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Published in: BMC Infectious Diseases 1/2019

Open Access 01-12-2019 | Research article

Evaluation of the complexity of indoor air in hospital wards based on PM2.5, real-time PCR, adenosine triphosphate bioluminescence assay, microbial culture and mass spectrometry

Authors: Shao Ling, Liu Hui

Published in: BMC Infectious Diseases | Issue 1/2019

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Abstract

Background

The aim of this study was to establish a set of assessment methods suitable for evaluating the complex indoor environment of hospital wards and to ascertain the composition of bacteria and microbial ecology of hospital wards.

Methods

Colony-forming units (CFUs), PM2.5 detection, real-time PCR, and adenosine triphosphate (ATP) bioluminescence assay were employed to evaluate the complexity of indoor air in 18 wards of nine departments in a hospital and two student dormitories in a university. Subsequently, the microbial samples were quantified and identified using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS).

Results

Although the studied indices were relatively independent, the PM2.5 content was correlated with bacterial CFUs determined by passive sedimentation method, bacterial and fungal counts measured by real-time PCR, and ATP bioluminescence assay. The composition of microorganisms in the air of hospital wards differed from that in the air of student dormitories. The dominant genera in hospital wards were Staphylococcus (39.4%), Micrococcus (21.9%), Corynebacterium (11.7%), Kocuria (4.4%), Bacillus (2.9%), Streptococcus (1.6%), Moraxella (1.6%), and Enterococcus (1.3%), and the microbial ecology differed between Respiration Dept. III and other hospital departments. Additionally, 11.1 and 27.3% of bacteria in hospital wards and student dormitories were not identified, respectively.

