March 2010
Preventing the spread of infectious diseases in
the European Union – targeted hygiene as a
framework for sustainable hygiene
March 2010
Authors:
Professor Sally F. Bloomfield1, Professor Martin Exner2, Professor Kumar
Jyoti Nath3, Mr John Pickup4, Professor Elizabeth A Scott5, Professor Carlo
Signorelli6
1London
School of Hygiene and Tropical Medicine, London, UK.
Institute for Hygiene and Public Health, Rheinische Friedrich-Wilhelms-Universität, Bonn,
Germany.
3Chairman, Sulabh International Social Service Organization, Calcutta, India.
4Consultant in Scientific Issues, Bridgnorth, Shropshire, UK.
5Director Of Undergraduate Program in Public Health, Co-director Simmons Center for Hygiene and
Health in Home and Community, Simmons College, Boston, MA USA.
6Department of Public Health, University of Parma, Italy.
2Director,
A report by the International Scientific Forum on Home Hygiene
2
This report was commissioned by Unilever who requested IFH to review the IFH
targeted approach to home hygiene as a framework for developing a sustainable
approach to hygiene. Most particularly IFH was asked to address the need to
balance concerns about environmental and human safety against recognition of the
important role of hygiene, and the need to ensure that EU citizens have access to
effective codes of hygiene practice, and hygiene products and processes, to protect
themselves against infectious disease.
The full report can be downloaded from the IFH website at: http://www.ifhhomehygiene.org/IntegratedCRD.nsf/f5236e2da2822fef8025750b000dc985/62812e8
ac19247fe802576c60054693f?OpenDocument
The International Scientific Forum on Home Hygiene (IFH; www.ifhhomehygiene.org) is a not for profit, non governmental organisation which was
established in 1997 to meet the need for an independent expert body who could
develop and promote a science-based approach to hygiene in home and everyday
life settings as a means to reduce the global burden of infectious diseases.
3
Contents
CONSENSUS STATEMENT
5
REPORT SUMMARY
8
1. INTRODUCTION
17
2. THE BURDEN OF HYGIENE-RELATED INFECTIOUS DISEASES IN THE
EUROPEAN UNION
18
2.1 INFECTIOUS INTESTINAL DISEASES
19
2.2 RESPIRATORY INFECTIONS
21
2.3 SKIN INFECTIONS - STAPHYLOCOCCUS AUREUS AND MRSA
21
2.4 FUNGAL INFECTIONS
22
2.5 ANTIBIOTIC RESISTANCE
23
2.6 PETS AND DOMESTIC ANIMALS AS A SOURCE OF INFECTION IN THE HOME
24
2.7 AT-RISK GROUPS IN THE HOME AND COMMUNITY
24
2.8 THE IMPACT OF SOCIAL DETERMINANTS ON THE SPREAD OF INFECTIOUS DISEASES
25
2.9 THE IMPACT OF SOCIAL TRENDS ON THE SPREAD OF INFECTIOUS DISEASES
26
2.10 CHRONIC SEQUELAE OF INFECTIOUS DISEASES
27
3. DEVELOPING A RISK-BASED APPROACH TO HOME HYGIENE
27
3.1 IDENTIFYING CRITICAL CONTROL POINTS IN THE CHAIN OF INFECTION TRANSMISSION
IN THE HOME
28
3.2 APPLYING HYGIENE PROCEDURES TO BREAK THE CHAIN OF INFECTION IN THE HOME
30
3.2.1 Hygiene procedures to prevent cross contamination during food
preparation
30
3.2.2 Hygiene procedures to prevent spread of norovirus between family
members
33
3.2.3 Hygiene procedures to prevent transmission of MRSA via clothing and
household linens
33
4. ESTABLISHING THE LINK BETWEEN TARGETED HYGIENE AND HEALTH
BENEFITS
36
5. IFH – DEVELOPING AND PROMOTING THE TARGETED APPROACH TO
HOME HYGIENE
37
6. SUSTAINABLE HYGIENE – THE KEY FACTORS
38
7. TARGETED HYGIENE – A FRAMEWORK FOR SUSTAINABLE HYGIENE IN
THE HOME AND EVERYDAY LIFE
42
8. CONCLUSIONS AND RECOMMENDATIONS
43
REFERENCES
46
4
CONSENSUS STATEMENT
Across Europe, infectious diseases continue to be a significant health and
economic burden:
 New pathogens (including antimicrobial resistant strains) such as MRSA,
avian and swine influenza and SARS are continually emerging.
 At the same time, social and demographic changes mean that people with
reduced immunity to infection, who are more vulnerable to infection, make up
an increasing proportion of the population (currently up to 20%).
 Infectious diseases can act as co-factors in other diseases that manifest at a
later date, such as cancer and chronic degenerative diseases, or as triggers
for development of allergic diseases such as asthma.
These ongoing changes demand new containment strategies, increasingly
involving the community as a whole. A number of interrelated factors need
consideration. For example:
 Whereas there has been a tendency to assume that common respiratory and
foodborne infections circulating in the community are a minor concern, in
reality the total burden in terms of absence from work and school is
considerable.
 Community and hospital care for vulnerable groups who become seriously ill,
or for those who develop ongoing sequelae are an additional healthcare cost.
 Technological and policy changes are being introduced to reduce costs
and/or environmental effects without regard to their potential impact on
infectious disease risks.
Governments are under considerable pressure to fund the level of healthcare that
people expect, and are now looking at disease prevention strategies as a means to
reduce health spending. Hygiene is increasingly recognised as a cost effective
means to reduce the burden of infectious diseases within the European Union
(EU). Increased homecare is one approach to reducing health spending, but, for this
to be effective, it must take account of the fact that gains are likely to be undermined
by inadequate infection control at home.
Targeted Hygiene & Sustainability
A parallel agenda of global importance is sustainable development, a concept that
refers to meeting the needs of society, and improving quality of life, in a way that
does not jeopardise the ability of future generations to meet theirs. Protecting health
by preventing infection is an intrinsically more sustainable approach than
treatment. Hygiene has the potential directly to improve sustainability because its
aim is to promote and protect health. However, hygiene measures must
themselves be sustainable, which means that issues such as the environment,
concerns about antibiotic resistance, and the much publicised notion that “we have
become too clean for our own good” need to be assessed and managed.
In response to the need for more emphasis on hygiene promotion in our homes and
everyday lives, the International Scientific Forum on Home Hygiene (IFH) has
developed a new approach to hygiene in the home and community, which is
designed to meet 21st century needs and support new community hygiene promotion
programmes. This approach is based on scientific data and risk assessment, and is
known as “targeted hygiene”. The aim of this approach is to maximise protection
against exposure to infectious microbes (germs) by breaking the chain of infection
5
transmission at critical points, before germs can spread any further. In some
situations, this is readily achieved by physical removal alone using cleaning products
such as hand soap, and rinsing with clean water. But in some situations, processes
that also inactivate germs, using heat or biocidal hygiene products and processes,
are needed to ensure effective and reliable results, and protection from infection. The
simple principle is that protecting the public from infection is not about unfocussed
daily or weekly deep down cleaning, but about acting where and when there is risk
of spread of infection.
Whilst targeted hygiene was originally developed by IFH as an effective approach to
hygiene practice in the home and community, it also provides an excellent framework
for building sustainability into hygiene. Through prudent and focussed use of hygiene
products and processes, it intrinsically minimises their life-cycle impacts, maximises
safety margins against any hazards and minimises any risks of encouraging the
development of antibiotic resistance through low level biocide exposure. It also
seeks, as far as possible, to sustain “normal” levels of exposure to the microbial flora
of our environment to the extent that is important to build a balanced immune system.
Developing and Promoting Hygiene within the European Union
Governmental bodies both at regional and national level are now working to develop
strategies that respond to the need for greater emphasis on hygiene. A key element
is the establishment of the European Centre for Disease Control and Prevention
(ECDC). The EU-funded “e-Bug” project http://www.e-bug.eu/ is also working to roll
out education on antibiotic resistance and hygiene at primary and secondary school
level across Europe. Recent years have seen significant investment in food hygiene,
handwashing and, most recently, respiratory hygiene campaigns aimed at reengaging the public and changing behaviour. IFH is working to support hygiene
promotion activities by producing home hygiene guidelines, training resources and
fact/advice sheets based on the targeted hygiene approach.
The Role of Biocidal Products
Sustainable use of biocidal hygiene products (i.e Biocidal products which act against
bacteria, viruses, fungi etc), in terms of life-cycle impacts and human and
environmental safety, can be assessed just as for other cleaning products and
ingredients. The Biocidal Products Directive (BPD) requires human health and
environmental risk assessments to be prepared in the coming years for all biocides in
relation to their uses. Individual biocidal products will also require authorisation under
BPD. Those not giving satisfactory risk assessments will be restricted or removed
from the market.
IFH is concerned that the environmental and safety assurance of hygiene
processes and products must not be addressed in isolation: the potential risks
must be balanced against EU citizens’ need for effective means of protecting
themselves against the real and continuing harm caused by infectious disease, which
may require the use of biocidal products or other biocidal processes involving e.g.
heat, UV irradiation, etc.
There is also in the EU an increasing focus on how to control antibiotic resistance,
and protect health with less reliance on antibiotics. As antibiotic resistance continues
to reduce our ability to treat infections, infection prevention through effective hygiene
becomes of even greater importance. By reducing the number of infections
through good hygiene, which in some cases requires the use of a biocidal
6
hygiene product, the number of courses of antibiotic treatment can be
reduced, which can in turn reduce the impact of antibiotic resistance.
Conclusions and Recommendations
One thing that is increasingly obvious is that if the burden of infectious diseases is to
be reduced in an economically sustainable manner, the responsibility must be shared
by the public. The key question is how do we achieve this? One problem that hinders
progress is that the responsibility for public health within Europe is structured such
that the separate aspects of home hygiene – food hygiene, hand washing, pandemic
flu preparedness, etc – are dealt with by separate agencies. If hygiene promotion is
to be successful in changing behaviour, we need an integrated family-centred
(rather than agency-convenient) approach to ensure a basic understanding of
infectious disease agents and how they spread , together with an
understanding of which people can adapt to meet changing needs. Hygiene
needs to be repositioned alongside other values of healthy living such as good diet
and exercise rather than something that is old fashioned, unnatural and potentially
unhealthy.
IFH concludes that if we are to sustain a high level of protection for EU citizens
against infectious disease, in the face of changing demographics and microbial
evolution, and at the same time derive real health benefits from investment in
hygiene promotion, the various stakeholders (public health bodies and health
professionals, environmentalists, immunologists, regulatory bodies and the
private sector) need to work together to develop an integrated approach to
public hygiene and hygiene promotion that takes account of and balances all
of these issues. We must build a more family-centred approach to hygiene that
recognises the importance of infectious disease prevention as a public health
measure and ensures the people of the EU have effective, safe and sustainable
means of achieving this.
Professor SF Bloomfield
Mr J Pickup
London School of Hygiene and Tropical
Medicine, London, UK
Consultant in Scientific Issues, Bridgnorth,
Shropshire, UK
Professor M Exner
Professor EA Scott
Institute for Hygiene and Public Health,
Rheinische Friedrich-Wilhelms-Universität,
Bonn, Germany
Simmons College, Boston, MA, USA
Professor KJ Nath
Professor C Signorelli
Dept of Public Health, University of Parma,
Parma, Italy
Sulabh International Social Service
Organization, Calcutta, India
International Scientific Forum on Home Hygiene. February 2010.
7
REPORT SUMMARY
In the late 1960s, the Surgeon General of the United States of America is alleged to
have said “it is time to close the book on infectious diseases, declare the war against
pestilence won, and shift national resources to such chronic problems as cancer and
heart disease". The last 40 years have shown that this optimism was misplaced;
infectious diseases are a continuing and significant burden on the health and
prosperity of the global community, not only in the developing world, but also in
developed world areas such as the European Union (EU).
Across the world, governments now recognise the need for more investment in
infectious disease surveillance and prevention strategies involving measures such as
immunisation and hygiene. Increasingly, this includes strategies to reduce the spread
of infection within the family at home, and in their everyday lives; there is a realisation
that, if the global burden of hygiene-related disease is to be reduced in a manner that
is economically sustainable it has to be a responsibility that is shared by the public. A
key response in Europe has been the establishment of the European Centre for
Disease Control and Prevention (ECDC).
A parallel agenda of global importance is sustainable development. Health is at the
heart of social sustainability, whilst poor health is a major drain on economic
sustainability. Hygiene seeks to promote and protect health by preventing infection
and is intrinsically a more sustainable approach than treatment. Of equal importance
is that hygiene measures must themselves be sustainable; hygiene needs to be
delivered in a way that is effective and efficient in social, economic and
environmental terms. In developing and promoting public hygiene strategies, various
potential impacts need to be assessed and managed appropriately:
 Life-cycle environmental impacts of hygiene procedures and products, including
the assurance of safety.
 Concerns that use of certain biocidal products could encourage the development
and spread of antibiotic resistance, and that widespread use of certain biocides
may lead to resistance to those biocides.
 The notion that lack of “exposure to infection” may be contributing to the
increased incidence of allergic diseases such as asthma and hay fever etc.
Currently, within the EU, various processes are being implemented that bear on the
above, notably initiatives on Sustainable Consumption and Production, the REACH
Regulation (Registration, Evaluation and Authorisation of Chemicals) and the
Biocidal Products Directive (BPD). There is also a focus on how to control antibiotic
resistance, and protect health with less reliance on antibiotics. We are also beginning
to gain a better understanding of the link between microbial exposure and
development of allergic diseases. Unfortunately, these issues – infectious diseases,
sustainability, environmental issues, product safety, antibiotic resistance and allergic
diseases – tend to be addressed in isolation, often by separate agencies, such that
there is relatively little opportunity to address and balance the incompatibilities
between them. IFH is concerned that, particularly in Northern Europe, environmental
and safety concerns, including about hygiene and hygiene products, have been the
major focus, with little attention paid to the need for effective means of reducing the
burden of infectious diseases. If we are to deliver maximum health benefit in a
manner that is sustainable, and engage the public in sharing responsibility for
reducing infectious diseases, it is of paramount importance that the benefits and risks
are properly weighed.
8
IFH has prepared this report in order to highlight the importance and potential of
“everyday life” hygiene to contribute to a more sustainable future by reducing the
social and economic burden of infectious disease, and to propose a strategy for
achieving this, which is itself sustainable. IFH has used the available scientific data to
formulate a risk-based or ‘targeted’ approach to hygiene in the home and community.
Whilst targeted hygiene, as outlined in this report, was adopted by IFH as a means to
develop an effective code of hygiene practice for the home, it also provides an
excellent framework for ensuring the hygiene measures used are themselves
sustainable.
The burden of hygiene-related infectious disease in the European Union
In the last 20 years or more, a number of events and/or trends can be identified that
have necessitated investment in public hygiene promotion campaigns. Many of these
derive from the constantly changing nature and range of pathogenic microbes to
which we are exposed. Despite significant investment, food-related, waterborne, and
non-food-related infectious intestinal diseases remain at unacceptably high levels. In
2003, the World Health Organisation assessed that about 40% of reported foodborne outbreaks in the European Region occur in private homes; in theory food
poisoning is 100% preventable through good food hygiene. Hygiene also plays a part
in limiting the spread of respiratory infections such as colds and influenza. The threat
posed by emerging diseases such as avian influenza, SARS and swine flu has
prompted the realisation that, in the event of a pandemic, hygiene is an important first
line of defence during the early critical period before mass vaccination becomes
available. Whereas there has been a tendency to assume that common
gastrointestinal, respiratory and skin infections circulating in the community are a
minor concern, the burden in terms of absence from work and school, together with
increased pressure on health services, is considerable. Data also increasingly show
that seemingly minor infectious diseases can act as co-factors in other diseases that
manifest at a later date, such as cancer and chronic degenerative diseases, or as
triggers for the development of allergic diseases.
A major focus within the EU is containing the threat from antibiotic resistance, which
increasingly undermines our ability to control infectious disease. Alongside prudent
antibiotic prescribing, hygiene is now seen as a key strategy for reducing the impact
of antibiotic resistance, by reducing the need for antibiotic prescribing and reducing
the circulation of antibiotic-resistant strains both in hospitals and the community.
The situation with regard to infectious disease is exacerbated by the ongoing social,
demographic and other changes that mean that people with reduced immunity to
infection now make up an increasing proportion of the global population - maybe as
much as 20%. The largest proportion are the elderly who have co-morbidities, which
can result in reduced immunity to infection. It also includes the very young, patients
discharged from hospital, taking immunosuppressive drugs or using invasive
systems, etc. Governments are under pressure to fund the level of healthcare that
people expect. Care of increasing numbers of patients in the community, including at
home, is one answer, but can be fatally undermined by inadequate infection control
in the home. Across Europe, there is an inequitable distribution of communicable
diseases. Populations at higher risk of infection coincide with those with a low level of
education, occupational class, or income level. In low income populations,
malnutrition also contributes to increased susceptibility to infection. These factors can
initiate a “vicious cycle” of infection predisposing to malnutrition and growth faltering,
which in turn leads to increased risk for further infection.
9
Technological advances are also being introduced to save costs or reduce
environmental impact without proper regard to their impact on infectious disease
risks. Trends in social behaviour and eating habits are increasing the risks of
transmission of infectious disease amongst family members at home. The demand
for different and “exotic foods” stimulates increasing movement of foodstuffs from
one region or country to another and creates problems in controlling microbial quality,
whilst increased population mobility means that new pathogens can be rapidly
spread into communities where there is little or no resistance.
The International Scientific Forum on Home Hygiene (IFH) – developing a riskbased, ‘targeted’ approach to home hygiene
The International Scientific Forum on Home Hygiene (IFH) is a global, professional,
non-government organisation which was established in 1997 to meet a growing need
to develop and promote an effective approach to home hygiene based on sound
scientific principles. To achieve this, IFH has drawn on the expanding volume of
scientific data, to formulate a risk-based approach to home hygiene. Risk
management is the standard approach for controlling microbial risks in food and
other manufacturing environments, and is becoming accepted as the optimum means
to prevent such risks in home and hospital settings. Applied to the home, this has
come to be known as “targeted hygiene”.
