Seasonal and spatial variations of bioaerosols and antibiotic resistance bacteria in different wards of the hospital
Abstract
Introduction: Transmission of bioaerosols through the air is known as an important route for a wide range of nosocomial infections. Therefore, in the present study, we aimed to evaluate the type and diversity of bioaerosols and antibiotic resistance of bacterial bioaerosols in the indoor environments of Sina Educational and Treatment Hospital, Tabriz, Iran.
Methods and materials: Bioaerosol samples were collected from February to March (winter) and June to July (summer) 2020 in three periods of daytime (morning, noon and evening). After sampling, fungal and bacterial samples were incubated and the disk diffusion agar method (Kirby-Bauer) was used for assessing the antibiotic resistance.
Results: the concentration of bioaerosols varied significantly in different wards. In addition, the concentration of bioaerosols in winter was observed to be higher than in summer. The highest and lowest airborne fungal concentrations were found in burns operating room and men's infectious ward (49 CFU/m3) and children's burns ward (28 CFU/m3), respectively. The predominantly isolated bacteria were Streptococcus spp. (38%) and Staphylococcus spp. (37%). Also, the main isolated fungi belonged to the genera Aspergillus (75.9%) and Penicillium (22.5%). The highest rates of antibiotic resistance were observed for colistin (100%) in Gram-negative and penicillin (84.2%) in Gram-positive.
Conclusion: Timely and regular disinfection of hospital wards can affect the density of bioaerosols. Owing to the prevalence of COVID-19 epidemic in the world, the staff and patients often were wearing masks, gloves and special clothing as well as using disinfectants to prevent coronavirus infection in wards during the summer sampling.
1. Azimi F, Nabizadeh R, Alimohammadi M, Naddafi K. Bacterial bioaerosols in the operating rooms: a case study in Tehran Shariati hospital. Journal of Air Pollution and Health. 2016;1(3):215-8.
2. Alsved M, Civilis A, Ekolind P, Tammelin A, Andersson AE, Jakobsson J, et al. Temperature-controlled airflow ventilation in operating rooms compared with laminar airflow and turbulent mixed airflow. Journal of Hospital Infection. 2018;98(2):181-90.
3. Bolookat F, Hassanvand MS, Faridi S, Hadei M, Rahmatinia M, Alimohammadi M. Assessment of bioaerosol particle characteristics at different hospital wards and operating theaters: A case study in Tehran. MethodsX. 2018;5:1588-96.
4. Roshan SK, Godini H, Nikmanesh B, Bakhshi H, Charsizadeh A. Study on the relationship between the concentration and type of fungal bio-aerosols at indoor and outdoor air in the Children’s Medical Center, Tehran, Iran. Environmental monitoring and assessment. 2019;191(2):48.
5. Perrino C, Marcovecchio F. A new method for assessing the contribution of primary biological atmospheric particles to the mass concentration of the atmospheric aerosol. Environment international. 2016;87:108-15.
6. Malakootian M, Amiri Gharghani M. Investigation of type and density of bio-aerosols in air samples from educational hospital wards of Kerman city, 2014. Environmental Health Engineering and Management 2016;3(4):197-202.
7. Dehghani M, Sorooshian A, Nazmara S, Baghani AN, Delikhoon M. Concentration and type of bioaerosols before and after conventional disinfection and sterilization procedures inside hospital operating rooms. Ecotoxicology and environmental safety. 2018;164:277-82.
8. Mirhoseini SH, Nikaeen M, Khanahmad H, Hatamzadeh M, Hassanzadeh A. Monitoring of airborne bacteria and aerosols in different wards of hospitals-Particle counting usefulness in investigation of airborne bacteria. Annals of Agricultural and Environmental Medicine. 2015;22(4).
9. Bisag A, Isabelli P, Laurita R, Bucci C, Capelli F, Dirani G, et al. Cold atmospheric plasma inactivation of aerosolized microdroplets containing bacteria and purified SARS‐CoV‐2 RNA to contrast airborne indoor transmission. Plasma Processes and Polymers. 2020;17(10):2000154.
10. Van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, et al. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. New England journal of medicine. 2020;382(16):1564-7.