Conclusions

Assessment of environmental quality of hospital wards should be based on comprehensive analysis with multiple indicators. There may be imbalances in the microbial diversity in the hospital wards, therefore, monitoring of the environmental quality of hospitals is important in the prevention of nosocomial infections.
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Literature
1.
go back to reference Dancer SJ. Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination. Clin Microbiol Rev. 2014;27(4):665–90.CrossRef Dancer SJ. Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination. Clin Microbiol Rev. 2014;27(4):665–90.CrossRef
2.
go back to reference Weber DJ, Anderson D, Rutala WA. The role of the surface environment in healthcare-associated infections. Curr Opin Infect Dis. 2013;26(4):338–44.CrossRef Weber DJ, Anderson D, Rutala WA. The role of the surface environment in healthcare-associated infections. Curr Opin Infect Dis. 2013;26(4):338–44.CrossRef
3.
go back to reference Drees M, Snydman DR, Schmid CH, Barefoot L, Hansjosten K, Vue PM, Cronin M, Nasraway SA, Golan Y. Prior environmental contamination increases the risk of acquisition of vancomycin-resistantenterococci. Clin Infect Dis. 2008;46(5):678–85.CrossRef Drees M, Snydman DR, Schmid CH, Barefoot L, Hansjosten K, Vue PM, Cronin M, Nasraway SA, Golan Y. Prior environmental contamination increases the risk of acquisition of vancomycin-resistantenterococci. Clin Infect Dis. 2008;46(5):678–85.CrossRef
4.
go back to reference Wilks M, Wilson A, Warwick S, Price E, Kennedy D, Ely A, Millar MR. Control of an outbreak of multidrug-resistant Acinetobacter baumannii-calcoaceticus colonization and infection in an intensive care unit (ICU) without closing the ICU or placing patients in isolation. Infect Control Hosp Epidemiol. 2006;27(7):654–8.CrossRef Wilks M, Wilson A, Warwick S, Price E, Kennedy D, Ely A, Millar MR. Control of an outbreak of multidrug-resistant Acinetobacter baumannii-calcoaceticus colonization and infection in an intensive care unit (ICU) without closing the ICU or placing patients in isolation. Infect Control Hosp Epidemiol. 2006;27(7):654–8.CrossRef
5.
go back to reference Nseir S, Blazejewski C, Lubret R, Wallet F, Courcol R, Durocher A. Risk of acquiring multidrug-resistant gram-negative bacilli from prior room occupants in the intensive care unit. Clin Microbiol Infect. 2011;17(8):1201–8.CrossRef Nseir S, Blazejewski C, Lubret R, Wallet F, Courcol R, Durocher A. Risk of acquiring multidrug-resistant gram-negative bacilli from prior room occupants in the intensive care unit. Clin Microbiol Infect. 2011;17(8):1201–8.CrossRef
6.
go back to reference Shaughnessy MK, Micielli RL, DePestel DD, Arndt J, Strachan CL, Welch KB, Chenoweth CE. Evaluation of hospital room assignment and acquisition of Clostridium difficile infection. Infect Control Hosp Epidemiol. 2011;32(3):201–6.CrossRef Shaughnessy MK, Micielli RL, DePestel DD, Arndt J, Strachan CL, Welch KB, Chenoweth CE. Evaluation of hospital room assignment and acquisition of Clostridium difficile infection. Infect Control Hosp Epidemiol. 2011;32(3):201–6.CrossRef
8.
go back to reference Kedjarune U, Kukiattrakoon B, Yapong B, Chowanadisai S, Leggat P. Bacterial aerosols in the dental clinic: effect of time, position and type of treatment. Int Dent J. 2000;50(2):103–7.CrossRef Kedjarune U, Kukiattrakoon B, Yapong B, Chowanadisai S, Leggat P. Bacterial aerosols in the dental clinic: effect of time, position and type of treatment. Int Dent J. 2000;50(2):103–7.CrossRef
9.
