Using “health outcomes” as the basis for developing effective and sustainable hygiene interventions – is 2019 the time for a rethink?

This is a guest post by Prof Sally Bloomfield…

For many years, “5 log reduction” (LR) has been the gold standard for disinfectant efficacy despite absence of dose:response data linking it to clinical outcomes.  The family of EN tests now used to support claims for disinfectant products has its origins in the European Suspension Test (5LR, 5 mins, 5 test organisms) where 5 LR was probably chosen because it is the limit of sensitivity in an assay where, traditionally, the initial bioburden is 108 colony forming units.  For soap, detergent or dry wiping procedures, until recently their effectiveness has been assumed – possibly on the basis that they produce visible cleanliness? It is only recently that we have had access to efficacy data based on lab models.  A trial of EN 1699 handwashing test showed a mean 2.76 LR when hands contaminated with E .coli are washed with soap.

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Who’s going to go for GNBSI? A reflection from HIS 2018

I attended a thought-provoking session at the recent Healthcare Infection Society (HIS) conference in Liverpool on reducing GNBSI (you can download some of the speaker abstracts here). It seems that the hefty majority of E. coli BSIs are rooted in issues outwith the walls of acute hospitals. So the question is, who’s going to tackle these issues to prevent GNBSI? Who’s going to go for GNBSI (sorry, couldn’t resist another pop-culture reference to the ‘80s – who could forget ‘Going for Gold’ with Henry Kelly).

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Community MRSA preys on the poor and deprived

deprivation mrsa

As you can probably tell from the title, this post comes with a warning: it presents some rather “un-PC” data, but I’ll do my best to deliver it calmly and dispassionately! My old research team from KCL have just published a paper in PLOS Medicine on the association between social and material deprivation, and MRSA.

I’ve been interested in the dynamic between hospital-associated (HA) and community-associated (CA) MRSA for years (not least because it was the subject of my PhD thesis). I wrote a review several years ago on how community MRSA should be seen as a genotypic phenomenon with epidemiological implications. Using this framework, it is possible to get your head around CA strains of MRSA beginning to cause hospital-acquired infections. The aim of this study was to use a large collection of MRSA from across several regions of London to explore the transmission dynamics and epidemiological associations of HA and CA types of MRSA.

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You wait for ages, and then two come at once..


Sometimes waiting for research highlighting an issue that you know is a problem is like waiting for a bus..  Following on from my colleague @jonotter who last week posted about MRSA spread in nursing home settings, I was interested to read this new paper from the USA, published in the Journal of the American Geriatric Society. The study notes the high prevalence of Multi-Drug Resistant Organism (MDRO) carriage in nursing homes that was in excess of that in hospital settings and sought to determine any associations. The findings are interesting, if not surprising.

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Acinetobacter contamination: is anywhere safe?

A study from New York City describes an environmental survey of contamination with antibiotic-resistant Gram-negative bacteria on surfaces in the community. The authors hypothesise that resistant Gram-negatives could be carried by staff, patients and visitors beyond the confines of the hospital.

Almost 500 environemntal samples were collected from surfaces in the public areas of six hospitals and surrounding communities (<1 mile from the hospital) (443 samples), with a further surfaces from communities >1.5 miles from any hospital as a control (50 samples). A total of 70 GNR were identified (Figure), mostly fairly inoccousous species from a human disease viewpoint. However, some potential human pathogens were identified (Table).

