice (infected). The inset indicates the symbols for status of infection. The regression coefficients (95% confidence interval) for the combined data for days 4 and 5 were 57 (39–75) for uninfected mice (<i>F</i><sub>1,22</sub> = 43.2; <i>p</i><10<sup>−4</sup>) and 175 (97–253) for infected mice (<i>F</i><sub>1,6</sub> = 30.4; <i>p</i> = 0.002). Lower panel: Six groups of 3 C.B-17-<i>scid</i> male mice infected on day 0 and 5 groups of 3 uninfeceted mice sampled on days 4 and 5. The inset indicates the symbols for status of infection and day of sampling. The regression coefficients for the combined data for days 4 and 5 were 30 (10–51) for uninfected mice (<i>F</i><sub>1,10</sub> = 11.3; <i>p</i> = 0.007) and 195 (131–259) for infected mice (<i>F</i><sub>1,10</sub> = 43.2; <i>p</i><10<sup>−4</sup>).</p>", "links"=>[], "tags"=>["microbiology", "immunity", "inflammation", "Bacterial pathogens", "Host-pathogen interaction", "Analytical chemistry", "Chemical analysis", "atmospheric chemistry", "chromatography", "Gas chromatography", "Anatomy and physiology", "Respiratory system", "Respiratory physiology", "Infectious diseases", "Bacterial diseases", "bloodstream infections", "Borrelia infection", "linear", "regressions", "carbon", "monoxide", "parts", "dioxide", "samples", "mice", "infected", "uninfected", "controls"], "article_id"=>760948, "categories"=>["Medicine", "Chemistry", "Biological Sciences"], "users"=>["Alan G. Barbour", "Charlotte M. Hirsch", "Arash Ghalyanchi Langeroudi", "Simone Meinardi", "Eric R. G. Lewis", "Azadeh Shojaee Estabragh", "Donald R. Blake"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0069802.g003", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Least_squares_linear_regressions_of_carbon_monoxide_CO_in_parts_per_billion_volume_ppbv_on_total_carbon_dioxide_CO_2_in_for_samples_of_collected_breath_from_mice_infected_with_B_hermsii_and_uninfected_controls_in_two_experiments_/760948", "title"=>"Least-squares linear regressions of carbon monoxide (CO) in parts per billion volume (ppbv) on total carbon dioxide (CO<sub>2</sub>) in % for samples of collected breath from mice infected with <i>B. hermsii</i> and uninfected controls in two experiments.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-31 02:22:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1138584"], "description"=>"<p>Breathhermsii samples were collected for 3 days before infection after the sampling on day 0. Inset, CO/CO<sub>2</sub> by sex of group.</p>", "links"=>[], "tags"=>["microbiology", "immunity", "inflammation", "Bacterial pathogens", "Host-pathogen interaction", "Analytical chemistry", "Chemical analysis", "atmospheric chemistry", "chromatography", "Gas chromatography", "Anatomy and physiology", "Respiratory system", "Respiratory physiology", "Infectious diseases", "Bacterial diseases", "bloodstream infections", "Borrelia infection", "normalized", "co", "concentrations", "exhaled", "samples", "groups", "scid", "mice", "infected"], "article_id"=>760949, "categories"=>["Medicine", "Chemistry", "Biological Sciences"], "users"=>["Alan G. Barbour", "Charlotte M. Hirsch", "Arash Ghalyanchi Langeroudi", "Simone Meinardi", "Eric R. G. Lewis", "Azadeh Shojaee Estabragh", "Donald R. Blake"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0069802.g004", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Box_whisker_plots_of_normalized_CO_concentrations_CO_CO_2_in_the_exhaled_breath_samples_from_8_groups_of_3_SCID_mice_infected_with_B_by_day_of_infection_/760949", "title"=>"Box-whisker plots of normalized CO concentrations (CO/CO<sub>2</sub>) in the exhaled breath samples from 8 groups of 3 SCID mice infected with <i>B. </i> by day of infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-31 02:22:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1138585"], "description"=>"<p><i>B. hermsii</i> infection was initiated on day 0 in 12 mice. On day 4 after the breath sampling, 5 infected mice were euthanized, 2 mice remained infected until euthanasia the next day, and 5 mice began treatment with the antibiotic ceftriaxone. Two uninfected mice were euthanized after day 5′s collection, and there is missing data for 1 treated mouse on day 9. The course for each mouse is given in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069802#pone.0069802.s002\" target=\"_blank\">Figure S2</a> of SI. Inset, box-whisker plots of CO/CO<sub>2</sub> values for 6 uninfected mice, which were all sampled on days 4 and 5, and 12 untreated infected mice, 10 of which were sampled on day 4 only and 2 of which were sampled on day 5 as well.