go back to reference Mirzaei R, Shahriary E, Qureshi MI, Rakhshkhorshid A, Khammary A, Mohammadi M. Quantitative and qualitative evaluation of bio-aerosols in surgery rooms and emergency department of an educational hospital. Jundishapur J Microbiol. 2014;7(10):e11688.PubMedPubMedCentral Mirzaei R, Shahriary E, Qureshi MI, Rakhshkhorshid A, Khammary A, Mohammadi M. Quantitative and qualitative evaluation of bio-aerosols in surgery rooms and emergency department of an educational hospital. Jundishapur J Microbiol. 2014;7(10):e11688.PubMedPubMedCentral
10.
go back to reference Okten S, Asan A. Airborne fungi and bacteria in indoor and outdoor environment of the pediatric unit of Edirne government hospital. Environ Monit Assess. 2012;184(3):1739–51.CrossRef Okten S, Asan A. Airborne fungi and bacteria in indoor and outdoor environment of the pediatric unit of Edirne government hospital. Environ Monit Assess. 2012;184(3):1739–51.CrossRef
11.
go back to reference Sautour M, Sixt N, Dalle F, L'Ollivier C, Fourquenet V, Calinon C, Paul K, Valvin S, Maurel A, Aho S, Couillault G, Cachia C, Vagner O, Cuisenier B, Caillot D, Bonnin A. Profiles and seasonal distribution of airborne fungi in indoor and outdoor environments at a French hospital. Sci Total Environ. 2009;407(12):3766–71.CrossRef Sautour M, Sixt N, Dalle F, L'Ollivier C, Fourquenet V, Calinon C, Paul K, Valvin S, Maurel A, Aho S, Couillault G, Cachia C, Vagner O, Cuisenier B, Caillot D, Bonnin A. Profiles and seasonal distribution of airborne fungi in indoor and outdoor environments at a French hospital. Sci Total Environ. 2009;407(12):3766–71.CrossRef
12.
go back to reference Fan J, Li S, Fan C, Bai Z, Yang K. The impact of PM2.5 on asthma emergency department visits: a systematic review and meta-analysis. Environ Sci Pollut Res Int. 2016;23(1):843–50.CrossRef Fan J, Li S, Fan C, Bai Z, Yang K. The impact of PM2.5 on asthma emergency department visits: a systematic review and meta-analysis. Environ Sci Pollut Res Int. 2016;23(1):843–50.CrossRef
14.
go back to reference Pope CA 3rd, Dockery DW. Health effects of fine particulate air pollution: lines that connect. J Air Waste Manag Assoc. 2006;56(6):709–42.CrossRef Pope CA 3rd, Dockery DW. Health effects of fine particulate air pollution: lines that connect. J Air Waste Manag Assoc. 2006;56(6):709–42.CrossRef
15.
go back to reference Brook RD, Rajagopalan S, Pope CA 3rd, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC Jr, Whitsel L, Kaufman JD. American Heart Association Council on Epidemiology and Prevention, Council on the Kidney in Cardiovascular Disease, and Council on Nutrition, Physical Activity and Metabolism. Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation. 2010;121(21):2331–78.CrossRef Brook RD, Rajagopalan S, Pope CA 3rd, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC Jr, Whitsel L, Kaufman JD. American Heart Association Council on Epidemiology and Prevention, Council on the Kidney in Cardiovascular Disease, and Council on Nutrition, Physical Activity and Metabolism. Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation. 2010;121(21):2331–78.CrossRef
17.
go back to reference Erqou S, Clougherty JE, Olafiranye O, Magnani JW, Aiyer A, Tripathy S, Kinnee E, Kip KE, Reis SE. Particulate matter air pollution and racial differences in cardiovascular disease risk. Arterioscler Thromb Vasc Biol. 2018;38(4):935–42.CrossRef Erqou S, Clougherty JE, Olafiranye O, Magnani JW, Aiyer A, Tripathy S, Kinnee E, Kip KE, Reis SE. Particulate matter air pollution and racial differences in cardiovascular disease risk. Arterioscler Thromb Vasc Biol. 2018;38(4):935–42.CrossRef
18.
go back to reference Puett RC, Hart JE, Yanosky JD, Paciorek C, Schwartz J, Suh H, Speizer FE, Laden F. Chronic fine and coarse particulate exposure, mortality, and coronary heart disease in the Nurses' health study. Environ Health Perspect. 2009;117(11):1697–701.CrossRef Puett RC, Hart JE, Yanosky JD, Paciorek C, Schwartz J, Suh H, Speizer FE, Laden F. Chronic fine and coarse particulate exposure, mortality, and coronary heart disease in the Nurses' health study. Environ Health Perspect. 2009;117(11):1697–701.CrossRef
