The concept of acquiring infectious agents from contact with contaminated surfaces is age-old and predates the germ theory of disease. The Book of Leviticus in the Old Testament of the Bible cites religious guidelines that apparently were intended not only to limit the acquisition of foodborne parasitic worms but also to limit the spread of infectious agents through contaminated drinking water and environmental surfaces, such as eating utensils and clothing, capable of transmitting infectious agents (pathogens).
In more modern times, concerns about public health issues date back to at least the mid-19th century and to the work of the sanitary reformers, who themselves were the precursors of the public health movement. The history of the development of hygiene and cleaning practices in the home dates to approximately the same period.
In recent years, there has been a significant shift in attitudes about microbes in our environment and their association with human health and disease. The revised viewpoints are likely to have a profound effect on hygiene
On the one hand, infectious diseases, including community-based infections such as respiratory, gastrointestinal, and skin infections, continue to exert a heavy toll on human health and prosperity.2
The problem is exacerbated by the aging of the population and the associated increase in percentage (approximately 20%) of immunocompromised individuals living in the community, who are often cared for at home.3
Contrary to predictions made during the mid-20th century, infectious diseases have clearly not been eradicated. Indeed, new infectious agents (eg, Zika virus, severe acute respiratory syndrome coronavirus [SARS-CoV], Middle East respiratory syndrome coronavirus [MERS-CoV], Ebola virus, pandemic influenza strains, Vibrio cholerae
, Escherichia coli
0157, and Yersinia pestis
) continue to emerge and/or reemerge globally. In addition, the emergence of antibiotic-resistant pathogens (eg, methicillin-resistant Staphylococcus aureus
[MRSA] and multidrug-resistant Mycobacterium tuberculosis
) has become, and continues to represent, a massive global concern. The concern is not only the risk in health care settings but also the risk in the home and general public settings. It is hard to overstate the risk associated with the emergence of such multidrug-resistant pathogens. The government of the United Kingdom has referred to this issue as a post-antibiotic apocalypse
, which threatens to kill 10 million people globally by 2050.4
At the same time, there also is much concern about the rapid rise in allergies (especially asthma and food allergies) and other chronic inflammatory diseases (CID). The hygiene hypothesis
proposed by Strachan5
postulated that a lower incidence of early childhood infection (predominantly in first-world countries) might explain the rapid rise of allergic diseases during the 20th century. As discussed in a 2016 review by Bloomfield et al,6
our current understanding of host-microbiome interactions and immune dysfunction suggests that increases in CID are the combined result of lifestyle, medical, and public health (hygiene
and sanitation) changes, all of which have deprived humans of exposure to potentially beneficial microbial agents currently described as old friends
(OF), particularly in early life.6
These OF microbes are not pathogenic (as argued by Strachan5
) and include nonharmful species that inhabit the human gastrointestinal tract and our natural environment. Based on these immunologic understandings, Dowling7
has introduced the concept of age-appropriate and health-appropriate hygiene practices for home and everyday life
. Such practices include age-appropriate vaccination and exposure to nonharmful microbes that prime the immune system.8
It is now widely accepted that the hygiene hypothesis
of Strachan resulted in the inherently dangerous concept of our being too clean
that has persisted in the media and in the minds of the public. The general public, as a result, now appears to be confused about the real meaning and value of hygiene
. This is happening at a time when health agencies worldwide are emphasizing the necessity of basic hygiene
practices at both the individual and community levels. Most importantly, hygiene
is now being seen as a key component of strategies to tackle the global problem of antibiotic resistance. It is hoped that by reducing the level of infections, fewer people will need to seek antibiotic treatment, thereby limiting the selective pressure for generating antibiotic-resistant strains of pathogens. A balance in the use of hygiene practices, such as surface decontamination or hand antisepsis, in order to fight pathogens and the restoration of natural microbial diversity is, therefore, thought to be essential for enabling a healthy coexistence with the microbial world (ie, “bidirectional hygiene
” or “bygiene”), a concept introduced by Al-Ghalith and Knights.9
The purpose of this chapter is to take a more holistic look at the risks posed by pathogen-contaminated surfaces, primarily in general living areas such as homes, by (1) taking a closer look at pathogen-contaminated environmental sites and surfaces in home and community settings in order to assess their roles for transmission of infectious agents; (2) exploring the role of human hands in disseminating infectious agents between common-touch surfaces (ie, the role of the air-surface-hands nexus in the chain of infection); (3) considering the current use of chemical and physical decontamination procedures; and (4) looking toward the future, including new technologies and probiotics, the potential insights to be gained from microbiome studies of the indoor environment, and best approaches for communicating information about targeted hygiene and surface decontamination practices in everyday settings.