</p>", "links"=>[], "tags"=>["microbiology", "immunity", "inflammation", "Bacterial pathogens", "Host-pathogen interaction", "Analytical chemistry", "Chemical analysis", "atmospheric chemistry", "chromatography", "Gas chromatography", "Anatomy and physiology", "Respiratory system", "Respiratory physiology", "Infectious diseases", "Bacterial diseases", "bloodstream infections", "Borrelia infection", "normalized", "co", "concentrations", "exhaled", "samples", "18", "scid", "mice"], "article_id"=>760950, "categories"=>["Medicine", "Chemistry", "Biological Sciences"], "users"=>["Alan G. Barbour", "Charlotte M. Hirsch", "Arash Ghalyanchi Langeroudi", "Simone Meinardi", "Eric R. G. Lewis", "Azadeh Shojaee Estabragh", "Donald R. Blake"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0069802.g005", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Daily_normalized_CO_concentrations_CO_CO_2_in_the_exhaled_breath_samples_from_18_individual_adult_male_SCID_mice_by_state_of_infection_uninfected_infected_or_treated_on_day_of_study_/760950", "title"=>"Daily normalized CO concentrations (CO/CO<sub>2</sub>) in the exhaled breath samples from 18 individual adult male SCID mice by state of infection (uninfected, infected, or treated) on day of study.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-31 02:22:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1138586"], "description"=>"<p>The least-squares linear regression line and the coefficient of determination (<i>R<sup>2</sup></i>) are shown.</p>", "links"=>[], "tags"=>["microbiology", "immunity", "inflammation", "Bacterial pathogens", "Host-pathogen interaction", "Analytical chemistry", "Chemical analysis", "atmospheric chemistry", "chromatography", "Gas chromatography", "Anatomy and physiology", "Respiratory system", "Respiratory physiology", "Infectious diseases", "Bacterial diseases", "bloodstream infections", "Borrelia infection", "normalized", "co", "samples", "serum", "heme", "oxygenase-1", "concentrations", "treated", "scid", "mice"], "article_id"=>760951, "categories"=>["Medicine", "Chemistry", "Biological Sciences"], "users"=>["Alan G. Barbour", "Charlotte M. Hirsch", "Arash Ghalyanchi Langeroudi", "Simone Meinardi", "Eric R. G. Lewis", "Azadeh Shojaee Estabragh", "Donald R. Blake"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0069802.g006", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Scatter_plot_of_normalized_CO_CO_CO_2_in_breath_samples_on_serum_heme_oxygenase_1_concentrations_in_6_uninfected_7_infected_and_5_treated_male_SCID_mice_at_the_time_of_euthanasia_as_described_in_text_and_in_Figure_5_legend_/760951", "title"=>"Scatter plot of normalized CO (CO/CO<sub>2</sub>) in breath samples on serum heme oxygenase-1 concentrations in 6 uninfected, 7 infected, and 5 treated male SCID mice at the time of euthanasia, as described in text and in Figure 5 legend.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-07-31 02:22:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1138587"], "description"=>"a<p>The number of days for each mouse were from day −3 until euthanasia (see text).</p>b<p><i>p</i> values by <i>t</i> test/Mann Whitney rank sum.</p>c<p>-, not applicable.</p>", "links"=>[], "tags"=>["microbiology", "immunity", "inflammation", "Bacterial pathogens", "Host-pathogen interaction", "Analytical chemistry", "Chemical analysis", "atmospheric chemistry", "chromatography", "Gas chromatography", "Anatomy and physiology", "Respiratory system", "Respiratory physiology", "Infectious diseases", "Bacterial diseases", "bloodstream infections", "Borrelia infection", "treated", "scid", "mice", "systemic"], "article_id"=>760952, "categories"=>["Medicine", "Chemistry", "Biological Sciences"], "users"=>["Alan G. Barbour", "Charlotte M. Hirsch", "Arash Ghalyanchi Langeroudi", "Simone Meinardi", "Eric R. G. Lewis", "Azadeh Shojaee Estabragh", "Donald R. Blake"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0069802.t001", "stats"=>{"downloads"=>3, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characteristics_of_uninfected_infected_and_treated_SCID_mice_with_systemic_Borrelia_hermsii_infections_/760952", "title"=>"Characteristics of uninfected, infected, and treated SCID mice with systemic <i>Borrelia hermsii</i> infections.