In this, the first of a series of mini blogs the Cupron team is going to be reviewing and breaking down a recent publication for you-the readers information. In other mini posts we are going to be introducing a number of key organisms from the environment as well as their pathogenic and resistance mechanisms. In this first post Dr Gadi Borkow is going to be reviewing a recent Nature paper from Tong et al who used a novel approach to look at what invasive fungi are circulating in the air of the hopsital by conducting large scale air capture and metagenome sequencing.

The notion that airborne transmission of bacteria, fungi and viruses, contributes significantly to hospital acquired infections (HAIs), has gained recognition in recent years (1-3). An airborne HAI refers to an infection which is contracted from microorganisms that have become airborne, usually from coughing, sneezing or some other form of aerosolization, including of dust particles and skin squamae carrying pathogenic microorganisms. But, may it be that the contribution of the airborne transmission of pathogens is significantly underestimated, as indicated by an article recently published (January 3rd 2017) in Nature, Science Reports (4).

The microbial hospital air environment, when sampled (it does not happen much), is mostly monitored using typical microbiological culture technologies. Microbial culture technologies for such a task have significant limitations. These include the need to isolate and grow each microorganism by using a different substrate, cultivation temperature and other different culture requirements. The article recently published (4) demonstrated that the diversity and bio-mass present in the clinical air environment of fungi and other microorganisms is significantly underrated. They did so by collecting air samples from 4 wards (Emergency Room (ER), Respiratory Intensive Care Unit (RICU), Surgical Intensive Care Unit (SICU), and Outpatient Department (OPD)) in a Beijing general hospital and analysing the airborne microorganisms present by using both typical culture-based technologies and a novel metagenomics sequencing analysis technology (5).

Aspergillus spp

The amount of air that was sampled reflected real respiratory activity, i.e. the air sample was set up at an average flow rate of 4L/min for 24 hours to imitate human breath. By the conventional culture-based technologies they found that the air was “quite clean”, i.e. they found only a very small amount of colony forming units of Micrococcus, Bacillus, Staphylococcus and Corynebacterium. In contrast, by using metagenomic sequencing they found 163 species of fungi, 74 species of Archaea, 1,826 species of bacteria and 117 species of virus in the RICU; 314 species of fungi, 106 species of Archaea, 2,170 species of bacteria and 211 species of virus in the SICU; 287 species of fungi, 72 species of Archaea, 1,597 species of bacteria and 60 species of virus in the ER; and 235 species of fungi, 98 species of Archaea, 2,261 species of bacteria and 81 species of virus in the OPD. The authors pointed out that many of the fungi identified are known nosocomial pathogens, such as aspergillus spp. 

It has been estimated that the airborne route of transmission accounts for between 10 and 20% of endemic nosocomial infections (6). Airborne transmission is known to be the route of infection for diseases such as tuberculosis and aspergillosis (1). It has been implicated in nosocomial outbreaks of S. aureus and MRSA in operating theatres, intensive care, burns and orthopaedic units (7-9). Aerosol transmission of other bacteria, such as Acinetobacter baumannii (10-12), Pseudomonas aeruginosa (13), and other Staphylococci spp (14) in hospital settings has also been reported. Similarly, airborne Scedosporium prolificans nosocomial infection was reported in Spain (15). Kelsen and McGuckin (16) found a significant correlation between the monthly rate of nosocomial respiratory tract infection and the average bacterial count in the ward air. But, can it be that the above reports are really only a “drop” in the number of HAI caused by transmission of pathogens through the air?

Tong et al recently published report (4), demonstrating the high amount and variety of bacterial and fungal pathogens present in the hospital air environment, is quite concerning. It indicates that the airborne transmission of nosocomial pathogens and their contribution to HAI is probably much underrated and unrecognised. Monitoring of bioburden in the hospital air is not routinely conducted and as demonstrated by Tong and his colleagues (4), the typical culture technologies significantly undervalue the diversity and biomass present in the hospital air environment.

What is the source of these microorganisms found in the air? Obviously sneezing, talking, movement, and contaminated air conditioners are a source of airborne nosocomial pathogens. But, I would like to shortly discuss a somewhat overlooked source of pathogens that are dispersed to the air in a hospital setting – the hospital beddings.

Textiles, under appropriate moisture and temperature conditions, are an excellent substrate for bacterial and fungal proliferation. Patients secrete bacteria all the time. When a bacterium is shed into a textile fabric between the patient and the bed, either in his pyjama or directly on the sheet, the moisture and temperature in the textile micro environment promotes its proliferation. Unfortunately, during bed making large quantities of microorganisms are released into the air. For example, Greene et al (17) found that the total viable count (TVC) in a patient room increased by 10 folds during vigorous bed making. They also found approximately two-fold increase in the TVC in the hallways following bed making, indicating that the bed making process dispersed microorganisms around the building. Shiomori et al (18) found a 25-26 fold increase (p<0.01) in the number of MRSA in the air immediately following bed making. The bacteria levels in the air fell back to background levels within 30 minutes. Accordingly, MRSA was detected following the bed making also on many surfaces, such as bed sheets, over bed tables, and patients’ clothing. Solberg (19) found strong positive correlation between the air counts of staphylococci and bed making. Similar results were reported by Noble and Davies (20) in patients following undressing and redressing.