11. Soltanian M, Mohajeri P, Najafi F, Kazemi S, Asadi F. Study of airborne bacterial density in surgery and infectious wards of hospitals affiliated with Kermakshah University Medical Science and its relationship with environmental factors. Iranian Journal of Epidemiology. 2018;13(4).
12. Memarzadeh F, Xu W, editors. Role of air changes per hour (ACH) in possible transmission of airborne infections. Building Simulation; 2012: Springer.
13. WHO. Indoor air quality: biological contaminants: report on a WHO meeting, Rautavaara, 29 August–2 September 1988: World Health Organization. Regional Office for Europe; 1990.
14. Veysi R, Heibati B, Jahangiri M, Kumar P, Latif MT, Karimi A. Indoor air quality-induced respiratory symptoms of a hospital staff in Iran. Environmental monitoring and assessment. 2019;191(2):50.
15. Bakhtiari R, Hadei M, Hopke PK, Shahsavani A, Rastkari N, Kermani M, et al. Investigation of in-cabin volatile organic compounds (VOCs) in taxis; influence of vehicle's age, model, fuel, and refueling. Environmental Pollution. 2018;237:348-55.
16. Neu HC. The crisis in antibiotic resistance. Science. 1992;257(5073):1064-73.
17. WHO. Global antimicrobial resistance surveillance system: manual for early implementation.[Google Scholar]. 2015.
18. Health UDo, Services H. Antibiotic resistance threats in the United States, 2013. Centers for disease control and prevention. 2013:1-113.
19. O’Neill J. Review on Antimicrobial Resistance Antimicrobial Resistance: Tackling a crisis for the health and wealth of nations. 2014. London: Wellcome Trust. 2018.
20. Montazer M, Soleimani N, Vahabi M, Abtahi M, Etemad K, Zendehdel R. Assessment of bacterial pathogens and their antibiotic resistance in the air of different wards of selected teaching hospitals in Tehran. Indian Journal of Occupational and Environmental Medicine. 2021;25(2):78.
21. Nunes ZG, Martins AS, Altoe ALF, Nishikawa MM, Leite MO, Aguiar PF, et al. Indoor air microbiological evaluation of offices, hospitals, industries, and shopping centers. Memórias do Instituto Oswaldo Cruz. 2005;100:351-7.
22. Napoli C, Tafuri S, Montenegro L, Cassano M, Notarnicola A, Lattarulo S, et al. Air sampling methods to evaluate microbial contamination in operating theatres: results of a comparative study in an orthopaedics department. Journal of Hospital Infection. 2012;80(2):128-32.
23. Kruczalak K, Olanczuk-Neyman K. Microorganisms in the Air Over Wastewater Treamtment Plants. Polish Journal of Environmental Studies. 2004;13(5).
24. Burkowska A, Kalwasińska A, Walczak M. Airborne mesophilic bacteria at the Ciechocinek health resort. Pol J Environ Stud. 2012;21(2):307-12.
25. Verde SC, Almeida SM, Matos J, Guerreiro D, Meneses M, Faria T, et al. Microbiological assessment of indoor air quality at different hospital sites. Research in Microbiology. 2015;166(7):557-63.
26. Yassin M, Almouqatea S. Assessment of airborne bacteria and fungi in an indoor and outdoor environment. International journal of environmental science & technology. 2010;7(3):535-44.
27. De la Maza LM, Pezzlo MT, Shigei JT, Tan GL, Peterson EM. Color atlas of medical bacteriology: ASM Press; 2013.
28. Holt JG, Krieg NR, Sneath PH. Bergey's manual of determinative bacterology. 1994.
29. Mousavi MS, Hadei M, Majlesi M, Hopke PK, Yarahmadi M, Emam B, et al. Investigating the effect of several factors on concentrations of bioaerosols in a well-ventilated hospital environment. Environmental monitoring and assessment. 2019;191(7):1-11.
30. Hwang SH, Park DU, Ha KC, Cho HW, Yoon CS. Airborne bacteria concentrations and related factors at university laboratories, hospital diagnostic laboratories and a biowaste site. Journal of clinical pathology. 2011;64(3):261-4.