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-07-31 02:22:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1138589", "https://ndownloader.figshare.com/files/1138599", "https://ndownloader.figshare.com/files/1138600", "https://ndownloader.figshare.com/files/1138601"], "description"=>"<div><p>Blood is the specimen of choice for most laboratory tests for diagnosis and disease monitoring. Sampling exhaled breath is a noninvasive alternative to phlebotomy and has the potential for real-time monitoring at the bedside. Improved instrumentation has advanced breath analysis for several gaseous compounds from humans. However, application to small animal models of diseases and physiology has been limited. To extend breath analysis to mice, we crafted a means for collecting nose-only breath samples from groups and individual animals who were awake. Samples were subjected to gas chromatography and mass spectrometry procedures developed for highly sensitive analysis of trace volatile organic compounds (VOCs) in the atmosphere. We evaluated the system with experimental systemic infections of severe combined immunodeficiency <i>Mus musculus</i> with the bacterium <i>Borrelia hermsii</i>. Infected mice developed bacterial densities of ∼10<sup>7</sup> per ml of blood by day 4 or 5 and in comparison to uninfected controls had hepatosplenomegaly and elevations of both inflammatory and anti-inflammatory cytokines. While 12 samples from individual infected mice on days 4 and 5 and 6 samples from uninfected mice did not significantly differ for 72 different VOCs, carbon monoxide (CO) was elevated in samples from infected mice, with a mean (95% confidence limits) effect size of 4.2 (2.8–5.6), when differences in CO<sub>2</sub> in the breath were taken into account. Normalized CO values declined to the uninfected range after one day of treatment with the antibiotic ceftriaxone. Strongly correlated with CO in the breath were levels of heme oxygenase-1 protein in serum and HMOX1 transcripts in whole blood. These results (i) provide further evidence of the informativeness of CO concentration in the exhaled breath during systemic infection and inflammation, and (ii) encourage evaluation of this noninvasive analytic approach in other various other rodent models of infection and for utility in clinical management.</p></div>", "links"=>[], "tags"=>["microbiology", "immunity", "inflammation", "Bacterial pathogens", "Host-pathogen interaction", "Analytical chemistry", "Chemical analysis", "atmospheric chemistry", "chromatography", "Gas chromatography", "Anatomy and physiology", "Respiratory system", "Respiratory physiology", "Infectious diseases", "Bacterial diseases", "bloodstream infections", "Borrelia infection", "carbon", "monoxide", "exhaled", "mice", "systemic", "bacterial"], "article_id"=>760954, "categories"=>["Medicine", "Chemistry", "Biological Sciences"], "users"=>["Alan G. Barbour", "Charlotte M. Hirsch", "Arash Ghalyanchi Langeroudi", "Simone Meinardi", "Eric R. G. Lewis", "Azadeh Shojaee Estabragh", "Donald R. Blake"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0069802.s001", "https://dx.doi.org/10.1371/journal.pone.0069802.s002", "https://dx.doi.org/10.1371/journal.pone.0069802.s003", "https://dx.doi.org/10.1371/journal.pone.0069802.s004"], "stats"=>{"downloads"=>13, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Elevated_Carbon_Monoxide_in_the_Exhaled_Breath_of_Mice_during_a_Systemic_Bacterial_Infection_/760954", "title"=>"Elevated Carbon Monoxide in the Exhaled Breath of Mice during a Systemic Bacterial Infection", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-07-31 02:22:04"}

PMC Usage Stats | Further Information

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