Targeted hygiene starts from the recognition that pathogens are introduced
continually into the home, by people (who may have an infection or may be
asymptomatic carriers), contaminated food and domestic animals, but also
sometimes in water or via the air. Additionally, sites where water accumulates such
as sinks, toilets, waste pipes, or items such as cleaning cloths readily support
microbial growth and can become primary reservoirs of infection; although species
are mostly those that represent a risk to vulnerable groups. In many homes, there will
also be at least one family member who is more susceptible to infection for one
reason or another. Within the home there is a chain of events (see Figure 1) that
results in transmission of infection from its source to a new recipient. The simple
principle is that, if we can break the chain of infection transmission, infection cannot
spread.
Figure 1: The chain of infection
10
A risk-based approach to hygiene examines each stage of the infection transmission
cycle in order to identify the “critical control points” for preventing spread. This allows
sites and surfaces to be ranked according to the level of risk; this indicates that in the
home the “critical points” are the hands, together with hand and food contact
surfaces, cleaning cloths and other cleaning utensils. These form the
“superhighways” for spreading pathogens around the home such that healthy family
members become exposed, directly or via the food they eat. Although this is a useful
“rule of thumb” ranking, it is not constant: in certain situations it can be quite different
and varies markedly at different times and according to circumstances. Toilets were
invented for controlling risks associated with human waste, but this does not mean
they are zero risk. They still have risks associated with them, which may become
critical at certain times e.g. when someone in the home has sickness or diarrhoea.
Targeted hygiene also means applying a suitable hygiene procedure at appropriate
times to interrupt the chain of infection. It is known that, even for healthy family
members, the infectious dose for some pathogens can be very small (10-100 viable
units or even less for some viruses) and that infection can result from direct transfer
from surfaces via hands or food to the mouth, nasal mucosa and conjunctiva. On this
basis IFH consider that, in risk situations, a 'hygienic cleaning' procedure should be
used to eliminate as many organisms as possible from critical surfaces. Hygienic
cleaning can be done in one of two ways:
 By mechanical removal involving soap or by detergent-based cleaning with
rinsing. The soap or detergent maximises detachment of microbes from surfaces.
To be effective this process must be accompanied with thorough rinsing under
running water that is disposed of safely from the home (e.g. into the public
wastewater system) such that pathogens cannot be further disseminated around
the home.
 By using a process or product that inactivates the pathogens in situ. Germ kill is
usually achieved using a disinfectant product or waterless hand rub, or by the
application of heat.
 Alternatively a combination of germ removal with kill can be used, e.g. clothing
and household linens should be laundered at 60ºC, but hygienic cleaning can
also be achieved using laundry wash and rinse cycles at 40ºC, using a bleachcontaining laundry product. Domestic dishwashers employ a combination of heat
and detergent-based cleaning with rinsing to decontaminate cooking and eating
utensils.
Even today, there is still a body of expert opinion that holds to the view that, in home
and everyday life hygiene, soap and water are all that is required, there is no need
for biocidal products. This recommendation makes the assumption that this process
is consistently effective as a “hygienic cleaning” process. The data presented in the
full IFH reportError! Bookmark not defined.1 clearly show that, in some situations, soap and
water alone are insufficient to eliminate contamination from critical control points and,
in reality, can be a very effective means of spreading contamination from one surface
to another. In these situations it is necessary to use a process, such as the
application of a biocidal product, waterless hand rub, or the use of heat, UV
irradiation or other process that inactivates microbes in situ. An argument put forward
against use of biocidal products or processes is that, although the germ removal by
cleaning alone is less than that which can be achieved by the use of biocidal
products and processes, it is sufficient to produce hands, surfaces and fabrics that
can be considered as safe i.e. for which the level of residual germs is no longer a
threat to health. This is despite the fact that data increasingly show that the infectious
dose for many common pathogens, particularly viruses, can be very small. It also
takes no account of the fact that a substantial proportion of “healthcare”, the care of
11
at-risk groups who are more susceptible, and to lower doses of pathogens, now
takes place in the home. The benefits of maximising germ removal from critical
surfaces have been demonstrated by application of quantitative risk modelling to
hand hygiene. This shows that although the benefit of using alcohol hand rubs, which
increase the log reduction on hands (as compared with handwashing with soap), is
not measurable in terms of the individual, it can translate into a significant decrease
in disease burden within a community.
Hygiene and sustainability – the key issues
Sustainability and sustainable development are concepts that refer to meeting the
needs of society, and improving quality of life, in a way that does not jeopardise the
ability of future generations to meet theirs. Hygiene has the potential directly to
improve sustainability because its aim is to promote and protect health. The hygiene
measures used, however, must themselves be not only safe, but sustainable.
Most aspects of the sustainability of hygiene measures, notably those involving
environmental impacts or safety, are typical of those arising in product and process
life cycles generally. A key tool is Life Cycle Assessment (LCA) which evaluates the
significant environmental impacts of products or processes in terms of inputs
required (such as materials, energy, water) and outputs (such as emissions and
waste). It is eminently applicable to evaluating the sustainability of hygiene products
(such as soaps, cleaners, disinfectants, paper towels) and procedures (such as
washing in hot water or heat sterilisation). However, while LCA can ascribe numerical
values with some accuracy to individual impacts from a particular process, the
relative importance of different types of impact is subjective and variable according to
prevailing conditions and even value judgements. In most cases, assessments are
concerned with comparing options, rather than ascribing exact values. Decisions
need to be based on comparison of alternative ways of delivering the same result.
Desired results must be defined, not only in terms of e.g. acceptable contamination
levels but also the reliability or likelihood with which they can be achieved. A sine qua
non is assurance of safety for people and the environment. This can be assessed
using well-established chemical risk assessment techniques, and manufacturers
have clear responsibilities to ensure the safety of their products. Such assessments
are now a formal requirement under the REACH legislation and/or the BPD.
Two specific possible long-term impacts, however, need additional consideration:
Sustainability of hygiene as an infection prevention measure
In delivering disease prevention through hygiene, on one hand, hygiene should
optimise protection against exposure to harmful microorganisms, but on the other, it
should minimise disruption of natural flora of the human body and the environment. A
particular concern, presently, is the so-called hygiene hypothesis. From a review of
the evidence IFH has concluded that, although there is good evidence that microbial
exposure in early childhood can protect against allergies, there is no evidence that
we need exposure to harmful microbes or to suffer a clinical infection. Nor is there
evidence that hygiene measures such as handwashing, food hygiene etc. are linked
to increased susceptibility to atopic disease. If this is the case, there is no conflict
between the goals of preventing infection and minimising allergies. A consensus is
now developing among experts that the answer lies in more fundamental changes in
lifestyle that have led to decreased exposure to certain microbial or other species,
such as helminths, that are important for development of immuno-regulatory
mechanisms. There is still much uncertainty as to which lifestyle factors are involved.
12
Although alarmist media coverage of the hygiene hypothesis has declined, a strong
‘collective mindset’ has become established that dirt is ‘healthy’ and hygiene
somehow ‘unnatural’. This has caused concern among health professionals that
everyday life hygiene behaviours, which are the foundation of public health, are being
undermined. Without clear evidence of the need for exposure to infectious doses of
pathogens to develop a healthy immune system, set against the firm knowledge that
germ exposure can cause disease, encouraging lower standards of hygiene in the
hope it might reduce the burden of allergic diseases would be a reckless and illadvised strategy with potential adverse consequences for public health. We are only
now beginning to understand how the normal resident and environmental microbial
flora interact within the body to maintain a healthy immune system.
Sustainability of the use of biocidal products and other biocidal processes
An implicit part of the IFH targeted hygiene approach is that, if we are to deliver
hygiene at the critical points, as needed to break the chain of infection, biocidal
products and processes are required in certain situations. Biocides, however, are not
a fundamentally distinct group of compounds; many substances have significant
biocidal action against microbes, but this does not per se mean they have very
different, or more adverse, safety and environmental profiles. Sustainable use of
biocides and biocidal products in terms of life-cycle impacts, and human and
environmental safety can thus be assessed and assured just as for other cleaning
products. The BPD requires human health and environmental risk assessments to be
prepared in the coming years for all biocides in relation to their uses. Individual
biocidal products will also require authorisation under BPD. Those not giving
satisfactory risk assessments will be restricted or removed from the market.
Once the safety of a biocidal product is assured as above, it could be argued that
sustainability improvement could then be addressed by reducing the life-cycle
impacts of the formulation and its ingredients. However, if all other things are equal, it
makes sense that ingredients with more favourable environmental and human safety
profiles should be preferred, as this could usefully increase margins of safety and
provide added assurance for the future against any hitherto unsuspected effects.
Favourable environmental safety characteristics include ready degradation or
removal during sewage treatment, and low lipophilicity and thus a low potential to
bioaccumulate. Ingredients with wide margins of safety, whose hazards are well
understood and characterised, should be preferred to those where there is greater
uncertainty.
A further question is whether disinfectant usage is encouraging the emergence of
antibiotic-resistant 'superbugs'. From literature reviews in 2002 and 2004, IFH
concluded that, although laboratory experiments demonstrate links between biocide
exposure and increased resistance to antimicrobials, there is currently no evidence
that biocide use in the community is linked to emergence and spread of antibiotic
resistance; antibiotic misuse is the most significant causative factor. These
conclusions differ in emphasis from those expressed in a 2009 report from the EU
Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR) that
concluded that current scientific evidence does indicate that use of certain types of
active substances in biocidal products in various settings may contribute to increased
occurrence of antibiotic resistance. Overall, however, both the IFH and SCENIHR
reports stress the important role of biocides in the control of microbes in a variety of
applications. Both reports caution that biocides are a precious resource that must be
managed through appropriate and prudent use. IFH further concludes, as have
others, that as antibiotic resistance continues to reduce our ability to treat infections,
infection prevention through hygiene in hospitals and the community becomes of
even greater importance. By reducing the number of infections through effective
13
hygiene, which in some cases may require the use of a biocidal hygiene product, the
number of antibiotic courses prescribed can be lowered, which can in turn reduce the
impact of antibiotic resistance.
IFH has also addressed concerns that widespread biocide usage may cause
resistance to those biocides. After review, IFH has concluded that, although
laboratory studies provide evidence that prolonged exposure to low levels of certain
biocides can be associated with reduced microbial susceptibility to those biocides,
there is currently no evidence that biocide usage at its current levels in domestic and
other settings compromises effectiveness of hygiene procedures under use
conditions. Again, however, prudent use is the sustainable approach.
Targeted hygiene – a framework for sustainable hygiene in the home and
everyday life
The essence of targeted hygiene is that it works to ensure that, as far as possible,
hygiene interventions are focussed on situations where they maximise protection
against infection, rather than in situations where there is little risk. Whilst targeted
hygiene was originally adopted by IFH as a means to develop an effective code of
hygiene practice for the home, it also provides a framework for sustainable hygiene
because, through prudent and focussed use of hygiene products and processes, it:
 minimises the life-cycle impacts of hygiene processes, and maximises safety
margins against any hazards of their use
 minimises any risks of development of antibiotic resistance from exposure to low
level biocide residues
 seeks, as far as possible, to sustain “normal” levels of exposure to the microbial
flora of our environment to the extent that it is important to build a balanced
immune system.
In developing and/or selecting biocidal products or processes for use within a
targeted approach to hygiene, a number of issues need to be considered in order to
satisfy the above criteria and thereby maximise sustainability:
 We need to select the most appropriate biocides. This means selecting, as far as
possible:
 Biocides that are effective against the spectrum of organisms that represent a
risk in the particular situation in which it will be used.
 Biocides that have a rapid biocidal action in order to break the chain of infection
transmission (e.g. on hands, hand contact and food contact surfaces) with
minimum delay. Note: In some situations (e.g. controlling growth of potentially
harmful fungal contamination on damp surfaces such as tiled walls) a sustained
biostatic (growth inhibiting) action is appropriate
 Biocides and biocidal products that are not environmentally persistent or
bioaccumulative, for which potential adverse effects are well characterised and
understood, and where there are good margins of safety.
 We need to think more innovatively about delivery of hygiene. For example, can
we use our growing understanding of microbial attachment and detachment to
better design products and processes that combine prevention of germ
attachment, germ removal and control (germ kill) to deliver the necessary
hygiene result in a more sustainable way?
 We need to ensure that, as far as possible, we use “doses” of biocidal products
and processes (cleaning, biocidal and physical agents either singly alone or in
combination) that achieve hygienic cleaning of sites, surfaces, fabrics etc with
minimum use of water, power or chemicals. This in turn depends on developing
14

in use/field test models that more closely mimic conditions of use and allow
comparison of processes that involve germ removal as well as germ kill.
We need to think more holistically about delivery of hygiene in relation to
sustainability i.e. in developing and selecting the most suitable hygienic cleaning
method for any situation, we need to consider ALL factors (infectious disease
prevention, environmental and human safety, sustainability, antimicrobial
resistance, the immune system) rather than each factor in isolation.
The key to targeted hygiene is that good hygiene is not a 'once weekly deep down
clean': it needs to be an ongoing part of our daily lives such that appropriate
measures are targeted where and when necessary. Hygiene requires well-formulated
products, which deliver “hygienic cleaning” through germ removal or kill (or
combinations of processes) in order to break the chain of infection transmission.
Targeted hygiene will not be delivered by adding arbitrary amounts of biocides to
cleaning products in order to give a “bit of extra hygiene”.
Conclusions and Recommendations
In the last 20 years we have seen significant investment across Europe in controlling
and reducing the burden of infectious diseases, not only with the establishment of
ECDC, but also through national hygiene promotion programmes. In the UK, for
example, there has been an extensive programme to promote food hygiene at home.
In recent months we have seen investment in promotion of hand hygiene as a means
to mitigate the spread of the 2009 pandemic H1N1 influenza strain. IFH believes
however that the impact of hygiene promotion programmes on the public is being
weakened by the fact that the different aspects of hygiene are dealt with by separate
agencies. This means that the information that the family receives is fragmented and
largely rule-based. If things are to improve we must recognise that fragmented, rulebased instructions are not enough to meet the challenges we face. At the very least
we must ensure that the principles of infectious disease transmission and hygiene
are part of the school curriculum. In line with this, the EU-funded e-Bug project
(http://www.e-bug.eu/) is working to roll out education on antibiotic resistance and
hygiene at primary and secondary school level across Europe.
In this review the targeted- or risk-based approach to home hygiene, as developed
by the IFH, is outlined. The aim of this approach is to maximise protection against
exposure to infectious agents by breaking the chain of infection transmission. This is
achieved by the timely application of processes that eliminate or control microbial
contamination at critical points in the chain of transmission. If we are to deliver
“hygiene” (i.e. a level of contamination not harmful to health) at the critical points,
targeted hygiene requires the use of not only cleaning but also, in certain situations,
biocidal hygiene products and processes (either alone or in combination with germ
removal).
In developing and promoting hygiene practice, the issue of sustainability must also
be addressed. The report1 shows that the IFH targeted hygiene approach provides a
framework for building sustainability into hygiene because it minimises the life-cycle
impacts of hygiene processes, maximises safety margins against any hazards of
their use, and minimises any risks of the development antibiotic resistance from
exposure to biocides. It also looks to sustain “normal” interaction with the microbial
flora of our environment.
If we are to sustain a high level of protection for EU citizens against infectious
disease, in the face of changing demographics and microbial evolution, and derive
15
real health benefits from investment in hygiene promotion, IFH concludes that the
various stakeholders need to work together to address the following issues:
 The public must be engaged so that they share the burden and bring the unique
contribution that only they can make, through good hygiene in the home and
community. To achieve this, hygiene promotion strategies should:
 Be family-centred rather than agency-oriented, building on what people
understand, know and need to know.
 Not only change behaviour but also engender more positive attitudes to hygiene
as a means to achieve health, well being and prosperity.
 Give people the opportunity for a more balanced understanding of how to protect
themselves from infectious diseases in a world where they also have conflicting
concerns about issues such as allergic diseases and the environment.
 The risk-based ‘targeted’ approach to home hygiene should be adopted as the
basis for development of hygiene codes for the home and everyday life since it
offers both the most effective approach to breaking the chain of infection
transmission as well as an intrinsically more sustainable framework.
 Within the targeted approach to home hygiene, we need not only cleaning
products that facilitate germ removal, but also biocidal products and processes
are required. These provide germ inactivation, alone or in combination with
cleaning processes, which can be used to ensure the elimination of pathogenic
contamination from critical control points when used by consumers.
 The selection of products or processes for hygiene tasks should be based on
assessment of their sustainability and safety as well as reliability in delivering the
required result. This can be assessed using well-established tools such as lifecycle assessment and risk assessment. Additional potential impacts on bacterial
resistance and immunity need to be considered and any risks weighed against
the risks and impacts of infectious disease, and managed appropriately.
 The European regulatory process should:
 Encourage and facilitate the development and marketing of products and
processes that deliver hygiene in a safe and sustainable way, using
combinations of germ removal and germ kill as appropriate.
 Encourage manufacturers to develop test methods that model use conditions
in order to ensure optimum efficacy and reliability with minimum impact
throughout the life cycle.
16
1. INTRODUCTION
In the late 1960s, the Surgeon General of the United States of America is alleged to
have said “it is time to close the book on infectious diseases, declare the war against
pestilence won, and shift national resources to such chronic problems as cancer and
heart disease". The last 40 years have shown that this optimism was misplaced;
infectious diseases are a continuing and significant burden on the health and
prosperity of the global community, not only in the developing world but also in
developed world communities such as the European Union (EU).
Across the world, governments now recognise the need for more investment in
disease prevention strategies involving measures such as immunisation and hygiene.
Increasingly, this includes strategies to reduce the spread of infection within the
family at home, and in their everyday lives; there is a realisation that, if the global
burden of hygiene-related disease is to be reduced in a manner that is economically
sustainable, it has to be a responsibility that is shared by the public. This is not about
shifting blame, it is about facing reality. Recent years have seen significant
investment in food hygiene, handwashing, and most recently, respiratory hygiene
campaigns aimed at re-engaging the public and changing behaviour.