Figure: breakdown of Gram-negative rods identified from surfaces in public areas of the hospital and surrounding community.GNR contam

Table: potential human pathogens identified from surfaces in public areas of the hospital and surrounding community.

n % Species
15 3.0 Acinetobacter baumannii
3 0.6 Citrobacter freundii
2 0.4 Escherichia coli
2 0.4 Stenotrophomonas maltophilia
1 0.2 Enterobacter cloacae

Some other important findings:

  • All of the A. baumannii isolates were resistant to ceftazidime, and one was resistant to imipenem (i.e. carbapenem-resistant). Eleven of the 15 were clonally related to one another and to a patient isolate from one of the hospitals.
  • One of the S. maltophilia isolates carried an integron-encoded VIM carbapenemase, which is potentially transmissible to other Gram-negative species (including Enterobacteriaceae).  
  • Each sample was cultured in an enrichment broth, and the broth was probed for the presence of a range of beta-lactamase genes (including ESBLs and carbapenemases). No beta-lactamases were detected (other than the S. maltophilia isolate). I suspect the picture would have been rather difference in New Dehli!
  • Although the survey included both surfaces in public areas of hospitals and in the community, it seems that most of the A. baumannii were identified on surfaces in the community.

So, is it a surprise to see environmental contamination with antibiotic-resistant Gram-negatvies on touch-surfaces in the community? Not really, A. baumannii in particular can survive on surfaces for ages, and ‘mimics’ Gram-positive bacteria in terms of its environmental longevity (i.e. months / years). That said, I performed a similar study looking for MRSA on touch surfaces in the community in London, and didn’t find any. More importantly, do we need to do anything about this? As the authors state, A. baumannii can be virtually impossible to eliminate from hospital surfaces without resorting to hydrogen peroxide vapour. So is it time to roll hydrogen peroxide vapour into your local Pizza Hut? Clearly not. You’d hope that cleaning and disinfection protocols, which should deal with this sort of contamination, are already established in these public places, but it would be prudent to reinforce these basic hygienic practices. Also, I agree with the authors that these findings represent and opportunity for the promotion of hand hygiene in the community.

The authors use strong words to describe NYC as ‘plagued’ with resistant Gram-negative bacteria, and a ‘dismal failure to control A. baumannii.’ If this epidemic continues, we can expect to see the focus of the problem – and the target for our interventions – shift from the acute hospital setting to encompass the community.

“Dirty money”: are you getting the right change from microbe-contaminated money?

SONY DSCThe phrase “Dirty money” may have different meanings for different people…but as far as microbiology is concerned….have you ever thought about what else you are getting back along with your change when you’re doing your shopping? I’m sure most of us are more concerned about getting the correct change rather than what microbes come for free with our change. For the few who have thought about what else they may be getting, I suspect that even fewer would answer: “pathogenic and sometimes multidrug-resistant bacteria, fungi and human parasites.”

In reality, we shouldn’t be surprised that bank notes and coins are contaminated with various bacteria. After all, we hardly expect them to be sterile. Our own hands are colonized with millions of bacteria and money is the most frequently passed item in the world. All studies that I have come across investigating bacterial contamination on money (paper notes or coins) have found a significant proportion to be contaminated (53-100%). I suspect that the microbiological techniques used in the various studies impacted on the results and my personal view is that the majority if not all money commonly exchanged between people will be contaminated.

The level of contamination and type or organisms on the money vary depending on the country, season, environmental conditions, type of money (paper vs coins), the type of material the money is made off, local community flora, the general hygiene level of the population and who is likely to be handling the money. Also dirty/damaged money (indication of frequent exchange) has been shown to be significantly more contaminated than clean and mint condition currency notes, and low denomination notes were more likely to be contaminated than higher denomination notes (probably reflecting frequency of use and socio-economic factors).1

The question to be asked, given the above, is: does it matter if money is contaminated with organisms? After all, this is not a new problem, as early as 1949, Nisbet and Skeoch2 have highlighted this issue. To answer this we need to look at a number of factors. These include: what type of organisms are on the money, how long are they able to survive and are they able to be transmitted to people and throughout the community from these contaminated currencies.  So let’s look at these factors in more detail:

1-  The type of organisms found on money

It is expected that bacteria will be found on bank notes and coins regardless of which country the money is from. Studies from Mexico, USA, India, Saudi Arabia, Nigeria, Kenya, Burma, China and Turkey to name few have all found significant contamination on their money. The type or bacteria found on money includes [deep breath]: E. coli, Vibrio spp., Klebsiella spp. including K. pneumoniae, Serratia spp., Enterobacter sp., Salmonella spp., Acinetobacter spp., Enterococcus spp., Staphylococcus including S. aureus, Bacillus spp., Staphylococcus epidermidis, Streptococcus pneumoniae, Proteus spp., Pseudomonas spp. including P. aeruginosa, Shigella spp.,  Corynebacterium, Lactobacillus spp., Burkholderia cepacia, Micrococcus spp. and Alcaligenes.

Looking at this list, it is clear that some of these bacteria are common environmental bacteria considered non-pathogenic. However, many are either potentially pathogenic or common human pathogens. For example, K. pneumoniae is a virulent organism and may cause both community and hospital-acquired infections. Even those organisms not commonly associated with disease in healthy hosts can cause clinically significant infections in immuno-compromised and hospitalised patients. These include even the natural inhabitants of the human skin such as Staphylococcus spp.

The story doesn’t end there since a number of studies have found multidrug-resistant and virulent strains on money. These have the potential to cause serious infections that are hard to treat, to disseminate in healthcare and community settings, and to spread antimicrobial resistant determinants to other bacteria. For example, one study3 found substantial S. aureus colonies on all 8 of the $1 and $5 bank notes collected from and around a University hospital in the USA. Tests for the presence of β-lactamases were positive and a significant number of the colonies showed resistance to erythromycin, tetracycline, chloramphenicol and vancomycin. Two isolates showed high-level resistance to vancomycin were found to harbour a plasmid conferring resistance to the drug. Taking that vancomycin is one of the last line antibiotics for treating multidrug resistant infection, this finding is very alarming. [A cautionary aside though – this work was published in the ‘Journal of Young Investigators’, so I can’t help thinking that the high-level resistance to vancomycin warrants some further investigation.] In another study,4 virulence genes were detected in S. aureus isolated from paper currency in India. Four virulence genes (cna, icaA, hlg and sdrE) were found in the isolates with 8 isolated possessing all 4 genes. Isolates harbouring these virulence genes showed higher antimicrobial resistance than those which didn’t contain these genes.

Bacteria are not the only organisms found on money. A number of studies show that fungal contamination of money is also common. Some of these are potentially pathogenic to humans and other life forms including plants. This may have implications far beyond human health to economic consequences if non-native pathogenic species are introduced into different countries via money carried during travel. For example, studies have found Penicillium spp., Aspergillus niger and A. flavus, Candida spp., Fusarium spp., Rhizopus spp., Alternaria spp, Trichoderma virie and white and brown mycelium on money.5.6 Some of these fungi can cause serious infections in humans and diseases in plants. In some countries, even parasites have been identified on bank notes. One study1 from Nigeria found that of the 250 currency notes collected from 4 major cities in the country, 21.6% were contaminated with enteric parasites including Ascaris lumbricoides, Enterobius vermicularis, Trichuris trichiura and Taenia spp. This parasite-contaminated currency was most frequently found in notes obtained from butchers and beggars. In another study,7 60.2% of 103 banknotes and 56.6% of 99 coins obtained from food-related workers in Egypt were found to be contaminated with one or more parasitic species. Protozoa were the predominant parasites, with microsporidia and Cryptosporidium spp. being the most prevalent.

2-  How long are organisms able to survive on money?

The survival of organisms on money depends on the type of the organism and their environmental resilience, the environmental conditions and the type of material the money is made of. Banknote paper is manufactured from cotton fibre, which gives the paper its strength and durability. Other additional elements maybe added to the cotton. Ploymer (or plastic) bank notes were developed to improve durability and incorporate some security features. One study8 investigated survival of MRSA, VRE and ESBL-producing E. coli on various bank notes from around the world including Euro, Croatian Kuna, Romanian Leu, Moroccan Dirham, US Dollar, Canadian Dollar, and the Indian Rupee. They found that the 3 organisms survived on the Romanian Leu for 6 hours after drying and VRE was isolated from the same notes after one day of drying. Other currencies had variable survival rates. Another in-vitro study4 found that S. aureus was able to survive on Indian paper currency for 8 days at room temperature.