19.
go back to reference Stafoggia M, Cesaroni G, Peters A, Andersen ZJ, Badaloni C, Beelen R, Caracciolo B, Cyrys J, de Faire U, de Hoogh K, et al. Long-term exposure to ambient air pollution and incidence of cerebrovascular events: results from 11 European cohorts within the ESCAPE project. Environ Health Perspect. 2014;122(9):919–25.CrossRef Stafoggia M, Cesaroni G, Peters A, Andersen ZJ, Badaloni C, Beelen R, Caracciolo B, Cyrys J, de Faire U, de Hoogh K, et al. Long-term exposure to ambient air pollution and incidence of cerebrovascular events: results from 11 European cohorts within the ESCAPE project. Environ Health Perspect. 2014;122(9):919–25.CrossRef
20.
go back to reference Hamra GB, Guha N, Cohen A, Laden F, Raaschou-Nielsen O, Samet JM, Vineis P, Forastiere F, Saldiva P, Yorifuji T, et al. Outdoor particulate matter exposure and lung cancer: a systematic review and meta-analysis. Environ Health Perspect. 2014;122(9):906–11.CrossRef Hamra GB, Guha N, Cohen A, Laden F, Raaschou-Nielsen O, Samet JM, Vineis P, Forastiere F, Saldiva P, Yorifuji T, et al. Outdoor particulate matter exposure and lung cancer: a systematic review and meta-analysis. Environ Health Perspect. 2014;122(9):906–11.CrossRef
21.
go back to reference Calderón-Garcidueñas L, Solt AC, Henríquez-Roldán C, Torres-Jardón R, Nuse B, Herritt L, Villarreal-Calderón R, Osnaya N, Stone I, García R, et al. Long-term air pollution exposure is associated with neuroinflammation, an altered innate immune response, disruption of the blood-brain barrier, ultrafine particulate deposition, and accumulation of amyloid beta-42 and alpha-synuclein in children and young adults. Toxicol Pathol. 2008;36(2):289–310.CrossRef Calderón-Garcidueñas L, Solt AC, Henríquez-Roldán C, Torres-Jardón R, Nuse B, Herritt L, Villarreal-Calderón R, Osnaya N, Stone I, García R, et al. Long-term air pollution exposure is associated with neuroinflammation, an altered innate immune response, disruption of the blood-brain barrier, ultrafine particulate deposition, and accumulation of amyloid beta-42 and alpha-synuclein in children and young adults. Toxicol Pathol. 2008;36(2):289–310.CrossRef
23.
go back to reference Han B, Zhang R, Yang W, Bai Z, Ma Z, Zhang W. Heavy haze episodes in Beijing during January 2013: inorganic ion chemistry and source analysis using highly time-resolved measurements from an urban site. Sci Total Environ. 2016;544:319–29.CrossRef Han B, Zhang R, Yang W, Bai Z, Ma Z, Zhang W. Heavy haze episodes in Beijing during January 2013: inorganic ion chemistry and source analysis using highly time-resolved measurements from an urban site. Sci Total Environ. 2016;544:319–29.CrossRef
24.
go back to reference Wang J, Hang Ho SS, Huang R, Gao M, Liu S, Zhao S, Cao J, Wang G, Shen Z, Han Y. Characterization of parent and oxygenated-polycyclic aromatic hydrocarbons(PAHs) in Xi’an, China during heating period: an investigation of spatial distribution and transformation. Chemosphere. 2016;159:367–77.CrossRef Wang J, Hang Ho SS, Huang R, Gao M, Liu S, Zhao S, Cao J, Wang G, Shen Z, Han Y. Characterization of parent and oxygenated-polycyclic aromatic hydrocarbons(PAHs) in Xi’an, China during heating period: an investigation of spatial distribution and transformation. Chemosphere. 2016;159:367–77.CrossRef
26.
go back to reference Hart JE, Liao X, Hong B, Puett RC, Yanosky JD, Suh H, Kioumourtzoglou MA, Spiegelman D, Laden F. The association of long-term exposure to PM2.5 on all-cause mortality in the Nurses' health study and the impact of measurement-error correction. Environ Health. 2015;14:38 https://doi.org/10.1186/s12940-015-0027-6.CrossRef Hart JE, Liao X, Hong B, Puett RC, Yanosky JD, Suh H, Kioumourtzoglou MA, Spiegelman D, Laden F. The association of long-term exposure to PM2.5 on all-cause mortality in the Nurses' health study and the impact of measurement-error correction. Environ Health. 2015;14:38 https://​doi.​org/​10.​1186/​s12940-015-0027-6.CrossRef