A parallel agenda of global importance is sustainable development. Health is a
fundamental human need. Improving health and life expectancy is one of the
fundamental goals of society. Health is also at the heart of social sustainability.
Conversely, poor health is a major drain on economic sustainability. Hygiene seeks
to promote and protect health by prevention of infection. Prevention is intrinsically a
more sustainable approach than treatment, which is not always successful.
Of equal importance is that hygiene measures to protect health must themselves be
sustainable; hygiene needs to be delivered in a way that is effective and efficient in
social, economic and environmental terms. In developing and promoting public
hygiene strategies, various potential impacts need to be assessed and managed
appropriately:
 The life-cycle environmental impacts of hygiene procedures and products,
including the proper assurance of safety.
 Concerns that the use of certain biocidal products could encourage development
and spread of antibiotic resistance, and that use of biocides may lead to
resistance to those biocides.
 The notion, based upon the hygiene hypothesis, that lack of “exposure to
“infection” may be contributing to increased incidence of allergic diseases such
as asthma, hay fever etc – i.e. that we are “being too clean”.
Currently, within the EU, various processes are being implemented that bear on the
above, notably initiatives on Sustainable Consumption and Production, the REACH
Regulation (Registration, Evaluation and Authorisation of Chemicals) and the
Biocidal Products Directive. There is also increasing focus on how to control the
development of antibiotic resistance, and how to protect health with less reliance of
antibiotics as a routine. We will also gain a better understanding of the link between
microbial exposure and the development of allergic diseases. Unfortunately, each of
these issues – infectious diseases, sustainability, environmental issues, product
safety, antibiotic resistance and allergic diseases – tends to be addressed in
isolation, often by separate agencies, such that there is relatively little opportunity to
address and balance the incompatibilities and tensions between them. If we are to
deliver maximum health benefit in a manner that is sustainable and to engage the
public in sharing the responsibility for reducing the burden of infectious disease, and
17
its social and economic impacts, it is of paramount importance that the benefits and
risks of the various measures must be properly weighed.
The purpose of this report is to highlight the importance and potential of “everyday
life” hygiene to contribute to a more sustainable future by reducing the social and
economic burden of infectious diseases, and to propose a strategy for achieving this
that is itself sustainable. The report has been prepared by the International Scientific
Forum on Home Hygiene (IFH). IFH is a global, professional, non-government
organisation which was established in 1997 to develop and promote an approach to
home hygiene based on sound scientific principles. IFH has used the growing volume
of scientific data to formulate a risk-based or ‘targeted’ approach to hygiene in the
home and community that can help maximise the protection against infection. Whilst
targeted hygiene was originally adopted by IFH as a means to develop an effective
code of hygiene practice for the home, it also, as outlined in this report, provides a
framework for ensuring sustainability of hygiene and hygiene products.
2. THE
BURDEN OF HYGIENE-RELATED INFECTIOUS DISEASES IN THE
EUROPEAN
UNION
A significant proportion of the infectious disease burden in the EU is caused by
diseases that are hygiene-related (i.e. transmitted via food, water, faecal and other
waste material, hands and other surfaces, and via the air). The burden of
communicable diseases in Europe is summarised in a series of European Centre for
Disease Control and Prevention (ECDC) annual reports.1
In the last 20 years or more, a number of events and/or trends can be identified that
have necessitated investment in public hygiene promotion campaigns. These derive
from the constantly changing nature and range of pathogenic micro-organisms to
which we are being exposed; experience now shows that as soon as we begin to get
one pathogen under control another emerges. Indications are that poor hygiene has
been a contributory factor in the global spread of pathogens such as norovirus,
Helicobacter pylori (H. pylori), Staphylococcus aureus, Legionella and
Campylobacter, pathogens that were largely unheard of before the 1980s. The threat
posed by emerging diseases such as avian influenza, SARS and swine flu has
prompted the realisation that, in the event of a pandemic, hygiene is an important first
line of defence during the early critical period before mass vaccination becomes
available.
Some of these emerging infections have been caused by species that are normally
present in the environment, but have become pathogenic as a result of changes in
technology (food technology, building design and operation etc) or societal changes.
Other emerging infections have involved new strains of already known and wellestablished pathogens. The most recent examples include SARS, avian and swine
flu, and community-acquired strains of methicillin resistant Staphylococcus aureus
(MRSA). Some of these are a concern because they have developed altered or
enhanced virulence properties (e.g. they have acquired the ability to produce a
specific toxin, or enhanced levels of toxin). Others are a problem because they have
become resistant to the action of antibiotics. Molecular and other improved
technologies for detecting pathogens now show the extent to which viral agents such
as the norovirus, rotavirus and adenovirus are a cause of community-acquired
infections. Since viral infections are not treatable by antibiotics, this reinforces the
need for prevention through hygiene.
18
The changing “hygiene climate” in the home and community not only reflects the
constantly changing nature and range of pathogenic micro-organisms to which we
are exposed, but also the social, demographic and other changes that are occurring
within the EU which affect our resistance to infection. Trends in hygiene-related
diseases are reviewed in a 2009 IFH report.2 The main findings are reviewed in this
section.
2.1 INFECTIOUS INTESTINAL DISEASES
Despite significant investment at all levels, food-related, waterborne, and other nonfood-related infectious intestinal diseases (IID) remain at unacceptably high levels.
This is despite the efforts of food producers to ensure the safety of the food chain. A
report by the European Food Safety Authority (EFSA) and the ECDC in 2007,
estimated that one third of populations in developed countries are affected by foodborne diseases every year.3 The 2003 World Health Organisation (WHO) report
concluded that about 40% of reported food-borne outbreaks in the WHO European
Region occur in private homes.4 Preventing food-related infections relies on a
combination of good hygiene practices during food preparation, cooking and storage;
in theory food poisoning is 100% preventable. The potential for food poisoning at
home is indicated by the prevalence of food-related pathogens in products purchased
from retail premises. A 2009 EFSA report based on data reported back from EU
countries in 20075 showed that Campylobacter was mostly found in raw poultry meat
with an average of 26% of samples showing contamination. Poultry and pig meat
were reported as the foods most frequently associated with Salmonella; on average
5.5% of fresh poultry meat samples was found to be contaminated. Chapman et al.
showed that 0.4-0.8% of meat products purchased from butchers in the United
Kingdom (UK) were positive for Escherichia coli O157. 6
It is now increasingly recognised that intestinal infections circulating in the community
are by no means all foodborne; a substantial proportion of the total IID burden in the
community is due to person-to-person spread within households, particularly for viral
infections such as norovirus. Person-to-person transmission in the home can occur
by direct hand-to-mouth transfer, via food prepared in the home by an infected
person, or by transmission due to aerosolised particles resulting from vomiting or
fluid diarrhoea. Apart from transmission by inhalation of airborne particles, these
infections are preventable by good hygiene practice. National surveillance systems
mostly focus on food-borne disease which means that non-food-borne cases are
under-reported. The 2003 WHO report stated that, of the total outbreaks reported in
Europe during 1999 and 2000, 60 and 69%, respectively, were due to person-toperson rather than food-borne transmission.4 A study of UK outbreaks7 suggested
that 19% of Salmonella outbreaks and more than half of E. coli O157 outbreaks are
transmitted by non-food-borne routes. Two large community studies have been
carried out in Europe, one in the UK8 and the other in The Netherlands.9 The UK
study, carried out between 1993 and 1996, estimated that only 1 in 136 cases of
gastrointestinal illness is detected by surveillance and that, for every one reported
case of Campylobacter, Salmonella, rotavirus and norovirus, another 7.6, 3.2, 35 and
1,562 cases, respectively, occur in the community. From this, it is possible to
estimate the true number of infections occurring in the community (Table 1).
19
Table 1 – Estimated number of cases of infectious gastrointestinal disease in
England and Wales associated with Campylobacter, Salmonella, rotavirus and
norovirus
Organism
Number of laboratory
reports from faecal
isolates in 2005
Campylobacter 42,679
Salmonella
11,191
Rotavirus
13,306
Norovirus
2,607
Ratio of actual
reported cases
7.6
3.2
35
1562
Estimated number of
cases in the
community
324,360
47,763
567,790
4,072,734
Indications are that norovirus is now the most significant cause of IID in the
developed world.10 It is thought that norovirus strains now circulating are more
“virulent” and more easily spread from person-to-person via hands and surfaces or
during food-handling.10 Rotavirus is the leading cause of gastroenteritis in children
under 5 years of age.11
The UK study indicated that as many as 1 in 5 people in the UK population develop
IID each year (an estimated 9.4 million cases) of which about 50% are non-foodborne.8,12 In The Netherlands9 it was estimated that about 1 in 3.5 people experience
a bout of IID each year. A 2007 report of food- and non–food-borne outbreaks in
Germany13 suggested that the most common settings for outbreaks are households
(53%). Of 14,566 outbreaks, 5,400 were indicated as person-to person transmission,
1637 to food, and 85 to water.
Clostridium difficile-associated intestinal disease occurs with increasing frequency in
the community, where it most usually affects home-based patients undergoing
antibiotic or other treatment, but occasionally affects otherwise healthy individuals.14
Over 80% of cases are in the over-65 age group. Carriage rates in healthy people in
the community may be around 3% to 5%.15, 16 Although there are no data to indicate
what proportion are carriers of toxin-producing strains, indications are that the
numbers that are toxin producers has increased.17, 18 It is estimated that, more than
13,000 cases of community-acquired infection occur each year in the UK.16 Data
from Sweden indicate that 42% of cases of C. difficile infection occur in the
community.19 In Ireland, 11% of cases presenting with C. difficile-related diarrhoea
had no hospitalisation within the previous 60 days.20
In general, it is assumed that community water supplies in developed countries are
safe with respect to microbial risks. This is not necessarily the case,21 particularly in
regions of Europe where political and economic upheaval have led to infrastructure
deterioration. Additionally, whereas towns and cities of Europe are generally well
supplied with running water, many rural populations still rely on small private
supplies, where contamination risks are higher. Water-borne disease is reviewed in
more detail in a 2005 IFH report.22 Despite the fact that water quality standards are
high in most European countries, outbreaks of water-borne disease continue to
occur. For 1986–1996, data from 17 countries in the European region indicated a
total of 2,567,210 cases of IID, 2% of which were linked to drinking water. It appears
that outbreaks of water-borne diseases have been increasing in countries that have
experienced recent breakdown in infrastructure, although reliable data on water
quality and incidence of disease are lacking. In situations where water quality is
consistently poor, or in emergency situations (e.g. where outbreaks of
Cryptosporidium occur as a result of breakdowns in the water treatment or
20
distribution system) point-of-use water treatment within the home becomes the
responsibility of the family, if gastro-intestinal infections are to be prevented.
2.2 RESPIRATORY INFECTIONS
Recent emergent respiratory tract (RT) pathogens include viruses such as SARS,
avian and swine flu. Until quite recently, it was generally thought that transmission of
RT infections was almost entirely by the air-borne route, involving aerosols (small
<10
droplet nuclei) or droplets generated by coughing and sneezing.23 Although,
supporting data related to colds have been available for some time, it is only in the
last 5 to 6 years that there has been any real awareness that not just coughs and
sneezes, but also hand and surface hygiene play a part in reducing the spread of not
only colds but also influenza.24, 25 Although colds are generally mild and self-limiting,
secondary infections produce complications, such as otitis media, sinusitis, or lower
respiratory infections such as pneumonia, which require hospitalisation and have
high risk of mortality, particularly in the elderly and other risk groups.26 Several
studies have demonstrated that colds are also a trigger for asthma.27 Influenza, is a
more serious RT illness which can cause hospitalisation and death, the risks being
highest among persons aged >65 years, children aged <2 years, and persons who
have medical conditions (e.g. diabetes, chronic lung disease).28,29 Colds and
influenza must also be considered in terms of days absent from work and school, and
costs to healthcare services.29 The incidence of influenza in EU countries is reviewed
in the 2009 ECDC communicable diseases report.1
A major concern is the emergence of novel subtypes capable of causing an influenza
epidemic or pandemic.30 Since new strains arise every 1 to 2 years, there is no
lasting immunity against influenza, neither after infection nor after vaccination.30
Across the world, preparations for the next influenza pandemic started in 2005.
Hygiene is seen as being important as a first line of defence to mitigate spread during
the early critical period before mass vaccination becomes available. 'Global
Preparedness' means that respiratory hygiene needs to become part of our daily
lives already before such an event. If the public are to play their part, however,
knowledge and awareness of these personal measures needs to be improved.31
Legionella infections are also known to be domestically acquired.32 In Germany 47%
of notified infections are estimated to be acquired at home.33 Surveys in Italian
houses indicate that Legionella contamination of domestic hot water ranges from
22.6% of samples from a countrywide investigation34 to 41.9% of samples obtained
from 59 apartments in Bologna.35
2.3 SKIN INFECTIONS - STAPHYLOCOCCUS AUREUS AND MRSA
Skin and wound infections are common in the home and community. S. aureus is the
most common cause of skin and soft tissue infections, which are mostly self-limiting,
but a small proportion of cases leads to severe invasive bacteraemias or
pneumonia.36 Between 30% and 60% of the general population37 carry S. aureus as
part of their normal body flora38. A UK study39 indicates a major increase in
pathogenic community-onset staphylococcal disease over the past 15 years. It was
found that hospital admission rates for staphylococcal septicemia, pneumonia,
impetigo etc increased >5-fold. It was postulated that this trend may be partly due to
changes in hygiene behaviour.
Of particular concern are the antibiotic resistant strains of S. aureus (MRSA). MRSA
in the home and community was reviewed in a 2006 IFH report. 14 This report shows
21
how problems related to MRSA are by no means confined to the hospital setting.
Infected patients discharged from hospitals may continue to carry MRSA, even after
their infection has healed, and pass it on to healthy family members who become
colonised, thereby spreading the organism into the community. Healthcare workers
caring for MRSA-infected hospital patients may also bring MRSA back into the home
on their hands or uniforms etc. MRSA has the same potential to infect the elderly and
immuno-compromised in a home setting whilst family members who are MRSA
carriers are at increased risk of infection following hospital admission or outpatient
treatments.
A new concern, also reviewed in the IFH report,14 is the emergence of new
“community” strains of MRSA (community-acquired MRSA or CA-MRSA). Whereas
healthcare associated (HCA) MRSA strains are mainly a risk to vulnerable people, for
CA-MRSA any family member is at risk, although US experience suggests that CAMRSA strains present a threat mainly to those engaging in activities involving close
skin contact and abrasion such as sports clubs and schools. Some S. aureus strains
circulating in the community [both CA-MRSA and methicillin sensitive S. aureus
strains (MSSA)] strains have also acquired the ability to produce Panton-Valentine
Leukocidin (PVL) toxin. These can cause severe invasive infections such as
bacteraemia, or necrotising pneumonia that kills more than 40% of patients. Although
CA-MRSA strains are now a major problem in the USA,40 they are still relatively
uncommon in Europe, and there is thus still an opportunity to avoid the problem
escalating to a similar same scale. CA-MRSA strains are already reported in UK,
France, Switzerland, Germany, Greece, Ireland, Nordic countries, Netherlands and
Latvia.41
Establishing the prevalence of MRSA circulating in the general community is difficult
and can vary significantly from one area to another. Establishing which cases are
healthcare-associated strains and which are “true” de novo community-acquired
strains is also difficult. In the UK, indications are that the proportion of the general
population carrying antibiotic-resistant strains of S. aureus (either HCA or CA-MRSA)
is somewhere between 0.5% and1.5%. The prevalence of PVL-producing strains
circulating in the UK community is currently small;42 perhaps around 2% of UK MRSA
strains are PVL-positive, but the figure may be much higher.
Data presented in the 2006 IFH review on MRSA14 shows that good hygiene is
important not only in protecting at-risk groups cared for at home, but also containing
the circulation of CA-MRSA and HCA-MRSA in the community. A number of case
studies are reviewed which showed that MRSA carriage in healthcare workers could
only be eliminated if skin decontamination was combined with a rigorous hygienic
cleaning programme aimed at eliminating MRSA from their home environment.
2.4 FUNGAL INFECTIONS
Fungi in indoor environments are a potential problem. They can be responsible for
infections, cause allergic responses, deteriorate/damage surfaces and cause
unpleasant odours. Moulds produce millions of spores, which, due to their small size
(average size 1–5 m) easily stay air-borne and may be breathed deep into the
airways. Air-borne fungi are usually associated with damp conditions, poor ventilation
or closed air systems. Primary sites of fungal growth are inanimate surfaces,
including carpets and soft furnishings.43
Some fungi are pathogenic to healthy humans, causing superficial infections
(mycoses), where the fungus grows on body surfaces such as the feet, skin, hair and
22
nails, as well as the oral or vaginal mucosa. They are spread by direct contact and
are highly contagious and easily spread to other individuals. Infections within the
body (deep mycoses) are rare in healthy humans but people with impaired immune
functions (e.g. cancer patients receiving chemotherapy or people with AIDS) are at
significant risk. They can be acquired by inhalation of spores or by entry through
wounds.44,45
Fungal infections in the home and the role of hygiene in preventing the spread of
fungal infections are described in more detail in a 2004 IFH review 46 and a review by
Scott.47
2.5 ANTIBIOTIC RESISTANCE
Antibiotic resistance is a major threat that severely undermines our ability to control
infectious diseases. The implication is that greater emphasis must now be placed on
preventive strategies such as hygiene, rather than reliance on antibiotic therapy, and
that these strategies need to be developed not only in hospitals but also in the
community. A number of aspects need consideration.
Firstly, hygiene is recognised as a strategy per se for reducing antibiotic resistance.
Good hygiene means fewer patients with infections demanding antibiotics from their
GP, thereby reducing the selective pressure that drives the ongoing emergence of
antibiotic-resistant strains. The benefits of this approach have been demonstrated in
clinical settings.48,49
The second aspect, as discussed in section 2.3, relates to the spread of pathogens
such as MRSA and ESBLs (extended spectrum  lactamase-producing E. coli) in the
home and community. Good hygiene is key to protecting risk groups, cared for at
home, from infection including with antibiotic-resistant strains of opportunist
pathogens such as HCA-MRSA and ESBLs. Circulation of resistant strains in the
community has important implications for delivering infection control in hospitals.