3-  Are organisms able to be transmitted from money?

Transmission of organisms from money is highly significant if it occurs. For example, transmission from the community to the hospital setting is relevant because normally non-pathogenic, or opportunistic pathogens can have a serious clinical impact in such settings. On the other hand, transmission from the healthcare environment to the community is relevant when antimicrobial resistant strains (commonly found in hospitals) are involved. A study mentioned above,3 found vancomycin-resistant S. aureus on bank notes. The resistant determinant was located on a plasmid, hence easily transferrable. Notwithstanding my reservations about this study (see above), the interesting point about this investigation was the sources of the bank notes tested. These were collected from a University Hospital’s gift shop, a snack cart outside the hospital’s door and a convenience store near the hospital. The vancomycin-resistant isolates have likely originated from the hospital where the antibiotic is commonly used and had been transmitted to outside the hospital on money. In another study,8 investigators artificially contaminated bank notes of a number of countries with S. aureus and E. coli, and investigated transmission after 3 subjects with disinfected hands came into contact with these notes. Transmission was not successful for the Euro notes but transmission from US Dollars and the Romanian Leu was observed.

So we probably should be concerned with contamination of money especially when virulent, pathogenic or multidrug-resistant strains are concerned. Transmission between the healthcare and community settings can also have important implications. What’s the solution? Disinfection of the currencies in banks with UV light, supersonic or chemical means, producing bank notes from materials which inhibit bacterial growth or material with antimicrobial activity as well as replacement of traditional methods of trading with electronic money transactions,  have all been proposed. Personally I think for now, proper hand hygiene and overall hygiene remain the best ways to counter this problem.


  1. Uneke CJ, Ogbu O. Potential for parasite and bacteria transmission by paper currency in Nigeria. J Environ Health. 2007;69:54-60.
  2. Nisbet BR, Skeoch T. Bacteria on bank notes. Med Off. 1949;81:225.
  3. Bhalakia N. Isolation and plasmid analysis of vancomycin-resistant Staphylococcus aureus. J Young Investigators. 2005.
  4. Kumar JD, Negi YK, Gaur A, Khanna D. Detection of virulence genes in Staphylococcus aureus isolated from paper currency. Int J Infect Dis. 2009;13:e450-5
  5. Wanule D, Jalander V, Gachande BD, Sirsikar AN. Currency notes and coins as a possible source of transmitting fungal pathogens of man and plants. J Environ Sci Eng. 201;53:515-8.
  6. Kuria JK, Wahome RG, Jobalamin M, Kariuki SM. Profile of bacteria and fungi on money coins. East Afr Med J. 2009;86:151-5.
  7. Hassan A, Farouk H, Hassanein F, Abdul-Ghani R. Currency as a potential environmental vehicle for transmitting parasites among food-related workers in Alexandria, Egypt. Trans R Soc Trop Med Hyg. 201;105:519-24.
  8. Gedik H, Voss TA, Voss A. Money and transmission of bacteria. Antimicrob Resist Infect Control. 2013;2:22.

Photo credit: Sam Setzler.

Is “community-acquired” CDI real?

A recent high profile US study delved into apparent community-associated CDI cases to evaluate healthcare exposures. The study was large, evaluating almost 1000 cases of community-associated CDI from 8 US states. Only 177 (18%) of the 984 cases had no recent healthcare exposure (Figure 1). Furthermore, healthcare exposure was only evaluated for the 12 weeks prior to the positive specimen, so I would wager that a portion of this 18% acquired their infecting C. difficile in a healthcare facility.  CA-CDIFigure 1. Data demonstrating that most MRSA and CDI presenting on admission to hospital are likely to have been acquired in a healthcare facility.  