31. Yousefzadeh A, Maleki A, Athar SD, Darvishi E, Ahmadi M, Mohammadi E, et al. Evaluation of bio-aerosols type, density, and modeling of dispersion in inside and outside of different wards of educational hospital. Environmental Science and Pollution Research. 2021:1-15.
32. Alsved M, Civilis A, Ekolind P, Tammelin A, Andersson AE, Jakobsson J, et al. Temperature-controlled airflow ventilation in operating rooms compared with laminar airflow and turbulent mixed airflow. Journal of Hospital Infection. 2018;98(2):181-90.
33. Yadav LR, Lingaraju K, Manjunath K, Raghu G, Kumar KS, Nagaraju G. Synergistic effect of MgO nanoparticles for electrochemical sensing, photocatalytic-dye degradation and antibacterial activity. Materials Research Express. 2017;4(2):025028.
34. Shokri S, Nikpey A, Varyani AS. Evaluation of hospital wards indoor air quality: the particles concentration. Journal of Air Pollution and Health. 2016;1(3):205-14.
35. Heo KJ, Lim CE, Kim HB, Lee BU. Effects of human activities on concentrations of culturable bioaerosols in indoor air environments. Journal of Aerosol Science. 2017;104:58-65.
36. Durack J, Boushey HA, Lynch SV. Airway microbiota and the implications of dysbiosis in asthma. Current allergy and asthma reports. 2016;16(8):52.
37. Bannerman TL, Rhoden DL, McAllister SK, Miller JM, Wilson LA. The source of coagulase-negative staphylococci in the Endophthalmitis Vitrectomy Study: a comparison of eyelid and intraocular isolates using pulsed-field gel electrophoresis. Archives of ophthalmology. 1997;115(3):357-61.
38. Engelhard D, Elishoov H, Strauss N, Naparstek E, Nagler A, Simhon A, et al. Nosocomial coagulase-negative staphylococcal infections in bone marrow transplantation recipients with central vein catheter: a 5-year prospective study. Transplantation. 1996;61(3):430-4.
39. Dinges MM, Orwin PM, Schlievert PM. Exotoxins of Staphylococcus aureus. Clinical microbiology reviews. 2000;13(1):16-34.
40. Archer GL, Climo MW. Antimicrobial susceptibility of coagulase-negative staphylococci. Antimicrobial agents and chemotherapy. 1994;38(10):2231-7.
41. Lowy FD. Staphylococcus aureus Infections. New England Journal of Medicine. 1998;339(8):520-32.
42. Caldwell CC, Chen Y, Goetzmann HS, Hao Y, Borchers MT, Hassett DJ, et al. Pseudomonas aeruginosa exotoxin pyocyanin causes cystic fibrosis airway pathogenesis. The American journal of pathology. 2009;175(6):2473-88.
43. Wu W, Jin Y, Bai F, Jin S. Pseudomonas aeruginosa. Molecular medical microbiology: Elsevier; 2015. p. 753-67.
44. McManus A, Mason A, McManus W, Pruitt B. Twenty-five year review of Pseudomonas aeruginosa bacteremia in a burn center. European journal of clinical microbiology. 1985;4(2):219-23.
45. Williams FN, Herndon DN, Hawkins HK, Lee JO, Cox RA, Kulp GA, et al. The leading causes of death after burn injury in a single pediatric burn center. Critical care. 2009;13(6):1-7.
46. Hardalo C, Edberg SC. Pseudomonas aeruginosa: assessment of risk from drinking water. Critical reviews in microbiology. 1997;23(1):47-75.
47. Blanc DS, Petignat C, Janin B, Bille J, Francioli P. Frequency and molecular diversity of Pseudomonas aeruginosa upon admission and during hospitalization: a prospective epidemiologic study. Clinical microbiology and infection. 1998;4(5):242-7.
48. Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW. Pseudomonas genomes: diverse and adaptable. FEMS microbiology reviews. 2011;35(4):652-80.
49. Keen III EF, Robinson BJ, Hospenthal DR, Aldous WK, Wolf SE, Chung KK, et al. Incidence and bacteriology of burn infections at a military burn center. Burns. 2010;36(4):461-8.