Hospital managers now realise that managing healthcare-associated infections is
hampered by people (new patients, visitors and healthcare workers) who are “silent”
carriers of resistant organisms such as MRSA, ESBLs, (and also C. difficile) that walk
into their facilities. By preventing the spread of these organisms through better
hygiene, we can reduce the reservoir of antibiotic-resistant strains circulating in the
community, which means that the opportunities for their introduction into hospitals via
new patients, healthcare workers and hospital visitors is reduced.
The need for improved hygiene to reduce the spread of antibiotic resistance was first
addressed in the 1999 report of the EU Scientific Steering Committee entitled
“Opinion on Antimicrobial Resistance”.50 The report stated that “there should be
action to reduce the risk of infection in individuals and in the population as a whole by
encouragement of uptake of immunisations, education regarding home hygiene,
attention to public health issues, and by the maintenance and/or improvement of
housing and social conditions”. The key action points set out by ECDC in their
initiative on antibiotic resistance are “using less antibiotics” and “preventing the
spread of antibiotic-resistant strains between people”.51 Educating primary and
secondary school pupils about antibiotic resistance and hygiene is the fundamental
aim of the EU-sponsored e-Bug project.52 This is a Europe-wide project that aims to
ensure that all children will leave school with knowledge of prudent antibiotic use and
how to reduce spread of infections for themselves and their children through hygiene.
23
2.6 PETS AND DOMESTIC ANIMALS AS A SOURCE OF INFECTION IN THE HOME
In the English-speaking world more than 50% of homes have cats and dogs.
Domestic cats and dogs can act as reservoirs of Salmonella, Campylobacter and
other enteric pathogens.53,54,55,56,57 Domestic animals can also be a source of S.
aureus, including MRSA and PVL-producing strains.58,59,60,61 Carriage of C. difficile in
household pets is common; 62 up to 23% of household pets are affected, although
carriage appears to be transient and not associated with IID. The increasing
popularity of exotic pets also increases the risk of humans acquiring zoonotic
infections.63
Although there is significant evidence that domestic pets have the potential to act as
a source of infection in the home, there are few data indicating the extent to which
this may or may not occur.64,65 In a study of 50 US homes where children under 4
years were known to be infected with Salmonella spp., in 34% of homes there was
also found to be illness in other family members.66 It was found that environmental
sources, infected family members and pets, were more significant risk factors for
development of salmonellosis than contaminated foods. Two further studies describe
discharged hospital patients and healthcare workers who were successfully treated
at home to eradicate MRSA carriage, but subsequently became recolonised. 58,59
Further investigation suggested that the source of re-colonisation was a domestic
dog. In a study carried out in the USA in 2006, 35 homes were recruited from the
Boston area. S. aureus was found in 34 of the 35 homes. MRSA was isolated from 9
of 35 homes, and was found on a variety of household surfaces. A positive
correlation was indicated for the presence of a cat and the isolation of MRSA from
surfaces.67
2.7 AT-RISK GROUPS IN THE HOME AND COMMUNITY
The changing “hygiene climate” in the home and community not only reflects the
constantly changing nature and range of pathogenic micro-organisms, but also the
social, demographic and other changes that are occurring within the global
population which affect our resistance to infection. Demographic changes and
changes in health service structure mean that the number of people in the home
needing special care, because they are at greater risk of infection is increasing. The
largest proportion is the elderly who have reduced immunity to infection, which is
often exacerbated by other illnesses such as diabetes, etc. Risk groups in the home
also include the very young, patients discharged recently from hospital, and family
members with invasive devices such as catheters. It also includes people whose
immuno-competence is impaired, either as a result of chronic and degenerative
illness (including those who are infected with HIV/AIDS), or because they are
undertaking certain drug or other therapies. This includes those undergoing
irradiation or chemotherapy for cancer, and organ transplant recipients.
Immunosuppressed persons are often also on other medications such as antibiotics,
which can further increase their susceptibility to infections.68
Data collected from several European countries suggest that at up to 1 in 5 of the
population belongs to an “at-risk” group (Table 2). The data suggest that between
12% and 18% of the population of these countries are >65 years of age.
24
Table 2 – Prevalence of “at-risk” persons in the domestic setting.
Total population
Over 65 years old
Living with cancer –
significant proportion
undergoing
chemotherapy
Under 1 year old
Discharged from
hospital within
previous 2 weeks
Hospital outpatients
at home
HIV cases*
AIDS cases
Total “at risk”
persons
UK
(2002)
60 million
9 million
Germany
(2002)
82 million
13 million
1 million
600,000
200,000
Holland
(2002)
16 million
2 million
Russia
(2003)
145 million
16 million
Ukraine
(2003)
50 million
14 million
1.3 million
400,000
177,000
500,000
>1 in 8
>1 in 3
160,000
800,000
100,000
60,000
1, 270,000
50,000
15,000
>1 in 6
>1 in 5.6
>1 in 6.3
*This does not include those who are HIV positive who may also have lowered resistance to infection
The elderly are at increased risk of death from gastro-intestinal disease.68 Problems
of faecal incontinence create an environment in which enteric and food-borne
pathogens are easily spread. Incidence of salmonellosis and Campylobacter
diarrhoea appears to be higher among the elderly. Data from the US68 suggest
increased case rates for Campylobacter and listeriosis among persons with AIDS, as
compared with the general population. An estimated 10–20% of cases of AIDSassociated diarrhoea are due to the waterborne pathogen Cryptosporidium.69 Cancer
cases have steadily increased in the past 20 years. Cancer patients undergoing
immuno-suppression therapy have higher risk rates of septicaemia and food-borne
infections.68 The number of people in the community living with organ transplants is
also increasing. Increased survival rates have been achieved by the use of
cyclosporine and other immune-suppressants but these in turn prevent the immune
system from reacting to infectious agents. According to the USA United Network of
Organ Sharing, approximately 15% of all deaths in transplant recipients are a result
of infection in the first 3 months.70
Across Europe, governments are increasingly under pressure to fund the level of
healthcare that people expect. Care of increasing numbers of patients in the
community, including at home is one answer, but can be fatally undermined by
inadequate infection control in the home. Increasingly, all of these “at-risk” groups are
cared for at home by a carer who may be a household member who thus requires a
good knowledge of hygiene.
2.8 THE IMPACT OF SOCIAL DETERMINANTS ON THE SPREAD OF INFECTIOUS DISEASES
Across Europe, there is an inequitable distribution of communicable diseases.
Populations at higher risk of infection in Europe coincide with those with a low level of
education, occupational class, or income level. These sub-populations suffer
disproportionately from a range of infections, including H. pylori, respiratory
infections, sexually transmitted diseases, and nosocomial infections. In low-income
populations, malnutrition also contributes to increased susceptibility to infection.
25
These factors can initiate a “vicious cycle” of infection predisposing to malnutrition
and growth faltering, which in turn leads to increased risk for further infection. The
self-perpetuating cycle leads to adverse health effects with differential consequences
because of poor access to care. The "vicious cycle" can result in a descent down the
socio-economic ladder, because healthcare costs and loss of work disproportionately
affect disadvantaged groups. The impact of social determinants on the incidence and
prevalence of communicable diseases in the newly expanded EU is discussed in a
2008 review by Semenza and Gieseke.71 They concluded that “unless the
fundamental causes of disease, namely the social determinants of health, are
improved, disparity in health outcomes will not be ameliorated”.
2.9 THE IMPACT OF SOCIAL TRENDS ON THE SPREAD OF INFECTIOUS DISEASES
Trends in social behaviour, eating habits, availability and use of home appliances etc
are also increasing the risks of transmission of infectious diseases in the home. The
demand for different and “exotic foods” stimulates increasing movement of foodstuffs
from one region or country to another and creates problems in controlling microbial
quality.63,72 Increasing population global mobility means that, as in the case of SARS,
virulent pathogens can move rapidly across the world, making it difficult to contain
epidemics related to novel strains.
In “westernised” homes, knowledge and skills in food handling and preparation have
declined with increasing reliance on refrigerators, freezers, microwave ovens and
dishwashers.63 In some cases, misuse of appliances contributes to the risks of
infection. The threat of listeriosis has increased with increasing use of refrigerators
because L. monocytogenes can multiply on certain types of foods even at
refrigeration temperatures.73 In the past few years, there has been a steady increase
in the use of microwave ovens in the home without proper appreciation that
microwaving may not make foods safe.74,75,76 Although, hygiene of dishes and
utensils has improved with the use of dishwashers, they are not universally used, and
water temperatures for washing dishes have declined. Although manually washed
eating utensils are normally wiped dry or left to air dry, which can inactivate microbial
pathogens,77 cross contamination can occur if contaminated water or contaminated
dish rags or sponges are used for washing or drying.78
Clothing, bed linens, towels and other items that are in contact with the body may be
a vector for transmission of infection. Cross contamination by household laundry has
been demonstrated by a number of studies.14, 79 Of current concern is the potential
for spread of S. aureus, particularly community-associated MRSA strains via clothing
and towels. Domestic clothes-washing practices have changed in the past 3 decades
to achieve energy conservation, but with little attention to the possible implications for
hygiene. Kniehl et al.80 described a study in Germany, of healthcare workers who had
regular close contact with MRSA-colonised patients. Sampling detected
contamination in 7/8 home environments affecting pillows, bed linen, brushes and
hand contact surfaces. Little is known about how well low-temperature washing
techniques eliminate pathogens from clothing and prevent cross contamination
between laundered items. A new study by Exner and co-workers is discussed in
section 3.2.
Heating and air conditioning systems mean that windows are often sealed, air is
recycled, and ducting can accumulate dust or act as a site for microbial growth.
Mechanical heating or air cooling can alter humidity, which can influence air-borne
survival of pathogens.81 Allergens and endotoxins produced by some bacterial and
fungal agents are increasingly implicated as causes of disease in humans.82
26
Legionnaires’ disease is an example of how conditioning of indoor air has turned an
environmental bacterium into a human pathogen.
2.10 CHRONIC SEQUELAE OF INFECTIOUS DISEASES
Whereas there has been a tendency to assume that common gastro-intestinal,
respiratory and skin infections circulating in the community are a relatively minor
concern, data increasingly show that both intestinal and also respiratory pathogens
can act as co-factors in diseases such as cancer and chronic degenerative diseases,
or as triggers for the development of allergic diseases. This further supports the need
to better control the spread of these diseases. Examples include Campylobacter
jejuni (Guillain Barré syndrome)83 and H. pylori (cancer).84 Clusters of Campylobacter
infections are known to arise in family households, and complications such as
Guillain Barré syndrome are a real concern.85,86 Food-borne illness has been
estimated to result in chronic sequelae in 2–3% of cases.87 A report from the
European Commission88 cited evidence of chronic disease, such as reactive arthritis,
following 5% of Salmonella cases, with 5% also of E. coli O157 cases progressing to
the serious and often fatal complication of uraemic syndrome.
Viral respiratory infections, even mild infections, can be important predisposing
factors to more severe and possibly fatal secondary bacterial infections.89 There is
also growing evidence that respiratory viruses may exacerbate attacks of
asthma.90,91,92 Recurrent wheezing in children has been associated with respiratory
infections early in life, RSV being one of the main viral agents thought to be
responsible.93,94 A study of the influence of childhood respiratory infections on adult
respiratory health95 suggests that the impact may not only last into adulthood but also
influence development and persistence of adult respiratory morbidity.
Richardson et al. present evidence that suggests that enteroviruses may be a trigger
for type 1 diabetes.96 Other studies show that infection may be more significant in
sudden unexpected death in infancy (SUDI) than previously thought.97,98,99,100 A UK
retrospective study of post-mortem data on 546 cases showed that S. aureus and E.
coli were more common than expected in babies whose deaths could not be
explained.97
3. DEVELOPING A RISK-BASED APPROACH TO HOME HYGIENE
The IFH (www.ifh-homehygiene.org) was established in 1997 in response to concerns
about the need for an international body that could speak from a scientific/medical
standpoint about home and community hygiene. The aim of IFH is the development of
an evidence-based approach to home hygiene, and the promotion of this approach to
scientists, opinion-formers, policy-makers and community health professionals. As
part of this work, IFH has developed an approach to home hygiene based on risk
management.24,101,102 Applied to the home, the risk-based approach has come to be
known as 'targeted hygiene'. Risk management is the standard approach for
controlling microbial risks in food and other manufacturing environments, and is
becoming accepted as the optimum means to prevent such risks in home and
hospital settings.103,104
27
3.1 IDENTIFYING CRITICAL CONTROL POINTS IN THE CHAIN OF INFECTION TRANSMISSION IN
THE HOME
Targeted hygiene starts from the principle that pathogens are introduced continually
into the home, by people (who may have an infection or may be asymptomatic),
contaminated food and domestic animals, but also sometimes in water, or via the air.
Additionally, sites where stagnant water accumulates such as sinks, toilets, waste
pipes, or items such as cleaning or face cloths readily support microbial growth and
can become primary reservoirs of infection, although these are mostly bacterial
species which only represent a risk to vulnerable groups.105 In many homes, there will
also be at least one family member who is more susceptible to infection for one
reason or another. Within the home, there is a chain of events, as described in Figure
1, which results in transmission of infection from its source to a new recipient. The
simple principle is that, if we can break the chain of infection transmission, infection
cannot spread.
Fig 1 – Chain of infection transmission in the home
Risk assessment is based on assessing the microbiological data related to each
stage of the infection transmission cycle in order to identify the critical control points
for preventing spread of infection. To identify these points, the frequency of
occurrence of pathogenic contamination at individual sites and surfaces is assessed,
together with the probability of transfer from that site such that family members may
be exposed. This means that, even if a particular site or surface is highly
contaminated, unless there is significant probability of transfer from that site, the risk
of exposure is low.
The risk-based approach to home hygiene is described in more detail by Bloomfield
and Scott.106,107 They suggest that sites and surfaces in the home should be
categorised into four main groups: reservoir sites, reservoir/disseminators, hands and
hand and food contact surfaces and other surfaces. From this it is possible to
determine the “critical control points” for preventing spread of infection. The data
suggest that:
28




For hands, and hand contact and food preparation surfaces, although the
probability of high counts of pathogens or potential pathogens is, in relative terms,
less than for wet sites such as toilets and cleaning cloths, there is still a significant
probability of pathogenic organisms being present, particularly, for example,
following contact with contaminated food, people, pets or other contaminated
surfaces such as door-, faucet- and toilet-flush handles. Since there is a constant
risk of spread from these surfaces, hygiene measures are important for these
surfaces.
For reservoir sites such as wet cleaning cloths (reservoir/disseminators), not only
is there high probability of significant contamination, but, by the very nature of
their usage, they carry a high risk of disseminating contamination to other
surfaces and to the hands.
For reservoir sites such as toilets, although the probability of contamination
(potentially pathogenic bacteria or viruses) is high, the risk of transfer is limited
unless there is a particular risk situation (e.g. a family member with enteric
infection and fluid diarrhea, when toilet flushing can produce splashing or aerosol
formation that can settle on contact surfaces around the toilet).105,108
For floors, walls, furniture etc risks are mainly due to pathogens such as S.
aureus and C. difficile that survive under dry conditions. Because the risks of
transfer and exposure are relatively low, these surfaces are considered low risk,
but where there is known contamination, for example, soiling of floors by pets,
crawling infants may be at risk. Cleaning can also re-circulate dust-borne
pathogens onto hand and food contact surfaces.
This approach allows us to rank sites and surfaces (Figure 2) according to the level of
risk; this suggests that the critical points are the hands, together with hand and food
contact surfaces, cleaning cloths and other cleaning utensils, which form the
'superhighways' for spreading pathogens around the home such that healthy family
members or the food they eat become exposed.
Fig 2 – Ranking of sites and surfaces in the home based on risk of transmission of
infections
Although this is a useful rule of thumb ranking, it is not constant and varies markedly
at different times and according to circumstances. Toilets were invented for the
purpose of dealing with human waste, but this does not mean that they are zero-risk
areas, they still have risks associated with them, particularly when someone in the
home has sickness, diarrhoea, or other contagious infections. Although floors,
however dirty they may appear, are assessed as relatively low risk, the risks increase
where a pet animal and a small child share a floor area, or where a floor surface is
contaminated with vomit or faeces.
29
3.2 APPLYING HYGIENE PROCEDURES TO BREAK THE CHAIN OF INFECTION IN THE HOME
Targeted hygiene also means applying a suitable hygiene procedure at appropriate
times to interrupt the chain of infection transmission. It is known that, even for healthy
family members, the infectious dose for some enteric and respiratory pathogens,
particularly viruses, can be very small (10-100 viable units or even less for some
viruses) and that infection can result from direct transfer from surfaces via hands or
food to the mouth, nasal mucosa and conjunctiva. Although the infectious dose for
enteric pathogens such as Salmonella is generally higher (up to 106 viable units), in
some situations it may be relatively low (<100 viable units). (see Bloomfield et al24 for
more details on infectious doses). On this basis one must argue that, in situations
where there is risk, a 'hygienic cleaning' procedure should be used which eliminates
as many organisms as possible from critical surfaces.
Hygienic cleaning can be done in one of two ways:
 By mechanical removal involving soap or by detergent-based cleaning with
rinsing. In this process, soap or detergent is used to maximise detachments of
microbes from the surface, whilst the rinsing process removes the organisms
from the surface. To be effective this process must be accompanied with
thorough rinsing under running water that is disposed of safely from the home
(e.g. into the public wastewater system) such that pathogens cannot be further
disseminated around the home.109,110,111
 By using a process or product that inactivates the pathogens in situ. This can be
achieved using a disinfectant product (such as a disinfectant or waterless hand
sanitizer) or by application of heat, UV irradiation etc. Heat is an effective means
of eliminating contamination from surfaces, either alone or in combination with a
chemical agent.