Taken together, these studies strongly support the notion that disturbance of textiles in clinical settings contribute to the dispersal of pathogens to the air, which then settle down and contaminate the immediate and non-immediate environment. Healthcare workers and others that touch the aerosol contaminated surfaces can then transport nosocomial pathogens to patients by the contact route.

In conclusion, Tong et al (4) manuscript, together with the above mentioned reports, strongly indicate that the airborne route of pathogens transmissions that results in HAI is undervalued and overlooked.

References cited in this article 

  1. Beggs CB. The airborne transmission of infection in hospital buildings: fact or fiction? Indoor Built Environ. 2003;12:9-18.
  2. Eames, I., Tang, J. W., Li, Y. & Wilson, P. Airborne transmission of disease in hospitals. Journal of the Royal Society, Interface/the Royal Society 6 Suppl 6, S697–702 (2009).
  3. Clark, R. P. & de Calcina-Goff, M. L. Some aspects of the airborne transmission of infection. J R Soc Interface 6 Suppl 6, S767–782 (2009).
  4. Tong et al., High diversity of airborne fungi in the hospital environment as revealed by meta-sequencing based microbiome analysis. Sci Rep. 2017; 7:39606.
  5. Wenjun, Jiang et al. Optimized DNA extraction and metagenomic sequencing of airborne microbial communities. Nature protocol 10, 768–779 (2015).
  6. Brachman PS. Nosocomial respiratory infections. Prev Med. 1974;3:500-506
  7. Walter CW, Kundsin RB, Brubaker MM. The incidence of airborne wound infection during operation. JAMA. 1963;186:908-913.
  8. Farrington M, Ling J, Ling T, French GL. Outbreaks of infection with methicillin-resistant Staphylococcus aureus on neonatal and burns units of a new hospital. Epidemiol Infect. 1990;105:215-228.
  9. Rutula WA. Environmental study of a methicillin-resistant Staphylococcus aureus epidemic in a burn unit. J Clin Microbiol. 1983;18:683-688.
  10. Bernards AT, Frenay HM, Lim BT, Hendriks WD, Dijkshoorn L, van Boven CP. Methicillin-resistant Staphylococcus aureus and Acinetobacter baumannii: an unexpected difference in epidemiologic behavior. Am J Infect Control. 1998;26:544-551.
  11. Allen KD, Green HT. Hospital outbreak of multi-resistant Acinetobacter anitratus: an airborne mode of spread? J Hosp Infect. 1987;9:110-119.
  12. Cox RA, Conquest C, Mallaghan C, Marples RR. A major outbreak of methicillin-resistant Staphylococcus aureus caused by a new phage-type (EMRSA-16). J Hosp Infect. 1995;29:87-106.
  13. Mortimer EA, Jr., Wolinsky E, Gonzaga AJ, Rammelkamp CH, Jr. Role of airborne transmission in staphylococcal infections. Br Med J. 1966;1:319-322.
  14. Lidwell OM, Lowbury EJ, Whyte W, Blowers R, Stanley SJ, Lowe D. Effect of ultraclean air in operating rooms on deep sepsis in the joint after total hip or knee replacement: a randomised study. Br Med J (Clin Res Ed). 1982;285:10-14.
  15. Walter EA, Bowden RA. Infection in the bone marrow transplant recipient. Infect Dis Clin North Am. 1995;9:823-847.
  16. Kelsen SG, McGuckin M. The role of airborne bacteria in the contamination of fine particle neubilizers and the development of nosocomial pneumonia. Ann N Y Acad Sci. 1980;353:218-229.
  17. Greene VW, Bond RG, Michaelsen GS. Air handling systems must be planned to reduce the spread of infection. Mod Hosp. 1960;95:136-144.
  18. Shiomori T, Miyamoto H, Makishima K et al. Evaluation of bedmaking-related airborne and surface methicillin-resistant Staphylococcus aureus contamination. J Hosp Infect. 2002;50:30-35.
  19. Solberg CO. A study of carriers of Staphylococcus aureus with special regard to quantitative bacterial estimations. Acta Med Scand Suppl. 1965;436:1-96.
  20. Noble WC, Davies RR. Studies on the dispersal of Staphylococci. J Clin Pathol. 1965;18:16-19.

Image credits

Aspergillus spp taken from Mark Pilgrim here, Sneezing person taken from Imgur here, and bed making taken from Mosby educational video here.