Globally, the home captures a large cross-section of the human population in terms of age, health, nutritional status, and susceptibility to infectious agents and is, therefore, representative of many other community settings in terms of the necessity for hygiene practices. A constant dynamic exists between the home and other settings (day care, work, school, travel, leisure, health care, etc) in terms of the dissemination of infectious agents from infected individuals, contaminated food, and domesticated animals to surfaces and, via the intermediacy of human hands, through the entire cycle of reinfection. In day care settings, young children are immunologically immature and exhibit behaviors that may encourage transmission of infectious agents (eg, poor personal hygiene and mouthing of objects). Problems associated with day care staffing and varying educational levels may compound the problem.
In determining the role that surfaces play in the transmission of disease, it is important first to develop a working definition of inanimate surface contamination. The chain of events leading to the occurrence and spread of infectious agents is then discussed. With the recognition that decontamination of environmental surfaces may not be necessary in all situations, the prudent use of effective targeted approaches as a possible means of reducing the burden of infectious agents is described.
The terminology that is commonly used for surface contamination includes the word fomite
(an environmental surface that might be contaminated and then serve as a vehicle for dissemination of the infectious agent) and terms describing a subclass of fomites, namely common-touch surfaces
(also referred to as high frequency-touch surfaces
[HITES] in health care settings).10 Common-touch surfaces
include fomites such as door knobs, toilet flush handles, faucet handles, light switches, remote controls, cell phones, and other digital devices. The concern over common-touch surfaces
reflects the important role that hands play in the dissemination of infectious agents in everyday settings.
To define the risk associated with surface contamination, several factors must be considered. These include (1) the presence of pathogenic contaminants in the environment and their minimum infective doses (MID), (2) the length of time over which such pathogens remain viable and infectious on fomites, and (3) the likelihood of their being transferred from such fomites to a new host. We must also consider the types of common-touch surfaces
that are most likely to become contaminated in the home. Pathogens travel via well-defined routes from an infected source to another individual. Numerous sampling studies have recorded the presence of both pathogenic bacteria, fungi, parasites, and viruses as well as nonpathogenic microbes on environmental surfaces in home and community settings. Both laboratory and field studies have evaluated the rates of transfer of pathogens via hands and common-touch surfaces
, as reviewed by Bloomfield et al.3
These studies demonstrate that the surfaces with the highest risk of transmitting pathogens and which are, therefore, the critical control points in the transmission of infection, are the hands, common-touch surfaces
, food-contact surfaces, and the cleaning utensils used on these surfaces, as shown in Figure 48.1
For an infection to result from human contact with a contaminated surface, the following must be in place: (1) the presence of an infectious agent (implying the existence of a source or reservoir for the pathogen), (2) a means or mode of transmission, and (3) the presence of a susceptible host. The greatest risk is associated with hosts characterized as at higher risk for infection (ie, the very young, very old, immunocompromised, malnourished, etc), although potentially any individual may be at risk of acquiring infectious agents from pathogen-contaminated surfaces. The cycle of pathogen contamination of surfaces leading to the reinfection of a new host, and possible approaches for interruption of this cycle, are displayed in Figure 48.2
. The overwhelming importance of the human hand in dissemination of pathogens that have been deposited on surfaces is depicted by the placement of the hands at the top of this figure. We return to the theme of the airsurface-hand nexus
throughout this chapter to emphasize that the surfaces serve as reservoirs for contamination, and the hand and air are primary disseminators for the contamination to other hosts and surfaces.
Ranking of sites and surfaces based on risk of transmission of infection through the intermediacy of the hand. The filled dots and unfilled dots represent pathogenic and nonpathogenic microorganisms, respectively. For a color version of this art, please consult the eBook. Modified from Bloomfield et al.6
Copyright © 2016 SAGE Publications.
Targeting those common-touch surfaces
at high risk for pathogen transmission/acquisition by hosts and applying appropriate decontamination practices form the basis for an evidence-based hygiene
policy known as targeted hygiene
. Targeted hygiene
is intended to manage the microbial diversity of environmental surfaces as well as the human microbiome6
and incorporates the novel concept of bygiene
DISSEMINATION OF PATHOGENS BY ENVIRONMENTAL SURFACES
may become contaminated by pathogens and subsequently serve as reservoirs for transmission of infectious agents through the intermediacy of the human hand.2
Knowledge of, and focus of remediation efforts on, such common-touch surfaces
will have the greatest economic and infectious disease prevention impact. According to the Centers for Disease Control and Prevention,13
80% of infectious diseases are transmitted by contaminated hands and, therefore, the human hand is a common denominator in transmission of infectious agents via common-touch surfaces
. According to this view, high-risk common-touch surfaces
include door knobs/handles, kitchen counters, toilet flush handles, telephone handsets, personal digital electronic devices, shopping carts, handrail belts for escalators and people movers, toys, contaminated fabrics, automated banking teller machines, currency coins and bills, etc (Figure 48.3
). Again, this figure emphasizes the central role of the human hand in dissemination of infectious agents acquired by handling various common-touch objects.