 Alternatively a combination of germ removal with kill can be used. For example,
to ensure elimination of pathogens, clothing and household linens should be
laundered at 60ºC. Alternatively this can be achieved at 40ºC using a bleachcontaining laundry product.112 Domestic dishwashers employ a combination of
heat and detergent-based cleaning with rinsing to decontaminate cooking and
eating utensils.
A whole range of laboratory and in use studies have been carried out to evaluate the
effectiveness of hygiene procedures used in the home. These are reviewed in detail
in an IFH report.113 The following examples are used to illustrate recent “in use”
studies to evaluate hygiene procedures used in food hygiene, in prevention of
norovirus cross infection and in elimination of MRSA from clothing and linens during
laundering.
3.2.1 Hygiene procedures to prevent cross contamination during food
preparation
In a study on cross contamination in the domestic kitchen,114 20 participants prepared
a meal using chickens naturally contaminated with either Salmonella or
Campylobacter. During preparation of the chicken (Table 3), contamination was
spread to the hands, hand and food contact surfaces, and cleaning cloths with a total
of 17.3% of the surfaces showing evidence of the target strain. In the second part of
the study, participants were instructed to clean up before sampling, using a typical
detergent-based procedure using a washing-up bowl. This process produced no
significant overall reduction in the incidence of contamination, the frequency
occurrence of contamination on hand and food contact surfaces remaining at 15.3%.
There was some reduction in contamination on hands and chopping boards, but this
30
was accompanied by an increase in contamination on some hands contact surfaces,
indicating that the contamination was actually spread via the cleaning cloth during the
cleaning process. In the final part of the study, disinfectant was used in addition to
detergent-based cleaning. Using this procedure, there was a significant reduction in
microbial risk; after cleaning with detergent and wiping surfaces with a cloth soaked in
hypochlorite disinfectant (5000 ppm available chlorine) the number of contaminated
surfaces was reduced to 2.3%.
Table 3 - Contamination of surfaces after preparation of a meal with a chicken
contaminated with Salmonella or Campylobacter, and after cleaning and disinfection
Percentage of sites contaminated with Salmonella
and/or Campylobacter
No of participants in each After meal
After cleaning with After cleaning with
group = 20
preparation
soap and water
soap and water +
hypochlorite
Chopping board
60
15
0
Utensils
5
25
5
Hands
35
20
0
Dishcloth
25
25
5
Sink surround
30
30
0
Sink rim
10
15
5
Taps, Fridge, Cupboard, Oven 9
8
1
and Kitchen Door, Condiments
TOTAL
17.3%
15.3%
2.3%
In a follow-up study,115 using the same methodology (Table 3), the effectiveness of
the “bowl washing procedure” was compared with a hygienic cleaning procedure
which involved cleaning with detergent followed by rinsing under clean running water
for 10 seconds. In this study surface samples were analysed to determine the number
of organisms that could be recovered. In this study the key surfaces (hands, cloths,
chopping board, utensils, tap handles) were evaluated. In the first part of the study,
where no cleaning was performed, it was found that, respectively, 8.3% and 50% of
samples taken after meal preparation showed counts of Salmonella and
Campylobacter exceeding 100 colony forming units (cfus) per sample area, with 3.3%
and 33% of sites showing counts of >1000 cfu. A significant reduction in the risk of
contamination could be achieved where surfaces were cleaned using a detergentbased bowl wash routine followed by rinsing under running water (as compared with
detergent-based cleaning alone). For Campylobacter, bowl washing with rinsing was
sufficient to reduce the number of contaminated sites to 1.7% with no sites showing
greater than 100 cfu. For Salmonella, on the other hand, following bowl wash with
rinsing 16.7% of 60 sites sampled still showed contamination, with 3.3% of sites
showing counts of greater than 100 cfu.
31
Table 4 - Viable counts on surfaces after preparation of a meal with a chicken
contaminated with Salmonella or Campylobacter, and after cleaning and disinfection
Cumulative % frequency occurrence of viable counts
(colony-forming units per total surface sample are or
200cm-2 of cloth)
>1
>100
>1000
Salmonella- contaminated chicken
Before cleaning
55
8.3
3.3
After bowl washing
40
13.3
8.3
After bowl washing +10 16.7
3.3
1.7
seconds rinsing
Campylobacter-contaminated chicken
Before cleaning
83.3
50
33
After bowl washing
13.3
5
1.7
After bowl washing +10 1.7
0
0
seconds rinsing
As a follow-up109 Barker et al. developed a laboratory model using chickens artificially
contaminated with Salmonella enteritidis PT4, to confirm the effectiveness of
detergent-based and disinfection procedures as determined previously with naturally
contaminated chickens. In this study, hygiene procedures were assessed on the
basis of their ability to reduce the number of recoverable salmonellas to <1 cfu.
Although detergent-based cleaning using a bowl-wash routine without rinsing
produced some reduction in risk (from 100% to 61.4% of contaminated surfaces), it
was insufficient to consistently restore surfaces to a hygienic state. By combining
detergent-based cleaning with a rinsing step or with hypochlorite at 500 ppm (of
available chlorine) some further reduction in microbial risk was achieved, but was not
considered satisfactory for food hygiene purposes. By contrast, the risk reduction
produced by hypochlorite at 5000 ppm was highly significant and was sufficient to
reduce the number of contaminated surfaces to 2.9%.
The extent of the risks associated with inadequate hygiene cleaning of hands, hand
and food contact surfaces during food preparation in the home is indicated by data
taken from other sources. A 2007/8 survey carried out by the UK Food Standards
Agency showed that up to 6.6% and 65.2% of chickens bought from retail premises
are contaminated with Salmonella and Campylobacter, respectively.116 As stated
previously, an EFSA report based on data reported back from EU countries in 2007
reported that, in foodstuffs, Campylobacter was mostly found in raw poultry meat with
an average of 26% of samples showing contamination. Poultry and pig meat were
reported as the foods most frequently associated with Salmonella, and on average
5.5 % of all fresh poultry meat samples was found to be contaminated. For the UK,
the stated contamination rates mean that around 1 in 25 UK homes prepares a meal
using a Salmonella- or Campylobacter-contaminated chicken every day. It has been
shown that contamination transferred to surfaces can survive for at least 4 hours up
to 24 hours for Salmonella.24 The infectious dose for Campylobacter is of the order of
100-500 cells72 whilst for Salmonella it may be as much as 106 cells, but may be as
little as 10 cells.117 A 2001 study of 192 food-borne outbreaks linked with private
residences in England and Wales suggested that cross contamination is a factor in
about 10% to 20%.118
The estimate from the community-based study of IID in England and Wales is that
the annual number of cases of Salmonella and Campylobacter infection in the
community is of the order of 400,000.8 In 2007, 204,104 cases of campylobacteriosis
32
were reported by 25 EU member states, and 157,739 cases of Salmonella were
reported by all EU and Euroean Club Association (ECA)/European Free Trade
Association (EFTA) states.1 It is likely however that the actual number of cases is
much higher. Taken together the data from the studies described in this section
suggest that a significant reduction in the number of cases of food poisoning could be
achieved by targeted use of an effective disinfectant product during handling of raw
foods such as poultry.
3.2.2 Hygiene procedures to prevent spread of norovirus between family
members
A study by Barker et al.110 shows the ease of spread of norovirus from environmental
surfaces via hands, cloths and other surfaces. In this study a small sample of a
faecal suspension from a person infected with norovirus was placed on a surface to
simulate a typical situation where there is an infected person in the home. The
presence of residual norovirus on surfaces was detected by RTP-PCR (Reverse
Transcriptase Polymerase Chain Reaction). The study showed that where
contaminated surfaces were cleaned using detergent and water applied with a cotton
woven cloth, on every occasion (the experiment was repeated 14 times), the virus
was not eliminated from the surface, and when the cloth was used to wipe another
clean surface, the virus was transferred to that surface and to the hands of the
person handling the cloth. Detergent-based cleaning was insufficient to eliminate
norovirus and prevent transfer, even where the cloth was rinsed out in clean water
and the surface re-wiped. In order to eliminate the norovirus from the cloths and
surfaces, it was necessary to use a hypochlorite disinfectant containing 5000 ppm
available chlorine. In situations where there was faecal soiling, it was necessary to
clean with detergent before application of disinfectant.
Data suggest that, where an infected person has fluid diarrhoea or vomiting, the virus
can be spread via aerosols generated by toilet flushing which can settle on surfaces
in the toilet such as the toilet seat, basin and toilet flush handle or by the settling of
particles of vomit on surfaces.105,108 It is known that a single vomiting incident can
produce 30 million norovirus particles.119 Other studies show that norovirus can
remain viable on these surfaces for several days and that the infectious disease
associated with hand to mouth transfer can be as little as 6-10 virus particles.119 In
the UK, it is estimated that about 4 million cases of norovirus occur annually. About
97% of these cases involve person to person rather than food borne transmission.
Overall this suggests that a significant reduction in the spread of norovirus from an
index case in the home could be achieved by good hand hygiene and targeted use of
an effective disinfectant product on critical contact surfaces.
3.2.3 Hygiene procedures to prevent transmission of MRSA via clothing and
household linens
As stated in section 2.8, domestic clothes-washing practices have changed
significantly in the past 3 decades. One of the driving factors has been to achieve
energy and water conservation, but with little attention to the possible implications for
hygiene. As discussed in section 2.3, in the USA, CA-MRSA is now a significant
concern. Although rates of colonisation in the community are still low, it is
nonetheless thought to be increasing.120, 121,122 A study of patients with skin and soft
tissue infections seeking treatment at a Los Angeles emergency department reported
that the proportion of CA-MRSA cases increased from 29% in 2001 to 2002 to 64%
in 2003 to 2004.123 A review of 1063 children 0 to 18 years old conducted by a Rhode
Island Hospital between 1997 and 200 showed that both the absolute number of
33
MRSA cases and the proportion of S. aureus cases due to MRSA rose more than
threefold. Of 57 MRSA cases, 23 (40%) were CA-MRSA.124 As stated in section 2.3,
although CA-MRSA strains have been detected in many European countries, there is
still an opportunity to avoid the problem escalating to a similar same scale in Europe
as in the USA. Experience in the USA suggests that CA-MRSA is easily
transmissible within families and community settings such as schools and sports
teams. Skin-to-skin contact (including intact skin) and indirect contact with
contaminated objects such as towels, sheets and sport equipment are the primary
vehicles of transmission.125 A study of US homes by Scott et al. showed that MRSA
could be isolated from a variety of frequently touched surfaces (including wiping
cloths and dishtowels) in 9 out of 35 homes.67 In German homes where there is a
carrier, MRSA has been isolated from laundered items (personal communication
from Martin Exner, May 2001).
In a 2009 study (Exner personal communication), Exner and co-workers studied the
hygiene effectiveness of machine laundry processes on cotton samples artificially
contaminated with S. aureus. Results (Table 5) showed that although premium
detergent cycles at 40°, 60° and 80° C produced an 8 log reduction in contamination
without the need for a pre-wash programme, cycles at 30° C produced only a 6 log
reduction with pre-wash and only a 3 log reduction without pre-wash. With nonpremium detergents (liquid colour detergent and gel detergent) cycles, although 60°C
cycles produced greater than 4 log reduction, 30°C cycles, even with pre-wash,
produced less than 1 log reduction, With 30°C and 60°C temperature cycles used
with non premium detergents there was also cross contamination between
contaminated and sterile laundry samples that were included in the cycle. Where
samples washed at 30°C with universal detergent were dried for 24 hours at room
temperature there was little or no increase in log reduction. Taken together, these
data indicate the importance of ensuring that recommended laundry processes
deliver hygiene using appropriate combinations of removal and microbial kill.
Table 5 - Disinfection of laundry samples inoculated with S. aureus in the main cycle
machine washing programmes. The study was carried out using the DGHM (German
Society for Hygiene and Microbiology) standard method.126
Pre-wash Temperature
No
80°C
No
60°C
No
40°C
No
30°C
Yes
Washing agent
Premium washing
pearls (contain a
bleaching agent based
on oxygen and an
optical brightener)
Mean Log 10 Cross contamination
Reduction to sterile cloth sample
Factor
included in cycle
8.15
No
8.18
No
8.06
No
3.07
No
30°C
6.31
No
No
60°C
4.22
no
Yes
60°C
6.99
Yes
No
30°C
≤1
Yes
Yes
30°C
≤1
Yes
No
30°C
1,75*
Yes
No
30°C
2,09**
Yes
Liquid colour detergent
(contain optical
brightener only)
Universal gel detergent
(contain optical
brightener only)
* wet cotton cloths; ** dried (24 h) cotton cloths
34
Even today, there is still a body of expert opinion, which holds to the view that, in
home and everyday life environments, soap and water are all that is required, there is
no need for the use of biocidal hygiene products. This recommendation makes no
reference to how soap/detergent-based processes should be applied in order to be
effective, and makes the assumption that the process is consistently effective. It also
takes no account of the data showing that, in reality, soap and water can be a very
effective means of spreading contamination from one surface to another. Overall the
data presented above, together with other data presented in the IFH review of home
hygiene procedures,113 clearly show that, in some situations, soap and water alone
are insufficient to eliminate contamination from critical control points. In these
situations it is necessary to use a process, such as the application of an effective
biocide, a waterless hand rub, or the use of heat, UV irradiation or other process that
can inactivate microbes in situ.
One of the arguments put forward against the use of biocidal hygiene products is that
although the germ removal by cleaning alone is less than that which can be achieved
by the use of biocidal products and processes, it is sufficient to produce hands,
surfaces, fabrics etc which can be considered as safe i.e. for which the level of
residual germs are no longer a threat to health. However, data increasingly show that
the infectious dose for many common pathogens, particularly viruses, but also
bacteria, can be very small, and that for pathogens such as Salmonella transferred to
food, a very small number of cells can multiply rapidly during storage at room
temperature to produce levels that are infectious. It also takes no account of the fact
that a substantial proportion of “healthcare”, the care of at-risk groups, now takes
place in the home, much of it provided by family members.
The benefits of maximising germ removal from critical surfaces has been
demonstrated by application of quantitative risk modelling techniques to hand
hygiene. A study by Haas and co-workers127 showed that, although the benefit of
using an alcohol hand rub which increases the log reduction on hands is not
measurable in terms of the individual, this can translate into a significant decrease in
disease burden within a community of individuals. In this study, data from the
literature were used to model transfer of E. coli O157:H7 from hand-to-mouth
following hand contact with ground beef during food preparation. Assuming that there
are 100 million individuals in the USA each of whom handles ground beef once per
month, and that 10% of these individuals contact hand-to-mouth after handling
ground beef, this amounts to 120 million infection incidents per year. From the
microbiological data on the typical levels of contamination of E.coli found in raw
meat, rates of transmission etc, it was assessed (Table 6) that if all individuals
washed their hands with soap following contact with ground beef (median log
reduction on hands assessed as 0.3) this would result in an estimated 0.014
infections per year. If, on the other hand, individuals used an alcohol hand rub
(median log reduction on hands assessed as 4.3) the risk would be reduced to an
estimated 0.00005 infections per year, equating to 99.9996% median risk reduction
compared with handwashing.
35
Table 6 – Risk of infection from handling raw beef contaminated with E. coli O157,
and subsequent hand-to-mouth contact following handwashing or use of an alcohol
handrub
Log reduction on hands
Mean
Median
Standard deviation
Handwashing
Median 0.3
(range 0.2 to 3.0)
1.25 x 10-2
1.18 x 10-10
7.52 x 10-2
Use of alcohol hand rub
Median 4.3
(range 2.6-5.8)
1.15 x 10-2
3.71 x 10-13
7.26 x 10-2
Overall the key to targeted hygiene as outlined in this section is that it recognises that
good hygiene is not a 'once weekly deep down clean': it needs to be an ongoing part
of our daily lives such that appropriate hygiene measures are targeted where and
when necessary to halt the spread on infection. The need for effective hygiene
processes is discussed in more detail below.
4. ESTABLISHING THE LINK BETWEEN TARGETED HYGIENE AND HEALTH BENEFITS
Data showing the strong association between hygiene and the prevention of
infectious diseases come from a range of sources including epidemiological and
microbiolgical/biological plausibility data.2,14,24,128,129
Across Europe, the targeted approach to hygiene is now being accepted as the
optimum means for developing an effective code of hygiene practice for the home.
The approach is well supported by the growing database of microbiological evidence
directly relevant to the home. This evidence is reviewed in a number of IFH and other
reports.2,24,129,130 The validity of a risk-based approach is well established through
several decades of application in food, pharmaceutical and cosmetics industries. It is
also now being used to develop strategies for reducing healthcare–associated
infections. A risk-based approach, for example has been adopted in developing the
WHO Global Patient Safety Challenge to promote hand hygiene in healthcare
facilities; the central concept ‘My five moments for hand hygiene’ focuses, not just on
getting people to wash their hands, but to do it at the right time and in conjunction
with other critical control measures.104
In contrast to the large database of microbiological data to support a risk-based
approach, however, there are few or no intervention study data that directly assess
the impact of targeted hygiene on infection rates in the home. This means that there
is no quantitative data that can be used to assess the relative benefits of investment
in targeted hygiene promotion compared to other interventions such as vaccination
programmes. The exception to this is two specific interventions which are an integral
part of targeted hygiene, namely hand hygiene and point- of-use water treatment in
the home.
Currently, there is a tendency to demand that data from intervention studies should
take precedence over data from other sources in formulating public health policy.
Although there are those who still adhere to this, it is increasingly accepted that,
since transmission of pathogens is highly complex, involving many different
pathogens each with multiple routes of spread, infection control policies and
guidelines must be based on the totality of the evidence including experimental
microbiological and other data. This is particularly important for home hygiene, for
which little or no intervention data are available and where it is virtually impossible to
36
isolate the effects of specific hygiene procedures (hand washing, surface hygiene,
laundry, washing and bathing etc).