50. Bayat A, Shaaban H, Dodgson A, Dunn K. Implications for Burns Unit design following outbreak of multi-resistant Acinetobacter infection in ICU and Burns Unit. Burns. 2003;29(4):303-6.
51. Kanamori H, Parobek CM, Weber DJ, Van Duin D, Rutala WA, Cairns BA, et al. Next-generation sequencing and comparative analysis of sequential outbreaks caused by multidrug-resistant Acinetobacter baumannii at a large academic burn center. Antimicrobial agents and chemotherapy. 2015;60(3):1249-57.
52. Rungruanghiranya S, Somboonwit C, Kanchanapoom T. Acinetobacter infection in the intensive care unit. Journal of Infectious Diseases and Antimicrobial Agents. 2005;22(2):77-92.
53. Zarrilli R, Crispino M, Bagattini M, Barretta E, Di Popolo A, Triassi M, et al. Molecular epidemiology of sequential outbreaks of Acinetobacter baumannii in an intensive care unit shows the emergence of carbapenem resistance. Journal of clinical microbiology. 2004;42(3):946-53.
54. Wieland K, Chhatwal P, Vonberg R-P. Nosocomial outbreaks caused by Acinetobacter baumannii and Pseudomonas aeruginosa: Results of a systematic review. American journal of infection control. 2018;46(6):643-8.
55. Binder U, Lass-Flörl C. Epidemiology of invasive fungal infections in the mediterranean area. Mediterranean journal of hematology and infectious diseases. 2011;3(1).
56. Sudharsanam S, Swaminathan S, Ramalingam A, Thangavel G, Annamalai R, Steinberg R, et al. Characterization of indoor bioaerosols from a hospital ward in a tropical setting. African health sciences. 2012;12(2):217-25.
57. Mok T, Koehler A, Yu M, Ellis D, Johnson P, Wickham N. Fatal Penicillium citrinum pneumonia with pericarditis in a patient with acute leukemia. Journal of clinical microbiology. 1997;35(10):2654-6.
58. Paul D, Biswas K, Sengupta C, Sinha SN. Studies on environmental monitoring of aeromicroflora in a hospital at Kalyani, West Bengal, India. Front Environ Microbiol. 2015;1:47-50.
59. Park D-U, Yeom J-K, Lee WJ, Lee K-M. Assessment of the levels of airborne bacteria, gram-negative bacteria, and fungi in hospital lobbies. International journal of environmental research and public health. 2013;10(2):541-55.
60. Ghasemian A, Khodaparast S, Moghadam FS, Nojoomi F, Vardanjani HR. Types and levels of Bioaerosols in healthcare and community indoor settings in Iran. Avicenna Journal of Clinical Microbiology and Infection. 2016;4(1):41036-.
61. Scaltriti S, Cencetti S, Rovesti S, Marchesi I, Bargellini A, Borella P. Risk factors for particulate and microbial contamination of air in operating theatres. Journal of Hospital Infection. 2007;66(4):320-6.
62. Wan G-H, Chung F-F, Tang C-S. Long-term surveillance of air quality in medical center operating rooms. American journal of infection control. 2011;39(4):302-8.
63. Sautour M, Sixt N, Dalle F, l'Ollivier C, Calinon C, Fourquenet V, et al. Prospective survey of indoor fungal contamination in hospital during a period of building construction. Journal of Hospital infection. 2007;67(4):367-73.
64. Pastuszka J, Marchwinska-Wyrwal E, Wlazlo A. Bacterial aerosol in Silesian hospitals: Preliminary results. Polish Journal of Environmental Studies. 2005;14(6):883.
65. Augustowska M, Dutkiewicz J. Variability of airborne microflora in a hospital ward within a period of one year. Annals of Agricultural and Environmental Medicine. 2006;13(1):99-106.
66. Tsakris A, Poulou A, Kristo I, Pittaras T, Spanakis N, Pournaras S, et al. Large dissemination of VIM-2-metallo-β-lactamase-producing Pseudomonas aeruginosa strains causing health care-associated community-onset infections. Journal of clinical Microbiology. 2009;47(11):3524-9.
67. Tabassum S. Multidrug-resistant (MDR) Acinetobacter: a major Nosocomial pathogen challenging physicians. Bangladesh Journal of Medical Microbiology. 2007;1(2):65-8.