27.
go back to reference Napoli C, Marcotrigiano V, Montagna MT. Air sampling procedures to evaluate microbial contamination: a comparison between active and passive methods in operating theatres. BMC Public Health. 2012;12:594.CrossRef Napoli C, Marcotrigiano V, Montagna MT. Air sampling procedures to evaluate microbial contamination: a comparison between active and passive methods in operating theatres. BMC Public Health. 2012;12:594.CrossRef
28.
go back to reference Sanna T, Dallolio L, Raggi A, Mazzetti M, Lorusso G, Zanni A, Farruggia P, Leoni E. ATP bioluminescence assay for evaluating cleaning practices in operating theatres: applicability and limitations. BMC Infect Dis. 2018;18(1):583.CrossRef Sanna T, Dallolio L, Raggi A, Mazzetti M, Lorusso G, Zanni A, Farruggia P, Leoni E. ATP bioluminescence assay for evaluating cleaning practices in operating theatres: applicability and limitations. BMC Infect Dis. 2018;18(1):583.CrossRef
29.
go back to reference Radosevich JL, Wilson WJ, Shinn JH, DeSantis TZ, Andersen GL. Development of a high-volume aerosol collection system for the identification of air-borne micro-organisms. Lett Appl Microbiol. 2002;34(3):162–7.CrossRef Radosevich JL, Wilson WJ, Shinn JH, DeSantis TZ, Andersen GL. Development of a high-volume aerosol collection system for the identification of air-borne micro-organisms. Lett Appl Microbiol. 2002;34(3):162–7.CrossRef
30.
go back to reference Toivola M, Alm S, Reponen T, Kolari S, Nevalainen A. Personal exposures and microenvironmental concentrations of particles and bioaerosols. J Environ Monit. 2002;4(1):166–74.CrossRef Toivola M, Alm S, Reponen T, Kolari S, Nevalainen A. Personal exposures and microenvironmental concentrations of particles and bioaerosols. J Environ Monit. 2002;4(1):166–74.CrossRef
31.
go back to reference Eduard W, Heederik D. Methods for quantitative assessment of airborne levels of noninfectious microorganisms in highly contaminated work environments. Am Ind Hyg Assoc J. 1998;59(2):113–27.CrossRef Eduard W, Heederik D. Methods for quantitative assessment of airborne levels of noninfectious microorganisms in highly contaminated work environments. Am Ind Hyg Assoc J. 1998;59(2):113–27.CrossRef
32.
go back to reference Croxatto A, Prod'hom G, Greub G. Applications of MALDI-TOF mass spectrometry in clinical diagnostic microbiology. FEMS Microbiol Rev. 2012;36(2):380–407.CrossRef Croxatto A, Prod'hom G, Greub G. Applications of MALDI-TOF mass spectrometry in clinical diagnostic microbiology. FEMS Microbiol Rev. 2012;36(2):380–407.CrossRef
33.
go back to reference Singhal N, Kumar M, Kanaujia PK, Virdi JS. MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis. Front Microbiol. 2015;6:791.CrossRef Singhal N, Kumar M, Kanaujia PK, Virdi JS. MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis. Front Microbiol. 2015;6:791.CrossRef
35.
go back to reference ASTM Standard E1792–-03(2016). Standard Specification for Wipe Sampling Materials for Lead in Surface Dust. West Conshohocken: ASTM International; 2016. https://www.astm.org. ASTM Standard E1792–-03(2016). Standard Specification for Wipe Sampling Materials for Lead in Surface Dust. West Conshohocken: ASTM International; 2016. https://​www.​astm.​org.
36.
go back to reference Yamamoto N, Shendell DG, Peccia J. Assessing allergenic fungi in house dust by floor wipe sampling and quantitative PCR. Indoor Air. 2011;21(6):521–30.CrossRef Yamamoto N, Shendell DG, Peccia J. Assessing allergenic fungi in house dust by floor wipe sampling and quantitative PCR. Indoor Air. 2011;21(6):521–30.CrossRef