In optimising the targeted approach to hygiene, one thing that is needed is an
accepted system for establishing the effectiveness of hygiene processes under use
conditions and comparing the effectiveness of processes that involve “germ removal”
with those that involve “germ kill”. Although suspension and surface tests, such as
those developed by CEN and Association of Official Agricultural Chemists (AOAC),
are important for establishing and comparing efficacy of disinfectant products under
standardised conditions, manufacturers need to develop “in use” models, such as
those described in the examples outlined above, to better ensure that products and
processes (which may involve combinations of germ removal with germ kill) deliver
effective hygiene under use conditions, and in consumers’ hands. The production of
standardised Phase 3 or “in use” tests by standards bodies such as CEN is not a
realistic option since the range of applications for biocidal products is infinite. What is
needed is official guidelines and criteria (repeatability and reproducibility, adequacy
of controls, peer review etc) that can be used by manufacturers and regulatory
authorities to judge the validity of models used to evaluate the efficacy of hygienic
cleaning processes under use conditions. This principle is outlined in the CEN
standard “Chemical disinfectants and antiseptics – Application of European
Standards for Chemical Disinfectants and Antiseptics.”131
5. IFH – DEVELOPING
AND PROMOTING THE TARGETED APPROACH TO HOME
HYGIENE
As part of our work in promoting hygiene, the IFH has produced a set of 'Guidelines
for Home Hygiene' together with 'Recommendations for selection of suitable hygiene
procedures'.132,133 These are based on the risk-based approach, and cover all aspects
of home hygiene including food and water hygiene, hand hygiene, general hygiene,
personal hygiene, care of pets, care of risk groups etc. IFH, in collaboration with the
UK Infection Prevention Society, has also produced a teaching resource which
presents home hygiene theory and practice in simple practical language which can be
understood by community workers with relatively little infection control background. 112
Most recently IFH has produced a range of plain language fact/advice sheets on
home hygiene and hygiene issues. All of these materials are available through the
IFH website (www.ifh-homehygiene.org) and are being promoted through a range of
activities (conferences, exhibition stands, partnership with other organisations etc).
If programmes to promote hygiene are to be successful in achieving behaviour
change, there are however a number of challenges. Experience now shows that
strategies that aim to change health behaviour simply by educating the public about
the risks of infection and instructing them about hygiene have little success. We need
to develop strategies based on understanding people’s motivations for hygiene
behaviour. In recent years, hygiene has had a somewhat negative image and has
come to be seen as old-fashioned and disciplinarian. We need to make hygiene more
appealing to the public by realigning it with positive attributes of health and wellbeing. Equally we must recognise the people are entitled to freedom of choice
according to their personal assessment of their needs, priorities and values.
Persuading the public of the need to share responsibility without being accused of
shifting blame may however be a significant challenge. In recent years, a significant
amount of research has been done to identify strategies for changing hygiene
behavior. Whilst we recognise that this aspect is fundamental, it is outside the scope
of this report and is reviewed elsewhere.134, 135,136,137
37
6. SUSTAINABLE HYGIENE – THE KEY FACTORS
As outlined in the introduction to this report, hygiene has the potential directly to
improve sustainability because its aim is to promote and protect health. Good health
is fundamental to the concept of a sustainable future and poor health is a severe and
increasing burden on economic sustainability. The hygiene measures used, however,
must themselves be sustainable. Most aspects of the sustainability of hygiene
measures, notably those that involve environmental impacts or safety, are typical of
those arising in product and process life cycles generally. Two specific possible longterm impacts, however, need additional consideration. First, there is the question of
whether protection against infection by limiting microbial exposure might in some
circumstances also have some adverse consequences i.e. the sustainability of
hygiene per se. Second is the question of whether use of biocides to deliver hygiene
might have additional impacts.
Sustainability and sustainable development are concepts that refer to meeting the
needs of society, and improving quality of life, in a way that does not jeopardise the
ability of future generations to meet theirs. Many aspects of modern life are currently
unsustainable, in that they are consuming resources or having other impacts (e.g. on
climate change) at a rate that cannot be sustained indefinitely. Equally, the world is
ever changing, and sustainability is not an absolute condition which can be attained
and be expected to remain attained; sustainability is an ongoing goal to be pursued
through continual improvement.
A key tool used in sustainability assessment is Life Cycle Assessment (LCA). This
methodology evaluates, in a quantitative way, the significant environmental impacts
of products or processes in terms of inputs required (such as materials, energy,
water) and outputs (such as emissions and waste). It is eminently applicable to
evaluating sustainability of hygiene products (such as soaps, cleaners, disinfectants,
paper towels) and procedures (such as washing in hot water or heat sterilisation).
However, while LCA can ascribe numerical values with some degree of accuracy to
individual impacts from a particular process, the relative importance of different types
of impact is subjective and variable according to prevailing conditions and even value
judgements. In most cases, assessments are concerned with comparing options,
rather than ascribing exact values. Improvements are more likely to be achieved by
seeking improvements in sustainability profiles (e.g., where some impacts can be
improved markedly, others stay the same) rather than trying to declare one of two
options with disparate impacts to be the more sustainable.
Numerous tools and initiatives are being developed to improve sustainability: it is not
the purpose of this document to review and assess these, which is outside the
expertise of IFH, simply to highlight important considerations when these tools are
applied to hygiene and prevention of infection. In the case of hygiene, sustainability
assessments need to systematically compare alternative ways of delivering the same
end result. It is thus important that desired results are defined, not only in terms of
e.g. acceptable contamination levels but also in terms of the reliability or likelihood
with which they can be achieved. Assessments must in principle consider the whole
process and impacts throughout the life cycle, but of course interchangeable
elements within a process (e.g. alternative products or procedures) can be compared
provided this is done on the basis of the same end result.
A sine qua non as regards sustainability is assurance of safety for people and the
environment. This can generally be assessed for formulated hygiene products using
38
well-established chemical risk assessment techniques, and manufacturers have clear
responsibilities to ensure the safety of their products. A substantial number of
ingredients commonly used in formulated hygiene products already have detailed,
published, risk assessments, e.g. under the EU Existing Chemicals legislation,
OECD (Organisation for Economic Development and Co-operation) programmes and
through voluntary industry initiatives such as HERA (Humanities in the European
Research Area). Such risk assessments are now a formal requirement under the
REACH legislation. These risk assessments and associated legislation consider in
detail the hazards of substances used as ingredients and assess for each significant
use scenario, including hygiene, whether exposure may be sufficient to give rise to
any significant risk. Where necessary, appropriate controls (risk management
measures) are then applied to ensure there will be no appreciable risk in use.
Taking the above as background, the two additional questions that relate specifically
to hygiene to can now be considered:
1. Sustainability of hygiene as an infection prevention measure
In delivering infectious disease prevention through hygiene, the sustainability of
hygiene itself must be considered. On one hand it must be designed to optimise
protection against exposure to harmful microorganisms, but the possibility that
reduced contact with such organisms could have some adverse effect also needs to
be considered. The prime example of such a potential effect is known as the ‘hygiene
hypothesis’.
This hypothesis was first formulated in 1989 by Strachan who observed that there
was an inverse relationship between family size and development of atopic disorders
– the more children in a family, the less likely they were to develop these allergies.
From this, he hypothesised that lack of exposure to “infections” in early childhood,
transmitted by contact with older siblings could be a cause of the rapid rise in atopic
disorders over the last thirty to forty years. Strachan further proposed that the reason
why this exposure no longer occurs is, not only because of the trend towards smaller
families, but also “improved household amenities and higher standards of personal
cleanliness”.
Although there is substantial evidence that some microbial exposures in early
childhood can in some way protect against allergies, there is no evidence that we
need exposure to harmful microbes or that we need to suffer a clinical
infection.138,139,140 Nor is there evidence that hygiene measures such as
handwashing, food hygiene etc. are linked to increased susceptibility to atopic
disease.138,139 If this is the case, there is no conflict between the goals of preventing
infection and minimising allergies. A consensus is now developing among experts
that the answer lies in more fundamental changes in lifestyle that have led to
decreased exposure to certain microbial or other species, such as helminths, that are
important for development of immuno-regulatory mechanisms.141 There is still much
uncertainty as to which lifestyle factors are involved. There is also no evidence to
suggest, as is often stated in the media, that we need to get regular infections to
boost our general immunity to infection. Weighed against any possible beneficial
effects, there is now growing evidence that respiratory viruses are a risk factor for
asthma and may actually exacerbate attacks.142,143,144
Alarmist media coverage of the hygiene hypothesis has declined, and become more
representative of expert consensus. But a strong ‘collective mindset’ has become
established that dirt is ‘healthy’ and hygiene somehow ‘unnatural’. This has caused
concern among health professionals that the hygiene behaviours of the general
public, which are the foundation of public health and our protection against infectious
39
disease, may become undermined.145 The reality is that, without clear evidence of the
need for exposure to infectious doses of pathogens (or suffering an infection) to
develop a healthy immune system, set against the firm knowledge that germ
exposure can cause disease, encouraging lower standards of hygiene in order to
reduce the burden of allergic diseases would be a reckless and ill-advised strategy
with potential major adverse consequences for public health.
We are only now beginning to understand how the normal resident and
environmental flora interact within the body to maintain a healthy immune system. It
is thus a prudent and precautionary approach that hygiene measures should be
targeted where they are most needed so as to avoid unnecessary disruption of
natural flora of both the human body as well as the environment. We need to explain
the difference between ‘dirt and ‘germs’ and promote a more balanced understanding
of the issues. This will enable people to see how they can follow a healthy lifestyle
that involves “getting dirty” while still maintaining hygienic behaviours that seek to
minimise risks of exposure to germs.
2. Sustainability of the use of biocidal products and other biocidal processes
An implicit part of the IFH targeted hygiene approach, as outlined in this report, is
that, if we are to deliver hygiene at the critical points as needed to break the chain of
infection transmission, biocidal products and processes are required in certain
situations. The sustainable use of biocides and biocidal products in terms of life-cycle
impacts, and their human and environmental safety can be assessed and assured,
as described above. The Biocidal Products Directive, now requires full human health
and environmental risk assessments to be prepared in the coming years for all other
biocides in relation to their uses and indeed individual biocidal products will also
require authorisation under BPD. Those not giving satisfactory risk assessments will
be restricted or removed from the market.
In assessing these issues, we need to bear in mind however that biocides are not a
fundamentally distinct group of compounds. While some biocides have been
developed and are exclusively used for their biocidal activity (e.g. triclosan,
phenolics, chlorhexidine, preservatives), there are many other substances that are
used in cleaning products (e.g. soaps, detergents, acids etc) which are not
traditionally regarded as biocides, but which can also have significant biocidal action.
Some compounds (e.g. hydrogen peroxide, hypochlorites, common acids) are
multifunctional i.e. they are included in products with the intention of providing both a
cleaning as well as a biocidal action. There are also families of substances (e.g.
quaternary ammonium compounds, alcohols, aldehydes) normally regarded as
biocides in which some members have little or no activity.
Thus in most respects the sustainability of biocides and biocidal products (in terms of
life-cycle impacts), and their human and environmental safety, can be assessed and
assured in just the same way as other ingredients and products. They will have a
wide range of human and environmental safety profiles, but, from existing knowledge
of chemical hazards, it is apparent that these are not uniformly more adverse than
other ingredients. Currently, detailed human and environmental risk assessments are
published for relatively limited range of biocidal ingredients, though human safety
assessments for biocidal ingredients used in cosmetics and personal care products
are also available.
Once the safety of a biocidal product is assured as above, i.e. no significant risk of
adverse effects, it could be argued that ingredients could then be selected only in
40
relation to their relative life-cycle impact profiles. On the other hand, from a
sustainability viewpoint, it makes sense that ingredients with more favourable
environmental and human safety profiles should be preferred, all other things being
equal, as this could usefully increase margins of safety and provide added assurance
for the future against any hitherto unsuspected effects. Favourable environmental
safety characteristics for example include ready degradation or removal during
sewage treatment, and low lipophilicity and thus a low potential to bioaccumulate. In
general terms, ingredients whose hazards are well understood and characterised
might likewise be preferred to those where there is greater uncertainty.
Apart from the above considerations of life-cycle impacts and safety, one question
that has particular relevance is whether use of biocidal products might encourage the
emergence or proliferation of so-called 'superbugs' which are resistant to antibiotics.
There is also concern that widespread use of biocides may lead to resistance to
those biocides.
From a literature review in 2002146 (updated in 2004147), IFH has concluded that,
although laboratory experiments demonstrate links between exposure to certain
biocides and increased resistance to antibiotics, there is currently no evidence that
use of biocides in the community is linked to emergence and spread of antibiotic
resistance; antibiotic misuse is the most significant causative factor. These
conclusions differ only in emphasis from those expressed in a 2009 report from the
EU Scientific Committee on Emerging and Newly Identified Health Risks
(SCENIHR)148 which concluded that current scientific evidence does indicate that
use of certain types of active substances in biocidal products in various settings may
contribute to increased occurrence of antibiotic resistant bacteria. They further
conclude that, to date, the lack of precise data, in particular on quantities of biocides
used, makes it impossible to determine which biocides create the highest risk. Their
conclusions are that “the most studied biocides, triclosan and quaternary ammonium
compounds, are likely to contribute to maintaining selective pressure allowing the
presence of mobile genetic elements harbouring specific genes involved in the
resistance to biocides and antibiotics. However, the lack of data on the other biocidal
compounds prevents reaching a definitive answer as to their role in selecting for or
maintaining bacterial antibiotic resistance”.
Overall however both the IFH and SCENIHR reports stress the important role of
biocides in the control of microbes in a variety of applications. Both reports caution
that biocides are a precious resource that must be managed through appropriate and
prudent use. IFH further concludes, as have others 50 that, as antibiotic resistance
continues to reduce our ability to treat infections, infection prevention through good
hygiene in hospitals and in the community becomes of even greater importance. By
reducing the number of infections through effective hygiene, the number of courses
of antibiotic treatment prescribed can also be reduced, which can in turn reduce the
impact of antibiotic resistance.
IFH recommends that, wherever possible, biocides should be used at concentrations
and under conditions that give rapid and effective inactivation of microbes. Reactive
biocides (e.g. peroxide and hypochlorite bleach) and those which evaporate
(alcohols) or disappear rapidly, leaving bacteria with no residue to which to develop
tolerance, should be preferred.
IFH has also addressed the concern that widespread use of biocides may lead to
resistance to those biocides. After review146,147 IFH has concluded that although
laboratory studies provide evidence that prolonged exposure to low levels of certain
41
biocides can be associated with reduced microbial susceptibility to those biocides,
there is currently no evidence that biocide usage at its current levels (i.e. in the
domestic and other settings) compromises effectiveness of hygiene procedures
under in-use conditions. Again, however, prudent use is advised.
7. TARGETED
HYGIENE
–
A FRAMEWORK FOR SUSTAINABLE HYGIENE IN THE HOME
AND EVERYDAY LIFE
In this review the targeted or risk-based approach to home hygiene, as developed by
the IFH, is outlined. The aim of this approach is to maximise protection against
exposure to infectious agents by breaking the chain of infection transmission. The
essence of targeted hygiene is that it works to ensure, as far as possible, that
hygiene interventions are focussed on situations where they maximise protection
against infection, rather than in situations where there is little risk. Whilst targeted
hygiene was originally adopted by IFH as a means to develop an effective code of
hygiene practice for the home, it also provides a framework for sustainable hygiene
because, through prudent and focussed use of hygiene products and processes, it:
 minimises the life-cycle impacts of hygiene processes, and maximises safety
margins against any hazards of their use
 minimises any risks of development of antibiotic resistance from exposure to
low level biocide residues
 seeks, as far as possible, to sustain “normal” levels of exposure to the
microbial flora of our environment to the extent that is important to build a
balanced immune system.
In developing and/or selecting biocidal products or processes for use within a
targeted approach to hygiene, a number of issues need to be considered in order to
satisfy the above criteria and thereby maximise sustainability:
 We need to select the most appropriate biocides. This means selecting, as far as
possible:
 biocides that are effective against the spectrum of organisms that represent a
risk in the particular situation in which it will be used
 biocides that have a rapid biocidal action in order to break the chain of
infection transmission (e.g. on hands, hand contact and food contact
surfaces) with minimum delay. Note: In some situations (e.g. controlling
growth of potentially harmful fungal contamination on damp surfaces such as
tiled walls) a sustained biostatic (growth inhibiting) action is appropriate
 biocides and biocidal products that are not environmentally persistent or
bioaccumulative, for which potential adverse effects are well characterised
and understood, and where there are good margins of safety.
 We need to think more innovatively about delivery of hygiene. For example, can
we use our growing understanding of microbial attachment and detachment to
better design products and processes that efficiently combine prevention of germ
attachment, germ removal and control (germ kill) in order to deliver the necessary
hygiene result in a more sustainable way?
 We need to ensure that, as far as possible, we use “doses” of biocidal products
and processes (cleaning, biocidal and physical agents either singly alone or in
combination) which achieve hygienic cleaning of sites, surfaces, fabrics etc with
minimum use of water, power or chemicals. This in turn however depends on
developing in use/field test models which most closely mimic conditions of use
and allow comparison of processes that involve both germ removal and germ kill.
 We need to think more holistically about delivery of hygiene in relation to
sustainability i.e. in developing and selecting the most suitable hygienic cleaning
42
method for any situation, we need to consider ALL factors (infectious disease
prevention, environmental and human safety, sustainability, antimicrobial
resistance, the immune system) rather than each factor in isolation.
The key to targeted hygiene is the recognition that good hygiene requires well
formulated products that can deliver “hygienic cleaning” through either germ removal
or kill (or combinations of processes) in order to break the chain of infection
transmission. Targeted hygiene will not be delivered by adding arbitrary amounts of
biocides to cleaning products in order to give a “bit of extra hygiene”.
8. CONCLUSIONS AND RECOMMENDATIONS
The evidence presented in section 2 of this report shows that infectious diseases
circulating in the home and community are a continuing and significant burden on the
health and prosperity of the EU, which could be significantly reduced by better
standards of hygiene. In Europe, it is estimated that up to 86% of deaths are now
attributed to chronic conditions. These mortality statistics have driven public health
investment towards reducing death rates from non-communicable diseases. The
chronic disease problem however masks the triumphs of the public health and
medicine that rolled back communicable disease mortality during the 20th century.