So, it seems that the majority of these cases are more likely to be community-onset, healthcare-acquired CDI, rather than community-acquired CDI. I feel like we’ve been here before. In the 1990s before the emergence of distinct strains of CA-MRSA, MRSA presenting at hospital admission was commonly termed ‘community-associated’ or, worse, ‘community-acquired’ when really it was MRSA that had been acquired in hospital during a previous stay (Figure 1). The situation has now changed since distinct MRSA clones have emerged that have the capacity to cause infection outside the healthcare environment.

Turning our attention to the UK, the mandatory report scheme classifies cases of CDI as ‘Trust-apportioned’ if the specimens is collected from patients who have been in hospital for four or more days (Figure 2). It is tempting to speculate that the cases of CDI that are non Trust-apportioned are CA-CDI. However, the definition for ‘Trust-apportioned’ does not account for previous healthcare contact, and the rate of Trust-apportioned and non-Trust-apportioned cases tracks so closely that, once again, these are likely to be healthcare-acquired CDI presenting on admission.

Slide1Figure 2. Number of cases of CDI in England through the mandatory reporting scheme, 2004-2013.

The epidemiology of C. difficile is fundamentally different to MRSA, in that healthy neonates typically have a high rate of C. difficile colonization. Thus, there is a ready reservoir for a low rate of genuinely community-acquired CDI. However, it seems to me that most “CA-CDI” reported thus are likely to be acquired in a healthcare facility and I have not seen any data to convince me that community-acquired CDI is increasing.

Article citation: Chitnis et al. Epidemiology of Community-Associated Clostridium difficile Infection, 2009 Through 2011. JAMA Intern Med 2013;173:1359-67.

What is “community-associated” MRSA?


A study in this month’s ICHE highlights the problems with using epidemiological definitions to designate MRSA as “nosocomial”. The study evaluated the impact of different numerators and denominators on the rate of apparent hospital-onset MRSA across 32 hospitals in California. The time that patients were hospitalized before being considered hospital-onset varied from 48 to more than three days and denominators were also variable. The particular combination of numerator and denominator used resulted in significant differences in the proportion of MRSA cases designated hospital-onset. This has clear implications for comparing rates of hospital-attributable MRSA in the era of public reporting.

The paper raises a wider problem of how to define healthcare- and community-associated MRSA in the era of CA-MRSA strains as a cause of healthcare-associated infections. A recent review in JHI (Otter & French 2012) made the case for a genotypic definition of CA-MRSA. Epidemiological definitions were useful for differentiating CA-MRSA and HA-MRSA strain types in the past. However, although HA-MRSA strain types are rarely transmitted in the community, CA-MRSA strains have now begun to be transmitted in healthcare facilities, so epidemiological definitions are breaking down. CA-MRSA are community strains of S. aureus that have acquired mecA. They are distinct from HA-MRSA and should be defined genetically. Carriage of the Panton-Valentine leukocidin (PVL) or antimicrobial susceptibly profiles can be useful indicators of CA-MRSA but should not be used to define them. For the full assessment of their epidemiology, MRSA infections should now be characterised as (1) caused by HA- or CA-MRSA strain types; (2) acquired in community or healthcare settings; and (3) onset in the community or healthcare facility. (This review made the 10 ten list of the JHI Editors choice and is freely available online here.)

Article citations:

Datta R, Kuo King M, Kim D et al. What Is Nosocomial? Large Variation in Hospital Choice of Numerators and Denominators Affects Rates of Hospital-Onset Methicillin-Resistant Staphylococcus aureus. Infect Control Hosp Epidemiol 2012; 33: 1166-9.

Otter JA, French GL. Community-associated meticillin-resistant Staphylococcus aureus: the case for a genotypic definition. J Hosp Infect 2012; 81: 143-8.