68. Wang A, Daneman N, Tan C, Brownstein JS, MacFadden DR. Evaluating the relationship between hospital antibiotic use and antibiotic resistance in common nosocomial pathogens. infection control & hospital epidemiology. 2017;38(12):1457-63.
69. Bialvaei AZ, Samadi Kafil H. Colistin, mechanisms and prevalence of resistance. Current medical research and opinion. 2015;31(4):707-21.
70. Kaye KS, Pogue JM, Tran TB, Nation RL, Li J. Agents of last resort: polymyxin resistance. Infectious Disease Clinics. 2016;30(2):391-414.
2. Alsved M, Civilis A, Ekolind P, Tammelin A, Andersson AE, Jakobsson J, et al. Temperature-controlled airflow ventilation in operating rooms compared with laminar airflow and turbulent mixed airflow. Journal of Hospital Infection. 2018;98(2):181-90.
3. Bolookat F, Hassanvand MS, Faridi S, Hadei M, Rahmatinia M, Alimohammadi M. Assessment of bioaerosol particle characteristics at different hospital wards and operating theaters: A case study in Tehran. MethodsX. 2018;5:1588-96.
4. Roshan SK, Godini H, Nikmanesh B, Bakhshi H, Charsizadeh A. Study on the relationship between the concentration and type of fungal bio-aerosols at indoor and outdoor air in the Children’s Medical Center, Tehran, Iran. Environmental monitoring and assessment. 2019;191(2):48.
5. Perrino C, Marcovecchio F. A new method for assessing the contribution of primary biological atmospheric particles to the mass concentration of the atmospheric aerosol. Environment international. 2016;87:108-15.
6. Malakootian M, Amiri Gharghani M. Investigation of type and density of bio-aerosols in air samples from educational hospital wards of Kerman city, 2014. Environmental Health Engineering and Management 2016;3(4):197-202.
7. Dehghani M, Sorooshian A, Nazmara S, Baghani AN, Delikhoon M. Concentration and type of bioaerosols before and after conventional disinfection and sterilization procedures inside hospital operating rooms. Ecotoxicology and environmental safety. 2018;164:277-82.
8. Mirhoseini SH, Nikaeen M, Khanahmad H, Hatamzadeh M, Hassanzadeh A. Monitoring of airborne bacteria and aerosols in different wards of hospitals-Particle counting usefulness in investigation of airborne bacteria. Annals of Agricultural and Environmental Medicine. 2015;22(4).
9. Bisag A, Isabelli P, Laurita R, Bucci C, Capelli F, Dirani G, et al. Cold atmospheric plasma inactivation of aerosolized microdroplets containing bacteria and purified SARS‐CoV‐2 RNA to contrast airborne indoor transmission. Plasma Processes and Polymers. 2020;17(10):2000154.
10. Van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, et al. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. New England journal of medicine. 2020;382(16):1564-7.
11. Soltanian M, Mohajeri P, Najafi F, Kazemi S, Asadi F. Study of airborne bacterial density in surgery and infectious wards of hospitals affiliated with Kermakshah University Medical Science and its relationship with environmental factors. Iranian Journal of Epidemiology. 2018;13(4).
12. Memarzadeh F, Xu W, editors. Role of air changes per hour (ACH) in possible transmission of airborne infections. Building Simulation; 2012: Springer.
13. WHO. Indoor air quality: biological contaminants: report on a WHO meeting, Rautavaara, 29 August–2 September 1988: World Health Organization. Regional Office for Europe; 1990.
14. Veysi R, Heibati B, Jahangiri M, Kumar P, Latif MT, Karimi A. Indoor air quality-induced respiratory symptoms of a hospital staff in Iran. Environmental monitoring and assessment. 2019;191(2):50.
15. Bakhtiari R, Hadei M, Hopke PK, Shahsavani A, Rastkari N, Kermani M, et al. Investigation of in-cabin volatile organic compounds (VOCs) in taxis; influence of vehicle's age, model, fuel, and refueling. Environmental Pollution. 2018;237:348-55.