The quandary of public health lies in the fact that successful communicable disease
control is indirectly responsible for high chronic disease mortality statistics and the
shift of investment away from the very systems that maintain it. It is now apparent
that there is need for more investment in controlling infection, not just in healthcare
settings or in association with food hygiene, but across the community. There is also
recognition that health service spending in Europe cannot be sustained at its current
level, and there is thus need for more emphasis on disease prevention strategies.
Vaccine and hygiene promotion strategies have the effect of reducing the burden of
infectious disease and the need for investment in care of those who are infected.
They can also reduce antibiotic prescribing which is driving the antibiotic resistance
issue.
In section 3 of this review the targeted or risk-based approach to home hygiene, as
developed by the IFH, is outlined. The aim of this approach is to maximise protection
against exposure to infectious agents by breaking the chain of infection transmission.
This is achieved by the timely application of processes that eliminate or control
microbial contamination at critical points in the chain of transmission. The evidence
presented in section 3.2 indicates that if we are to deliver “hygiene” (i.e. a level of
contamination not harmful to health) at the critical points, it requires use of biocidal
hygiene products and processes (alone or in combination with germ removal) in
certain situations.
In developing and promoting hygiene practice in the home and everyday life, as
discussed in sections 2 to 5, the issue of sustainability must also be addressed. As
stated in section 7, whilst targeted hygiene was originally adopted by IFH as a means
to develop an effective code of hygiene practice for the home, what it also does is
provide a framework for building sustainability into hygiene because it minimises the
life-cycle impacts of hygiene processes, maximises safety margins against any
hazards of their use and minimises any risks of the development of antibiotic
resistance from exposure to biocides. It also looks to sustain “normal” interaction with
the microbial flora of our environment.
In the last 20 years, we have seen growing investment across Europe in controlling
infectious diseases, not only with the establishment of ECDC, but also through
43
national hygiene promotion programmes which recognise that if the burden of
infectious disease is to be contained in a manner that is economically sustainable, it
is a responsibility that must be shared by the public. In the UK, there has been an
intensive interactive programme to improve standards of food hygiene in the home.
In response to the need for education on respiratory hygiene, ECDC has produced
an 'Influenza Communication Toolkit'149 for use by health communicators in devising
campaigns to tackle seasonal influenza. In November 2007, the UK launched a
winter communications campaign to encourage the public to practise correct
respiratory and hand hygiene when coughing and sneezing.150 In recent months we
have seen intensive investment in promotion of hand hygiene in the home and
community as a means to mitigate the spread of swine flu.
IFH believes, however, that the impact of hygiene promotion programmes on the
public is being weakened by the fact that the different aspects of hygiene are being
dealt with by separate agencies. This means that the information that the family
receives is fragmented and largely rule-based. If things are to change we must
recognise that fragmented, rule-based knowledge is not enough to meet the
challenges we face. Hand hygiene, for example is a central component of all hygiene
issues and it is only by adopting a holistic approach that the causal link between
hands and infection transmission in the home can be properly addressed. At the very
least we need to ensure that the principles of infectious disease transmission and the
role of hygiene are part of the school curriculum. In line with this, the EU-funded eBug project is working to roll out education on antibiotic resistance and hygiene at
primary and secondary school level across Europe.52
If we are to sustain a high level of protection for EU citizens against infectious
disease, in the face of changing demographics and microbial evolution, and derive
real health benefits from investment in hygiene promotion, IFH concludes that the
various stakeholders need to work together to address the following issues:
 the public must be engaged so that they share the burden and bring the unique
contribution that only they can make, through good hygiene in the home and
community. To achieve this, hygiene promotion strategies should :
 be family-centred rather than agency-oriented, building on what people
understand, know, and need to know.
 not only change behaviour but also engender more positive attitudes to
hygiene as a means to achieve health, well being and prosperity.
 give people the opportunity for a more balanced understanding of how to
protect themselves from infectious diseases in a world where they also have
conflicting concerns about issues such as allergic diseases and the
environment.
 the risk-based ‘targeted’ approach to home hygiene should be adopted as the
basis for development of hygiene codes for the home and everyday life since it
offers both the most effective approach to breaking the chain of infection
transmission as well as an intrinsically more sustainable framework.
 within the targeted approach to home hygiene, we need not only cleaning
products that facilitate germ removal, but also biocidal products and processes
are required. These provide germ inactivation, alone or in combination with
cleaning processes, which can be used to ensure the elimination of pathogenic
contamination from critical control points when used by consumers.
 The selection of products or processes for hygiene tasks should be based on
assessment of their sustainability and safety as well as reliability in delivering the
required result. Additional potential impacts on bacterial resistance and immunity
need to be considered and any risks need to be accurately weighed against the
risks and impacts of infectious disease, and managed appropriately.
44

The European regulatory process should:
 Encourage and facilitate the development and marketing of products and
processes that deliver hygiene in a safe and sustainable way, using
combinations of germ removal and germ kill as appropriate.
 Encourage manufacturers to develop test methods that model use conditions
in order to ensure optimum efficacy and reliability with minimum impact
throughout the life cycle.
45
REFERENCES
1
European Centre for Disease Control and Prevention. Annual epidemiological
report on communicable diseases in Europe 2009
http://www.ecdc.europa.eu/en/publications/Publications/0910_SUR_Annual_Epidemi
ological_Report_on_Communicable_Diseases_in_Europe.pdf
2
Bloomfield SF, Exner M, Fara GM, Nath KJ, Scott EA, Van der Voorden C. The
global burden of hygiene-related diseases in relation to the home and community.
(2009) International Scientific Forum on Home Hygiene. Available from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/111e68ea0824afe1802575070003f039/29858a
a006faaa22802572970064b6e8?OpenDocument
3
Denny J, Boelaert F, Borck B, Heuer OE, Ammon A, Makela P. Zoonotic infections
in Europe: trends and figures - a summary of the EFSA-ECDC annual report. Euro
Surveill. 2007;12(12):E071220.6. Available from:
http://www.eurosurveillance.org/ew/2007/071220.asp#6
4
World Health Organization. Several foodborne diseases are increasing in Europe.
Press Release EURO/16/03. Available from:
http://www.euro.who.int/eprise/main/who/mediacentre/PR/2003/20031212_2
5
European Food Standards Agency. The Community Summary Report on Trends
and Sources of Zoonoses and Zoonotic Agents in the European Union in 2007.
http://www.efsa.europa.eu/EFSA/efsa_locale-1178620753812_1211902269834.htm
6
Chapman PA, Cerdan Malo AT, Ellin M, Ashton R, Harkin MA. Escherichia coli
0157 in cattle and sheep at slaughter, on beef and lamb carcasses and in raw beef
and lamb products in South Yorkshire, UK. International Journal of Food
Microbiology 2001;64(1-2):139-50.
Le Baigue S, Long S, Adak GK, O’Brien SJ. Infectious intestinal disease – it’s not
all foodborne! PHLS 25th annual scientific conference, 2000.
7
8
Wheeler JG, Sethi D, Cowden JM, Wall PG, Rodrigues LC, Tompkins DS, et al.
Study of infectious intestinal disease in England: rates in the community, presenting
to general practice and reported to national surveillance. British Medical Journal
1999;318:1046-50.
9
de Wit MA, Koopmans MP, Kortbeek LM, van Leeuwen NJ, Bartelds AI, van
Duynhoven YT. Gastroenteritis in sentinel general practices in The Netherlands.
Emerging Infectious Diseases 2001;7:82-91.
10
Widdowson MA, Monroe SS, Glass RI. Are noroviruses emerging? Emerging
Infectious Diseases 2005;11:735-7.
11
Soriano-Gabarró M, Mrukowicz J, Vesikari T, Verstraeten T. Burden of rotavirus
disease in European Union countries. Pediatric Infectious Disease Journal 2006;25(1
Suppl):S7-S11.
12
Food Standards Agency. A Report of the Study of Infectious Intestinal Disease in
England. London: The Stationery Office; 2000.
46
13
Krause G, Altmann D, Faensen D, et al. SurvNet electronic surveillance system for
infectious disease outbreaks, Germany. Emerging Infectious Diseases
2007;13:1548-55.
14
Bloomfield SF, Cookson B, Falkiner F, Griffith C, Cleary V. Methicillin resistant
Staphylococcus aureus (MRSA), Clostridium difficile and ESBL-producing
Escherichia coli in the home and community: assessing the problem, controlling the
spread. (2006). International Scientific Forum on Home Hygiene. Available from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/eb85eb9d8ecd365280257545005e8966/c63d0
7b19fa214d3802574dd003efc1a?OpenDocument
15
Knoop FC, Owens M, Crocker IC. Clostridium difficile clinical disease and
diagnosis. Clinical Microbiology Reviews 1993;6:251-65.
16
Starr J. Hospital acquired infection. Control measures for Clostridium difficile need
to extend into the community. British Medical Journal 2007;334:708.
17
Burgner D, Siarakas S, Eagles G, McCarthy A, Bradbury R, Stevens M. A
prospective study of Clostridium difficile infection and colonization in pediatric
oncology patients. Pediatric Infectious Disease Journal 1997;16:1131-4.
18
McFarland LV, Brandmarker SA, Guandalini S. Pediatric Clostridium difficile: a
phantom menace or clinical reality? Journal of Pediatric Gastroenterology and
Nutrition 2000;31:220-31.
19
Karlstrom O, Fryklund B, Tullus K, Burman LG. A prospective nationwide study of
Clostridium difficile-associated diarrhea in Sweden. The Swedish C. difficile Study
Group. Clinical Infectious Diseases 1998;26:141-5.
Kyne L, Merry C, O’Connell B, Keane C, O’Neill D. Community-acquired
Clostridium difficile infection. Journal of Infection 1998;36:287-8.
20
21
WHO Guidelines for Drinking Water Quality
http://www.who.int/water_sanitation_health/dwq/guidelines/en/
22
Nath KJ, Bloomfield SF and Jones MV, Household water storage, handling and
point-of-use treatment (2005) International Scientific Forum on Home Hygiene.
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/a639aacb2d462a2180257506004d35db/aa885
658ec1f19ee8025752200559653?OpenDocument
23
Goldmann DA. Transmission of viral respiratory infections in the home. Pediatric
Infectious Disease Journal 2000;19(10 suppl):S97-102.
Bloomfield SF, Aiello AE, Cookson B, O’Boyle C, Larson EL. The effectiveness of
hand hygiene procedures including handwashing and alcohol-based hand sanitizers
in reducing the risks of infections in home and community settings. American Journal
of Infection Control 2007;35(suppl 1):S1-64.
24
25
Lo JY, Tsang TH, Leung YH, Yeung EY, Wu T, Lim WW. Respiratory infections
during SARS outbreak, Hong Kong, 2003. Emerging Infectious Diseases
2005;11:1738-41.
47
26
Ewig S, Birkner N, Strauss R, Schaefer E, Pauletzki J, Bischoff H, Schraeder P,
Welte T, Hoeffken G. New perspectives on community-acquired pneumonia in
388,406
patients.
Thorax
published
online
18
May
2009;
doi:10.1136/thx.2008.109785
27
Gem JE, Busse WW. The effects of rhinovirus infections on allergic airway
responses. American Journal of Respiratory and Critical Care Medicine
1995;152:S40-5.
28
Thompson WW, Shay DK, Brammer L, Cox N, Anderson LJ, Fukuda K. Mortality
associated with influenza and respiratory syncytial virus in the United States. Journal
of the American Medical Association 2003;289:179-86.
29
Larson EL. Warned, but not well armed: preventing viral upper respiratory
infections in households. Public Health Nursing 2007;24:48-59.
30
Kamps BS, Reyes-Terán G, Preiser W. Influenza Report 2006. Available from:
http://www.influenzareport.com/ir/overview.htm
31
Gupta RK, Toby M, Bandopadhyay G, Cooke M, Gelb D, Nguyen-Van-Tam JS.
Public understanding of pandemic influenza, United Kingdom [letter]. Emerging
Infectious Diseases [serial on the Internet]. 2006 Oct.
http://www.who.int/csr/resources/publications/influenza/WHO_CDS_CSR_GIP_2005
_5.pdf
32
Pereira AJ, Broadbent J, Mahgoub H, Morgan O, Bracebridge S, Reacher M,
Ibbotson S, Lee JV, Harrison TG, Nair P. Legionnaires' disease: when an 'outbreak'
is not an outbreak. Euro Surveill. 2006;11(48):pii=3089. Available online:
http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=3089
33
Legionellose im Jahr 2006. Robert Koch Institute Epidemiologisches Bulletin 2007;
50:469-73.
34
Borella P, Montagna MT, Romano-Spica V, Stampi S, Stancanelli G, Triassi M,
Neglia R, Marchesi I, Fantuzzi G, Tatò D, Napoli C, Quaranta G, Laurenti P, Leoni E,
De Luca G, Ossi C, Moro M, Ribera D'Alcalà G. Legionella infection risk from
domestic hot water. Emerging Infectious Diseases. 2004;10(3):457-64. Erratum in:
Emerging Infectious Diseases 2004;10(7):1353.
35
Leoni E, De Luca G, Legnani PP, Sacchetti R, Stampi S, Zanetti F. Legionella
waterline colonization: detection of Legionella species in domestic, hotel and hospital
hot water systems. Journal of Applied Microbiology 2005;98:373-9.
36
Lowy FD. Staphylococcus aureus infections. New England Journal of Medicine
1998;339:520-32.
37
Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus
aureus: epidemiology, underlying mechanisms, and associated risks. Clinical
Microbiology Reviews 1997;10:505-20.
38
Graham PL, Lin SX, Larson EL. A US population-based survey of Staphylococcus
aureus colonization. Annals of Internal Medicine 2006;144:318-25.
48
39
Hayward A, Knott F, Petersen I, Livermore DM, Duckworth G, Islam A. Increasing
hospitalizations and general practice prescriptions for community-onset
staphylococcal disease, England. Emerging Infectious Diseases [serial on the
Internet]. 2008 May [date cited]. Available from
http://www.cdc.gov/EID/content/14/05/720.htm.
40
Klein E, Smith DL, Laxminarayan R. Community-associated Methicillin- Resistant
Staphylococcus aureus in Outpatients, United States, 1999–2006. Emerging
Infectious Diseases 2009;15:1925-30.
41
Skov RL, Jensen KS. Community-associated methicillin resistannt Staphylococcus
aureus as a cause of hospital-acquired infections. Journal of Hospital Infection
2009;73:364-70.
42
Miller R, Esmail H, Peto T, et al. Is MRSA admission bacteraemia community
acquired? A case control study. Journal of Infection 2008;56:163-70.
43
Cole E. Allergen control through routine cleaning of pollutant reservoirs in the
home environment. Proceedings of Healthy Building 2000;4:435-6.
44
Cook CE, Cole EC, Dulaney PD, Leese KE. Reservoirs of opportunistic fungi in the
home environment: a guide for exposure reduction in the immunocompromised.
Proceedings of 8th International Conference on Indoor Air Quality and Climate
1999;1:905-9.
45
Warnock DW, Campbell CK. Medical Mycology. Mycological Research
1996;100:1153-62.
Stevens D. Fungi in the domestic environment and community settings –
association with health problems (2004). International Scientific Forum on Home
Hygiene. Available from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/f5236e2da2822fef8025750b000dc985/2611f43
1855806f2802575220056347c?OpenDocument
46
47
Scott E. Microbial Risk Reduction: The Benefits of Effective Cleaning. 2010 In
preparation
48
BMA submission to the Lords Select Committee into antimicrobial resistance.
London: British Medical Association, 1997.
49
Schmitz F-J, Verhoef J, Idel H, Hadding U, Heinz HP, Jones ME. Impact of
hygienic measures on the development of methicillin resistance among staphylococci
between 1991 and 1996 in a university hospital. Journal of Hospital Infection
1998;38:237-40.
50
EU Scientific Steering Committee in its opinion on Antimicrobial Resistance
(adopted on 28 May 1999): http://ec.europa.eu/food/fs/sc/ssc/out50_en.pdf
51
European Centre for Disease Control and Prevention 2009. Antibiotic resistance.
http://www.ecdc.europa.eu/en/healthtopics/Pages/Antimicrobial_Resistance.aspx
49
52
The e-Bug project. UK Health Protection Agency. The e-Bug project - a European
wide, DG SANCO funded, antibiotic and hygiene teaching resource for junior and
senior school children. Available from:
http://www.e-bug.eu/ebug.nsf/Home?OpenPage
53
Moreno JS, Griffiths PL, Connerton IF, Park RWA. Occurrence of campylobacters
in small domestic and laboratory animals. Journal of Applied Bacteriology
1993;75:49-54.
54
Wall PG, Threllfall EJ, Ward LR, Rowe B. Multiresistant Salmonella typhimurium
DT104 in cats: a public health risk. Lancet 1996;348:471.
55
Hald B, Madsen M. Healthy puppies and kittens as carriers of Campylobacter spp.,
with special reference to Campylobacter upsaliensis. Journal of Clinical Microbiology
1999;35:3351-2.
56
Baker J, Barton MD, Lanser J. Campylobacter species in cats and dogs in South
Australia. Australian Veterinary Journal 1999;77:662-6.
57
Harrison SJ. The prevalence of Campylobacter upslaiensis in cats. PHLS 25th
Annual scientific conference, Sept 2000, PHLS Colindale, London.
58
Cefai C, Ashurst S, Owens C. Human carriage of methicillin-resistant
Staphylococcus aureus linked with pet dog. Lancet 1994;344:539-40.
59
Manian FA. Asymptomatic nasal carriage of mupirocin resistant, methicillinresistant Staphylococcus aureus (MRSA) in a pet dog associated with MRSA
infection in household contacts. Clinical Infectious Diseases 2003;36:26-8.
Rankin S, Roberts S, O’Shea K, Maloney D, Lorenzo M, Benson CE. Panton
valentine leukocidin (PVL) toxin positive MRSA strains isolated from companion
animals. Veterinary Microbiology 2005;108:145-8.