37.
go back to reference Adams RI, Tian Y, Taylor JW, Bruns TD, Hyvärinen A, Täubel M. Passive dust collectors for assessing airborne microbial material. Microbiome. 2015;3:46.CrossRef Adams RI, Tian Y, Taylor JW, Bruns TD, Hyvärinen A, Täubel M. Passive dust collectors for assessing airborne microbial material. Microbiome. 2015;3:46.CrossRef
38.
go back to reference Tseng CP, Cheng JC, Tseng CC, Wang C, Chen YL, Chiu DT, Liao HC, Chang SS. Broad-range ribosomal RNA real-time PCR after removal of DNA from reagents: melting profiles for clinically important bacteria. Clin Chem. 2003;49(2):306–9.CrossRef Tseng CP, Cheng JC, Tseng CC, Wang C, Chen YL, Chiu DT, Liao HC, Chang SS. Broad-range ribosomal RNA real-time PCR after removal of DNA from reagents: melting profiles for clinically important bacteria. Clin Chem. 2003;49(2):306–9.CrossRef
39.
go back to reference Vollmer T, Störmer M, Kleesiek K, Dreier J. Evaluation of novel broad-range real-time PCR assay for rapid detection of human pathogenic fungi in various clinical specimens. J Clin Microbiol. 2008;46(6):1919–26.CrossRef Vollmer T, Störmer M, Kleesiek K, Dreier J. Evaluation of novel broad-range real-time PCR assay for rapid detection of human pathogenic fungi in various clinical specimens. J Clin Microbiol. 2008;46(6):1919–26.CrossRef
41.
go back to reference Liakopoulos V, Petinaki E, Efthimiadi G, Klapsa D, Giannopoulou M, Dovas S, Eleftheriadis T, Mertens PR, Stefanidis I. Clonal relatedness of methicillin-resistant coagulase-negative staphylococci in the haemodialysis unit of a single university Centre in Greece. Nephrol Dial Transplant. 2008;23(8):2599–603.CrossRef Liakopoulos V, Petinaki E, Efthimiadi G, Klapsa D, Giannopoulou M, Dovas S, Eleftheriadis T, Mertens PR, Stefanidis I. Clonal relatedness of methicillin-resistant coagulase-negative staphylococci in the haemodialysis unit of a single university Centre in Greece. Nephrol Dial Transplant. 2008;23(8):2599–603.CrossRef
42.
go back to reference Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev. 2014;27:870–926.CrossRef Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin Microbiol Rev. 2014;27:870–926.CrossRef
43.
go back to reference Takeuchi F, Watanabe S, Baba T, Yuzawa H, Ito T, Morimoto Y, Kuroda M, Cui L, Takahashi M, Ankai A, Baba S, Fukui S, Lee JC, Hiramatsu K. Whole-genome sequencing of staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol. 2005;187(21):7292–308.CrossRef Takeuchi F, Watanabe S, Baba T, Yuzawa H, Ito T, Morimoto Y, Kuroda M, Cui L, Takahashi M, Ankai A, Baba S, Fukui S, Lee JC, Hiramatsu K. Whole-genome sequencing of staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol. 2005;187(21):7292–308.CrossRef
44.
go back to reference Silva PV, Cruz RS, Keim LS, Paula GR, Carvalho BT, Coelho LR, Carvalho MC, Rosa JM, Figueiredo AM, Teixeira LA. The antimicrobial susceptibility, biofilm formation and genotypic profiles of staphylococcus haemolyticus from bloodstream infections. Mem Inst Oswaldo Cruz. 2013;108(6):812–3.CrossRef Silva PV, Cruz RS, Keim LS, Paula GR, Carvalho BT, Coelho LR, Carvalho MC, Rosa JM, Figueiredo AM, Teixeira LA. The antimicrobial susceptibility, biofilm formation and genotypic profiles of staphylococcus haemolyticus from bloodstream infections. Mem Inst Oswaldo Cruz. 2013;108(6):812–3.CrossRef
45.
go back to reference Barros EM, Ceotto H, Bastos MC, Dos Santos KR, Giambiagi-Demarval M. Staphylococcus haemolyticus as an important hospital pathogen and carrier of methicillin resistance genes. J Clin Microbiol. 2012;50(1):166–8.CrossRef Barros EM, Ceotto H, Bastos MC, Dos Santos KR, Giambiagi-Demarval M. Staphylococcus haemolyticus as an important hospital pathogen and carrier of methicillin resistance genes. J Clin Microbiol. 2012;50(1):166–8.CrossRef
46.