16. Neu HC. The crisis in antibiotic resistance. Science. 1992;257(5073):1064-73.
17. WHO. Global antimicrobial resistance surveillance system: manual for early implementation.[Google Scholar]. 2015.
18. Health UDo, Services H. Antibiotic resistance threats in the United States, 2013. Centers for disease control and prevention. 2013:1-113.
19. O’Neill J. Review on Antimicrobial Resistance Antimicrobial Resistance: Tackling a crisis for the health and wealth of nations. 2014. London: Wellcome Trust. 2018.
20. Montazer M, Soleimani N, Vahabi M, Abtahi M, Etemad K, Zendehdel R. Assessment of bacterial pathogens and their antibiotic resistance in the air of different wards of selected teaching hospitals in Tehran. Indian Journal of Occupational and Environmental Medicine. 2021;25(2):78.
21. Nunes ZG, Martins AS, Altoe ALF, Nishikawa MM, Leite MO, Aguiar PF, et al. Indoor air microbiological evaluation of offices, hospitals, industries, and shopping centers. Memórias do Instituto Oswaldo Cruz. 2005;100:351-7.
22. Napoli C, Tafuri S, Montenegro L, Cassano M, Notarnicola A, Lattarulo S, et al. Air sampling methods to evaluate microbial contamination in operating theatres: results of a comparative study in an orthopaedics department. Journal of Hospital Infection. 2012;80(2):128-32.
23. Kruczalak K, Olanczuk-Neyman K. Microorganisms in the Air Over Wastewater Treamtment Plants. Polish Journal of Environmental Studies. 2004;13(5).
24. Burkowska A, Kalwasińska A, Walczak M. Airborne mesophilic bacteria at the Ciechocinek health resort. Pol J Environ Stud. 2012;21(2):307-12.
25. Verde SC, Almeida SM, Matos J, Guerreiro D, Meneses M, Faria T, et al. Microbiological assessment of indoor air quality at different hospital sites. Research in Microbiology. 2015;166(7):557-63.
26. Yassin M, Almouqatea S. Assessment of airborne bacteria and fungi in an indoor and outdoor environment. International journal of environmental science & technology. 2010;7(3):535-44.
27. De la Maza LM, Pezzlo MT, Shigei JT, Tan GL, Peterson EM. Color atlas of medical bacteriology: ASM Press; 2013.
28. Holt JG, Krieg NR, Sneath PH. Bergey's manual of determinative bacterology. 1994.
29. Mousavi MS, Hadei M, Majlesi M, Hopke PK, Yarahmadi M, Emam B, et al. Investigating the effect of several factors on concentrations of bioaerosols in a well-ventilated hospital environment. Environmental monitoring and assessment. 2019;191(7):1-11.
30. Hwang SH, Park DU, Ha KC, Cho HW, Yoon CS. Airborne bacteria concentrations and related factors at university laboratories, hospital diagnostic laboratories and a biowaste site. Journal of clinical pathology. 2011;64(3):261-4.
31. Yousefzadeh A, Maleki A, Athar SD, Darvishi E, Ahmadi M, Mohammadi E, et al. Evaluation of bio-aerosols type, density, and modeling of dispersion in inside and outside of different wards of educational hospital. Environmental Science and Pollution Research. 2021:1-15.
32. Alsved M, Civilis A, Ekolind P, Tammelin A, Andersson AE, Jakobsson J, et al. Temperature-controlled airflow ventilation in operating rooms compared with laminar airflow and turbulent mixed airflow. Journal of Hospital Infection. 2018;98(2):181-90.
33. Yadav LR, Lingaraju K, Manjunath K, Raghu G, Kumar KS, Nagaraju G. Synergistic effect of MgO nanoparticles for electrochemical sensing, photocatalytic-dye degradation and antibacterial activity. Materials Research Express. 2017;4(2):025028.
34. Shokri S, Nikpey A, Varyani AS. Evaluation of hospital wards indoor air quality: the particles concentration. Journal of Air Pollution and Health. 2016;1(3):205-14.
35. Heo KJ, Lim CE, Kim HB, Lee BU. Effects of human activities on concentrations of culturable bioaerosols in indoor air environments. Journal of Aerosol Science. 2017;104:58-65.