60
61
van Duijkeren E, Wolfhagen MJ, Box AT, Heck ME, Wannet WJ, Fluit AC. Humanto-dog transmission of methicillin-resistant Staphylococcus aureus. Emerging
Infectious Diseases 2004;10:2235-7.
62
Borriello SP, Honour P, Turner T, et al. Household pets as a potential reservoir for
Clostridium difficile infection. Journal of Clinical Pathology 1983;36:84-7.
63
Sattar SA, Tetro J, Springthorpe VS. Impact of changing societal trends on the
spread of infections in American and Canadian homes. American Journal of Infection
Control 1999;27:S4-21.
64
Centre for Diseases Control and Prevention. Preliminary FoodNet data on the
incidence of infection with pathogens transmitted commonly through food – 10 states,
2007 April 11, 2008 / 57(14);366-370. Available at:
http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5714a2.htm
65
Stenberg A, Macdonald C, Hunter PR. How effective is good domestic kitchen
hygiene at reducing diarrhoeal disease in developed countries? A systematic review
and reanalysis of the UK IID study. BMC Public Health 2008, 8:71-9.
50
66
Schutze GE, Sikes JD, Stefanova R, Cave MD. The home environment and
Salmonellosis in children. Pediatrics 1999;103:E11-5.
67
Scott EA, Duty S, McCue K. A critical evaluation of methicillin-resistant S aureus
and other bacteria of medical interest on commonly-touched household surfaces in
relation to household demographics. American Journal of Infection Control 2009; in
press.
68
Morris JG, Potter M. Emergence of new pathogens as a function of changes in
host susceptibility. Emerging Infectious Diseases 1997;3:435-41.
69
Centers for Disease Control and Prevention. Assessing the public health threat
associated with waterborne cryptosporidiosis: report of a workshop. MMWR Morbidity
and Mortality Weekly Report 1995;44(RR-6):19.
70
United Network for Organ Sharing, 1997 report of center specific graft and patient
survival rates, UNOS, Richmond, VA, and the Division of Transplantation, Office of
Special Programs, Health Resources and Services Administration, US Department of
Health and Human Services, Rockville (MD) (1997).
71
Semenza JC, Gieseke J. Intervening to reduce inequalities in infections in Europe.
American Journal of Public Health 2008;98:787-92.
72
Tauxe RV. Emerging foodborne diseases: an evolving public health challenge.
Emerging Infectious Diseases 1997;3425-34.
73
Buchanan RL, Klawitter LA. Effect of temperature history on the growth of Listeria
monocytogenes Scott A at refrigeration temperatures. International Journal of Food
Microbiology 1991;12:235-46.
74
Bates CJ, Spencer RC. Survival of Salmonella species in eggs poached using a
microwave oven. Journal of Hospital Infection 1995;29:121-7.
75
Hollywood NW, Varabioff Y, Mitchell GE. The effect of microwave and conventional
cooking on the temperature profiles and microbial flora of minced beef. International
Journal of Food Microbiology 1991;14:67-75.
76
Evans MR, Parry SM, Ribeiro CD. Salmonella outbreak from microwave cooked
food. Epidemiology and Infection 1995;115:227-30.
77
Scott E, Sockett P. How to Prevent Food Poisoning: A Practical Guide to Safe
Cooking, Eating and Food Handling. New York: John Wiley & Sons, 1998.
78
Mattick K, Durham K, Domingue G, Jorgensen F, Sen, M, Schaffner DW,
Humphrey T. The survival of foodborne pathogens during domestic washing-up and
subsequent transfer onto washing-up sponges, kitchen surfaces and food.
International Journal of Food Microbiology 2003;85(3):213-26.
79
Sattar SA, Tetro J, Springthorpe VS. Impact of changing societal trends on the
spread of infections in American and Canadian homes. American Journal of Infection
Control 1999;27:S4-21.
51
80
Kniehl E, Becker A, Forster DH. Bed, bath and beyond: pitfalls in prompt
eradication of methicillin-resistant Staphylococcus aureus carrier status in healthcare
workers. Journal of Hospital Infection 2005;59:180-7.
81
Ansari SA, Springthorpe VS, Sattar SA. Survival and vehicular spread of human
rotaviruses: possible relation to seasonality of outbreaks. Reviews of Infectious
Diseases 1991;13:448-61.
82
Menzies D, Bourbeau J. Building-related illnesses. New England Journal of
Medicine 1997;337:1524-31.
83
Skirrow MB. Campylobacteriosis. In: Palmer SR, Soulsby Lord, Simpson DIH, eds.
Zoonoses. Oxford: Oxford University Press, 1998;37-46.
84
Forman D. Helicobacter pylori infection and cancer. British Medical Bulletin
1998;54(1):71-8.
85
Allos BM. Association between Campylobacter infection and Guillain-Barré
syndrome. Journal of Infectious Diseases 1997;176(suppl 2):S125-8.
86
Ribeiro CD, Frost JA. Family cluster of Campylobacter infection. Communicable
Disease and Public Health 2000;3:274-6.
87
Lindsay JA. Chronic sequelae of foodborne disease. Emerging Infectious Diseases
1997;3:443-52.
88
Opinion of the Scientific Committee on Veterinary Measures relating to Public
Health. Brussels: European Commission, 2000: EC DG24.
89
Hament JM, Klimpen JL, Fleer A, Wolfs TF. Respiratory viral infection predisposing
for bacterial diseases: a review. FEMS Immunology and Medical Microbiology
1999;26:189-95.
90
Reid DW, Bromly CL, Stenton SC, Hendrick DJ, Bourke SJ. A double-blind
placebo-controlled study of the effect of influenza vaccination on airway
responsiveness in asthma. Respiratory Medicine 1998;92:1010-1.
91
Oliver BGG, Lim S, Wark P, et al. Rhinovirus exposure impairs immune responses
to bacterial products in human alveolar macrophages. Thorax 2008;63:519-25.
92
Khetsuriani N, Lu X, Teague GW, et al. Novel human rhinoviruses and
exacerbation of asthma in children. Emerging Infectious Diseases 2008;14:1793-6.
93
Openshaw PJ, Yamaguchi Y, Tregoning JS. Childhood infections, the developing
immune system, and the origins of asthma. Journal of Allergy and Clinical
Immunology 2004;114:1275-7.
94
Jackson DJ, Gangnon RE, Evans MD, et al. Wheezing rhinovirus illnesses in early
life predict asthma development in high risk children. American Journal of
Respiratory and Critical Care Medicine 2008;178(7):667-72.
95
Dharmage SC, Erbas B, Jarvis D, et al. Do childhood respiratory infections
continue to influence adult respiratory morbidity? European Respiratory Journal
2009;33(2):237-44.
52
96
Richardson SJ, Willcox A, Bone AJ, Foulis AK, Morgan NG. The prevalence of
enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1
diabetes. Diabetologia. 2009 Mar 6. [Epub ahead of print]
97
Weber MA, Klein NJ, Hartley JC, Lock PE, M Malone M, Sebire NJ. Infection and
sudden unexpected death in infancy: a systematic retrospective case review. Lancet
2008; 371:1848-53.
98
Blackwell C. Bacterial toxins and sudden unexpected death in infancy. Lancet
2008;372:714.
99
Prtak L, Cohen M, Fenton P, Adnani M, Kudesia G. Bacterial toxins and sudden
unexpected death in infancy. Lancet 2008;372:715.
100
Goldwater PN. Sterile site infection at autopsy in sudden unexpected deaths in
infancy. Archives of Disease in Childhood 2008. Published online first: 15 September
2008. doi:10.1136/adc.2007.135939.
101
Bloomfield SF. Preventing infection in the home. Br J Infect Control. 2002;3(1):714:14-7.
Bloomfield S, Exner M, Fara GM, Scott EA. Prevention of the spread of infection –
the need for a family-centred approach to hygiene promotion Eurosurveillance,
Volume 13, Issue 22, 29 May 2008 available at:
http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=18889
102
103
Larson E, Aiello AE. Systematic risk assessment methods for the infection control
professional. Am J Infect Control 2006;34(5):323-6.
Sax H, Allegranzi B, Uçkay I, Larson E, Boyce J, Pittet D. ‘My five moments for
hand hygiene’: a user-centred design approach to understand, train, monitor and
report hand hygiene. Journal of Hospital Infections 2007;67(1):9-21.
104
105
Barker J, Bloomfield SF. Survival of Salmonella in bathrooms and toilets in
domestic homes following salmonellosis. Journal of Applied Microbiology
2000;89(1):137-44.
106
Bloomfield SF, Scott EA. Cross-contamination and infection in the domestic
environment and the role of chemical disinfectants. Journal of Applied Microbiology
1997;83:1-9.
107
Bloomfield SF. Preventing infection in the home. British Journal of Infection
Control 2002;3:14-7.
108
Barker J, Jones MV. The potential spread of infection caused by aerosol
contamination of surfaces after flushing a domestic toilet. Journal of Applied
Microbiology 2005;99:339-47.
109
Barker J, Naeeni M, Bloomfield SF. The effects of cleaning and disinfection in
reducing Salmonella contamination in a laboratory model kitchen. Journal of Applied
Microbiology 2003;95:1351-60.
53
110
Barker J, Vipond IB, Bloomfield SF. The effects of cleaning and disinfection in
reducing the spread of Norwalk-like virus contamination via environmental surfaces.
Journal of Hospital Infections 2004;58:42-9.
111
Exner M, Vacata V, Hornei B, Dietlein E, Gebel J. Household cleaning and
surface disinfection: new insights and strategies. Journal of Hospital Infections
2004;56 (suppl 2):S70-5.
112
Home hygiene - prevention of infection at home: a training resource for carers and
their trainers. International Scientific Forum on Home Hygiene. Available from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/571fd4bd2ff8f2118025750700031676/9aaaeb3
06bb3c50c80257522004b4fdc?OpenDocument
113
Beumer R, Bloomfield SF, Exner M, Fara GM, Nath KJ, Scott EA. Hygiene
procedures in the home and their effectiveness: a review of the scientific evidence
base (2008). International Scientific Forum on Home Hygiene. Available from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/111e68ea0824afe1802575070003f039/c9bf235
b5d76ad09802572970063c5d8?OpenDocument
114
Cogan TA, Bloomfield SF, Humphrey TJ. The effectiveness of hygiene procedures
for the prevention of cross contamination from chicken carcasses in the domestic
kitchen. Letters in Applied Microbiology 1999;29:354-8.
115
Cogan TA, Slader J, Bloomfield SF, Humphrey TJ. Achieving hygiene in the
domestic kitchen: the effectiveness of commonly-used cleaning products. Journal of
Applied Microbiology 2002;92:885-92.
116
Food Standards Agency 2009. A UK survey of Campylobacter and Salmonella
contamination
of
fresh
chicken
at
retail
sale.
Available
from:
http://www.food.gov.uk/multimedia/pdfs/fsis0409.pdf
117
Waterman SR, Small PL. Acid sensitive enteric pathogens are protected from
killing under extremely acidic conditions of pH 2.5 when they are inoculated into
certain solid food sources. Applied Environmental Microbiology 1998;64:3882-6.
Gillespie IA, O’Brien SJ, Adak KA. (2001) General outbreaks of infectious
intestinal disease linked with private residences in England and Wales 1992-9:
questionnaire study. British Medical Journal 2001;323;1097-8.
118
119
Caul EO. Small round structured viruses: airborne transmission and hospital
control. Lancet 1994;343:1240-2.
120
Centers for Disease Control and Prevention. Methicillin-resistant Staphylococcus
aureus skin or soft tissue infections in a state prison - Mississippi, 2000. MMWR
Morbidity Mortality Weekly Report 2001;50:919-22.
121
Centers for Disease Control and Prevention. Outbreak of community associated
methicillin-resistant Staphylococcus aureus skin infections - Los Angeles County,
California, 2002-2003. MMWR Morbidity Mortality Weekly Report 2003; 52: 88.
122
Purcell K, Fergie JE. Exponential increase in community-acquired methicillinresistant Staphylococcus aureus infections in South Texas children. Pediatric
Infectious Disease Journal 2002; 21: 988-9.
54
123
Moran GJ, Amii RN, Abrahamian FM, Talan DA. Methicillin-resistant
Staphylococcus aureus in community acquired skin infections. Emerging Infectious
Disease 2005;11:928-30.
124
Dietrich DW, Auld DB, Mermel LA. Community-acquired methicillin-resistant
Staphylococcus aureus in Southern New England Children. Pediatrics 2004;113:34752.
125
Johnson LB, Louis D, Saravolatz L. Community-acquired MRSA: current
epidemiology and management issues. Infectious Medicine 2005;22:16-20.
126
Chemical-Thermal Linen Disinfection. DGHM Standard Methods for Chemical
Disinfection Process Testing 2001 German: German Society for Hygiene and
Microbiology, Berlin, Germany.
127
Haas CN, Marie JR, Rose JB, Gerba CP. Assessment of benefits from use of
antimicrobial hand products: reduction in risk from handling ground beef.
International Journal of Hygiene and Environmental Health 2005;208:461-6.
128
Aiello AE, Larson EL, Sedlak R. .Hidden heroes of the health revolution Sanitation
and personal hygiene. American Journal of Infection Control 2008; 36(suppl 3):S128151.
129
The infection potential in the domestic setting and the role of hygiene practice in
reducing infection (2002). International Scientific Forum on Home Hygiene. Available
from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/f5236e2da2822fef8025750b000dc985/9df1597
d905889868025729700617093?OpenDocument
130
Aiello AE, Larson EL, Sedlak R. Personal health bringing good hygiene home.
American Journal of Infection Control 2008; 36(suppl 3):S152-65
EN14885 Chemical disinfectants and antiseptics – Application of European
standards for chemical disinfectants and antiseptics. British Standards Institute,
London, UK.
131
132
Guidelines for prevention of infection and cross infection the domestic
environment. (2004) International Scientific Forum on Home Hygiene. Available from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/70f1953cec47d5458025750700035d86/92111a
e38986bfbb802574dd003fc2c1?OpenDocument
133
Recommendations for suitable procedure for use in the domestic environment
(2001). International Scientific Forum on Home Hygiene. Available from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/70f1953cec47d5458025750700035d86/24401f
935e57e79e802574e200391c43?OpenDocument
134
Griffith C, Redmond E. Evaluating hygiene behaviour in the domestic setting and
the impact of hygiene behaviour. Journal of Infection 2001;43:70-4.
135
Pittet D. Improving adherence to hygiene practice: a multidisciplinary approach.
Emerging Infectious Diseases 2001;7:234-40.
55
136
Curtis V. Talking dirty: how to save a million lives. International Journal of
Environmental Health Research 2003;13 Suppl 1:S73-80.
137
Whitby M, Pessoa-Silva CL, McLaws ML, Allegranzi B, Sax H, Larson E, et al.
Behavioural considerations for hand hygiene practices: the basic building blocks.
Journal of Hospital Infections 2007;65:1-8.
138
Stanwell Smith R, Bloomfield SF. The hygiene hypothesis and implications for
home hygiene. (2004) International Scientific Forum on Home Hygiene. Available
from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/111e68ea0824afe1802575070003f039/ce9bc2
e0228ad9d480257522005b4748?OpenDocument
139
Bloomfield SF, Stanwell-Smith R. Crevel RWR, Pickup J. Too clean, or not too
clean: the Hygiene Hypothesis and home hygiene. Clinical and Experimental Allergy
2006; 36:402-25.
140
Bremner SA, Carey IM, DeWilde S, Richards N, Maier WC, Hilton SR, Strachan
DP, Cook DG. Infections presenting for clinical care in early life and later risk of hay
fever in two UK birth cohorts. Allergy 2008;63(3):274–83.
141
Rook GAW, Rosa Brunet L. Old friends for breakfast. Clinical and Experimental
Allergy. 2005;35:841–42.
142
Reid DW, Bromly CL, Stenton SC, Hendrick DJ, Bourke SJ. A double-blind
placebo-controlled study of the effect of influenza vaccination on airway
responsiveness in asthma. Respiratory Medicine 1998;92:1010-1.
143
Oliver BGG, Lim S, Wark P, et al. Rhinovirus exposure impairs immune responses
to bacterial products in human alveolar macrophages. Thorax 2008;63:519-25.
144
Khetsuriani N, Lu X, Teague GW, et al. Novel human rhinoviruses and
exacerbation of asthma in children. Emerging Infectious Diseases 2008;14:1793-6.
145
Are we too clean: a report of a symposium on the hygiene hypothesis and its
implications at the Royal Institute of Public Health, London, September 2002.
Available from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/111e68ea0824afe1802575070003f039/5febdba
bad45d9558025753c00554b5c?OpenDocument
146
Beumer R, Bloomfield SF, Exner M, Fara GM, Nath KJ, Scott, EA. Microbial
resistance and biocides - a review and consensus statement (2000). International
Scientific Forum on Home Hygiene. Available from:
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/111e68ea0824afe1802575070003f039/f309bd6
a403617fa80257522005bc5f9?OpenDocument
147
Beumer R, Bloomfield SF, Exner M, Fara GM, Nath KJ, Scott, EA. Biocide usage
and antimicrobial resistance in home settings: an update (2004). International
Scientific Forum on Home Hygiene. Available from:
56
http://www.ifhhomehygiene.org/IntegratedCRD.nsf/111e68ea0824afe1802575070003f039/cc7769
a53d5cd88780257522005c0093?OpenDocument
148
Assessment of the Antibiotic Resistance Effects of Biocides. European
Commission. Scientific Committee on Emerging and Newly Identified Health Risks
2009. Available from:
http://ec.europa.eu/health/ph_risk/committees/04_scenihr/docs/scenihr_o_021.pdf
149
Influenza Communication Toolkit. European Centre for Disease Control and
prevention. Available from:
http://ecdc.eu.int/Health_topics/Seasonal%20Influenza/toolkit/index.html
150
Catch it, Bin it, Kill it - Respiratory and hand hygiene campaign 2007-2008. UK
Department of Health. Available from:
http://www.dh.gov.uk/en/Publicationsandstatistics/Publications/PublicationsPolicyAnd
Guidance/DH_080839
57