go back to reference Czekaj T, Ciszewski M, Szewczyk EM. Staphylococcus haemolyticus - an emerging threat in the twilight of the antibiotics age. Microbiology. 2015;161(11):2061–8.CrossRef Czekaj T, Ciszewski M, Szewczyk EM. Staphylococcus haemolyticus - an emerging threat in the twilight of the antibiotics age. Microbiology. 2015;161(11):2061–8.CrossRef
47.
go back to reference Froggatt JW, Johnston JL, Galetto DW, Archer GL. Antimicrobial resistance in nosocomial isolates of staphylococcus haemolyticus. Antimicrob Agents Chemother. 1989;33(4):460–6.CrossRef Froggatt JW, Johnston JL, Galetto DW, Archer GL. Antimicrobial resistance in nosocomial isolates of staphylococcus haemolyticus. Antimicrob Agents Chemother. 1989;33(4):460–6.CrossRef
48.
go back to reference Chiew YF, Charles M, Johnstone MC, Thompson KM, Parnell KD, Penno EC. Detection of vancomycin heteroresistant staphylococcus haemolyticus and vancomycin intermediate resistant Staphylococcus epidermidis by means of vancomycin screening agar. Pathology. 2007;39(3):375–7.CrossRef Chiew YF, Charles M, Johnstone MC, Thompson KM, Parnell KD, Penno EC. Detection of vancomycin heteroresistant staphylococcus haemolyticus and vancomycin intermediate resistant Staphylococcus epidermidis by means of vancomycin screening agar. Pathology. 2007;39(3):375–7.CrossRef
50.
go back to reference Savini V, Catavitello C, Masciarelli G, Astolfi D, Balbinot A, Bianco A, Febbo F, D'Amario C, D'Antonio D. Drug sensitivity and clinical impact of members of the genus Kocuria. J Med Microbiol. 2010;59(Pt 12):1395–402.CrossRef Savini V, Catavitello C, Masciarelli G, Astolfi D, Balbinot A, Bianco A, Febbo F, D'Amario C, D'Antonio D. Drug sensitivity and clinical impact of members of the genus Kocuria. J Med Microbiol. 2010;59(Pt 12):1395–402.CrossRef
51.
go back to reference Kumar CG, Sujitha P. Kocuran, an exopolysaccharide isolated from Kocuria rosea strain BS-1 and evaluation of its in vitro immunosuppression activities. Enzym Microb Technol. 2014;55:113–20.CrossRef Kumar CG, Sujitha P. Kocuran, an exopolysaccharide isolated from Kocuria rosea strain BS-1 and evaluation of its in vitro immunosuppression activities. Enzym Microb Technol. 2014;55:113–20.CrossRef
52.
go back to reference Kandi V, Palange P, Vaish R, Bhatti AB, Kale V, Kandi MR, Bhoomagiri MR. Emerging bacterial infection: identification and clinical significance of Kocuria species. Cureus. 2016;8(8):e731.PubMedPubMedCentral Kandi V, Palange P, Vaish R, Bhatti AB, Kale V, Kandi MR, Bhoomagiri MR. Emerging bacterial infection: identification and clinical significance of Kocuria species. Cureus. 2016;8(8):e731.PubMedPubMedCentral
53.
go back to reference Chen HM, Chi H, Chiu NC, Huang FY. Kocuria kristinae: a true pathogen in pediatric patients. J Microbiol Immunol Infect. 2015;48(1):80–4.CrossRef Chen HM, Chi H, Chiu NC, Huang FY. Kocuria kristinae: a true pathogen in pediatric patients. J Microbiol Immunol Infect. 2015;48(1):80–4.CrossRef
54.
go back to reference Moreira JS, Riccetto AG, Silva MT, Vilela MM. Study group Centro Médico de Campinas/Franceschi Medicina laboratorial. Endocarditis by Kocuria rosea in an immunocompetent child. Braz J Infect Dis. 2015;19(1):82–4.CrossRef Moreira JS, Riccetto AG, Silva MT, Vilela MM. Study group Centro Médico de Campinas/Franceschi Medicina laboratorial. Endocarditis by Kocuria rosea in an immunocompetent child. Braz J Infect Dis. 2015;19(1):82–4.CrossRef
Metadata
Title
Evaluation of the complexity of indoor air in hospital wards based on PM2.5, real-time PCR, adenosine triphosphate bioluminescence assay, microbial culture and mass spectrometry
Authors
Shao Ling
Liu Hui
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2019
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-019-4249-z

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