36. Durack J, Boushey HA, Lynch SV. Airway microbiota and the implications of dysbiosis in asthma. Current allergy and asthma reports. 2016;16(8):52.
37. Bannerman TL, Rhoden DL, McAllister SK, Miller JM, Wilson LA. The source of coagulase-negative staphylococci in the Endophthalmitis Vitrectomy Study: a comparison of eyelid and intraocular isolates using pulsed-field gel electrophoresis. Archives of ophthalmology. 1997;115(3):357-61.
38. Engelhard D, Elishoov H, Strauss N, Naparstek E, Nagler A, Simhon A, et al. Nosocomial coagulase-negative staphylococcal infections in bone marrow transplantation recipients with central vein catheter: a 5-year prospective study. Transplantation. 1996;61(3):430-4.
39. Dinges MM, Orwin PM, Schlievert PM. Exotoxins of Staphylococcus aureus. Clinical microbiology reviews. 2000;13(1):16-34.
40. Archer GL, Climo MW. Antimicrobial susceptibility of coagulase-negative staphylococci. Antimicrobial agents and chemotherapy. 1994;38(10):2231-7.
41. Lowy FD. Staphylococcus aureus Infections. New England Journal of Medicine. 1998;339(8):520-32.
42. Caldwell CC, Chen Y, Goetzmann HS, Hao Y, Borchers MT, Hassett DJ, et al. Pseudomonas aeruginosa exotoxin pyocyanin causes cystic fibrosis airway pathogenesis. The American journal of pathology. 2009;175(6):2473-88.
43. Wu W, Jin Y, Bai F, Jin S. Pseudomonas aeruginosa. Molecular medical microbiology: Elsevier; 2015. p. 753-67.
44. McManus A, Mason A, McManus W, Pruitt B. Twenty-five year review of Pseudomonas aeruginosa bacteremia in a burn center. European journal of clinical microbiology. 1985;4(2):219-23.
45. Williams FN, Herndon DN, Hawkins HK, Lee JO, Cox RA, Kulp GA, et al. The leading causes of death after burn injury in a single pediatric burn center. Critical care. 2009;13(6):1-7.
46. Hardalo C, Edberg SC. Pseudomonas aeruginosa: assessment of risk from drinking water. Critical reviews in microbiology. 1997;23(1):47-75.
47. Blanc DS, Petignat C, Janin B, Bille J, Francioli P. Frequency and molecular diversity of Pseudomonas aeruginosa upon admission and during hospitalization: a prospective epidemiologic study. Clinical microbiology and infection. 1998;4(5):242-7.
48. Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW. Pseudomonas genomes: diverse and adaptable. FEMS microbiology reviews. 2011;35(4):652-80.
49. Keen III EF, Robinson BJ, Hospenthal DR, Aldous WK, Wolf SE, Chung KK, et al. Incidence and bacteriology of burn infections at a military burn center. Burns. 2010;36(4):461-8.
50. Bayat A, Shaaban H, Dodgson A, Dunn K. Implications for Burns Unit design following outbreak of multi-resistant Acinetobacter infection in ICU and Burns Unit. Burns. 2003;29(4):303-6.
51. Kanamori H, Parobek CM, Weber DJ, Van Duin D, Rutala WA, Cairns BA, et al. Next-generation sequencing and comparative analysis of sequential outbreaks caused by multidrug-resistant Acinetobacter baumannii at a large academic burn center. Antimicrobial agents and chemotherapy. 2015;60(3):1249-57.
52. Rungruanghiranya S, Somboonwit C, Kanchanapoom T. Acinetobacter infection in the intensive care unit. Journal of Infectious Diseases and Antimicrobial Agents. 2005;22(2):77-92.
53. Zarrilli R, Crispino M, Bagattini M, Barretta E, Di Popolo A, Triassi M, et al. Molecular epidemiology of sequential outbreaks of Acinetobacter baumannii in an intensive care unit shows the emergence of carbapenem resistance. Journal of clinical microbiology. 2004;42(3):946-53.
54. Wieland K, Chhatwal P, Vonberg R-P. Nosocomial outbreaks caused by Acinetobacter baumannii and Pseudomonas aeruginosa: Results of a systematic review. American journal of infection control. 2018;46(6):643-8.
55. Binder U, Lass-Flörl C. Epidemiology of invasive fungal infections in the mediterranean area. Mediterranean journal of hematology and infectious diseases. 2011;3(1).
56. Sudharsanam S, Swaminathan S, Ramalingam A, Thangavel G, Annamalai R, Steinberg R, et al. Characterization of indoor bioaerosols from a hospital ward in a tropical setting. African health sciences. 2012;12(2):217-25.
57. Mok T, Koehler A, Yu M, Ellis D, Johnson P, Wickham N. Fatal Penicillium citrinum pneumonia with pericarditis in a patient with acute leukemia. Journal of clinical microbiology. 1997;35(10):2654-6.
58. Paul D, Biswas K, Sengupta C, Sinha SN. Studies on environmental monitoring of aeromicroflora in a hospital at Kalyani, West Bengal, India. Front Environ Microbiol. 2015;1:47-50.
59. Park D-U, Yeom J-K, Lee WJ, Lee K-M. Assessment of the levels of airborne bacteria, gram-negative bacteria, and fungi in hospital lobbies. International journal of environmental research and public health. 2013;10(2):541-55.
60. Ghasemian A, Khodaparast S, Moghadam FS, Nojoomi F, Vardanjani HR. Types and levels of Bioaerosols in healthcare and community indoor settings in Iran. Avicenna Journal of Clinical Microbiology and Infection. 2016;4(1):41036-.
61. Scaltriti S, Cencetti S, Rovesti S, Marchesi I, Bargellini A, Borella P. Risk factors for particulate and microbial contamination of air in operating theatres. Journal of Hospital Infection. 2007;66(4):320-6.
62. Wan G-H, Chung F-F, Tang C-S. Long-term surveillance of air quality in medical center operating rooms. American journal of infection control. 2011;39(4):302-8.
63. Sautour M, Sixt N, Dalle F, l'Ollivier C, Calinon C, Fourquenet V, et al. Prospective survey of indoor fungal contamination in hospital during a period of building construction. Journal of Hospital infection. 2007;67(4):367-73.
64. Pastuszka J, Marchwinska-Wyrwal E, Wlazlo A. Bacterial aerosol in Silesian hospitals: Preliminary results. Polish Journal of Environmental Studies. 2005;14(6):883.
65. Augustowska M, Dutkiewicz J. Variability of airborne microflora in a hospital ward within a period of one year. Annals of Agricultural and Environmental Medicine. 2006;13(1):99-106.
66. Tsakris A, Poulou A, Kristo I, Pittaras T, Spanakis N, Pournaras S, et al. Large dissemination of VIM-2-metallo-β-lactamase-producing Pseudomonas aeruginosa strains causing health care-associated community-onset infections. Journal of clinical Microbiology. 2009;47(11):3524-9.
67. Tabassum S. Multidrug-resistant (MDR) Acinetobacter: a major Nosocomial pathogen challenging physicians. Bangladesh Journal of Medical Microbiology. 2007;1(2):65-8.
68. Wang A, Daneman N, Tan C, Brownstein JS, MacFadden DR. Evaluating the relationship between hospital antibiotic use and antibiotic resistance in common nosocomial pathogens. infection control & hospital epidemiology. 2017;38(12):1457-63.
69. Bialvaei AZ, Samadi Kafil H. Colistin, mechanisms and prevalence of resistance. Current medical research and opinion. 2015;31(4):707-21.
70. Kaye KS, Pogue JM, Tran TB, Nation RL, Li J. Agents of last resort: polymyxin resistance. Infectious Disease Clinics. 2016;30(2):391-414.
| Files | ||
| Issue | Vol 7 No 4 (2022): Autumn 2022 | |
| Section | Original Research | |
| DOI | https://doi.org/10.18502/japh.v7i4.11387 | |
| Keywords | ||
| Indoor air; Bioaerosols; Bacteria and fungi; Antibiotic resistance; Hospital wards | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Hosseini S, Kafil H, Mousavi S, Gholampour A. Seasonal and spatial variations of bioaerosols and antibiotic resistance bacteria in different wards of the hospital. JAPH. 2022;7(4):409-422.