Pathogens that are most likely to be transmitted from common-touch reservoirs are those that are capable of surviving in the absence of a host under ambient conditions following release from a source of infectious agents. For this reason, pathogens of particular concern include nonenveloped viruses, spore-forming bacteria, fungi, and parasitic ova/(oo)cysts. Although the ambient environment is relatively less conducive for survival of vegetative bacteria and enveloped viruses, these also may be disseminated from common-touch surfaces. To better appreciate the risk of pathogen spread via common-touch surfaces and the mitigation of such risk, the following need to be considered:
Certain pathogens may remain infectious outside of a host for extended periods of time.
There is evidence for the recovery of pathogens from environmental surfaces.
The transmission of pathogens from contaminated surfaces to human hands has been demonstrated.
Targeted use of microbicidal products and hygienic practices may disrupt pathogen transfer from environmental surfaces to human hands.
The combination of hygiene practices and education (including knowledge of when, where, and how to apply these practices) can reduce the transmission and thus the risk of infectious diseases in home and community settings.
FIGURE 48.2 The cycle of surface contamination, dissemination, and reinfection and possible approaches for interrupting the cycle.
PATHOGENS MAY REMAIN INFECTIOUS ON SURFACES FOR EXTENDED PERIODS OF TIME IN THE ABSENCE OF A HOST
Pathogens such as bacteria, fungi, viruses (especially nonenveloped), and enteric parasitic ova/(oo)cysts have been found to remain infectious for extended periods of time following contamination of environmental surfaces. For instance, nonenveloped viruses including the adenoviruses, astroviruses, picornaviruses (eg, coxsackie virus, hepatitis A virus, poliovirus, and rhinovirus), caliciviruses (eg, norovirus and feline calicivirus), and reoviruses (eg, rotavirus) have been found to survive for up to 3 months on contaminated environmental surfaces (reviewed by Kramer et al15
and Boone and Gerba11
). On the other hand, enveloped viruses, such as the herpesviruses (eg, cytomegalovirus, herpes simplex), paramyxoviruses (eg, Sendai virus, respiratory syncytial virus), orthomyxoviruses (eg, influenza A and B viruses), and coronaviruses (eg, SARS-CoV, MERS-CoV), and blood-borne retroviruses (eg, human immunodeficiency virus) tend to remain infectious on the order of hours or days, rather than months (Table 48.1
Most gram-positive bacteria, such as Enterococcus species
. (including vancomycin-resistant enterococcus
), S aureus
(including MRSA), or Streptococcus pyogenes
, survive for months on dry surfaces.15
Many gram-negative bacteria, such as Acinetobacter species
, E coli
, Klebsiella species
, Pseudomonas aeruginosa
, Serratia marcescens
, or Shigella species
, can also survive for months.15
The fungal pathogen Candida albicans
can survive up to 4 months on surfaces.15
Enteric parasitic (oo)cysts (Cryptosporidium
) or (oo)cysts (Giardia
) and enteric parasitic ova have been found to survive on experimentally contaminated environmental surfaces (both animate and inanimate) for weeks to months (A. Alum et al, unpublished data, August 19, 2011) (see Table 48.1
High-risk common-touch surfaces
for transmission of pathogens in the home or outside of the home. Adapted from Alum et al.14
Copyright © 2010 International Society for Infectious Diseases. With permission.
In general, it can be assumed that the nonenveloped viruses (hepatitis A, rhinoviruses, noroviruses, and rotaviruses) will survive longer than enveloped viruses. In the case of bacteria, sporeformers (eg, Clostridium difficile
) will survive the longest, and for parasites, the encysted (Cryptosporidium
) forms will survive longer than nonencysted parasites. Vegetative bacteria such as MRSA, Acinetobacter
species, and E coli
may also survive for months. Although enveloped viruses (eg, influenza) may survive only for days, the human minimal infective dose for these viruses may be low enough that, for instance, it might take 6 to 9 days for an influenza-contaminated surface to be rendered noninfectious (see Table 48.1
Surface porosity or roughness, temperature, relative humidity (RH), and presence of organic matter associated with pathogens released from the source are also significant determinants of pathogen survival outside of a host.11
Biofilm formation also promotes persistence of bacteria.33
As a generality, the lower the temperature, the longer the time that the pathogen will remain infectious (see also chapter 67
The presence of organic matter has been found to provide added stability to infectious agents present on contaminated environmental surfaces.16
Indoor air temperature, RH, presence of organic load, and types of environmental surfaces (hard/soft and porous/nonporous) have each been shown to impact the survival of viruses. At room temperature, survival of enveloped viruses such as transmissible gastroenteritis virus and murine hepatitis virus (surrogates for SARS-CoV) on surfaces is greater at relatively low RH (20%),21
whereas human coronavirus 229E has been reported to persist on six surface materials common to communal and domestic environments for at least 5 days under
ambient conditions (21°C; RH, 30%-40%).19
At room temperature, nonenveloped viruses (eg, picornaviruses including poliovirus and murine norovirus [used as a surrogate for human norovirus]) remain infectious longer on surfaces at higher RH,32
with the exception of rotavirus and hepatitis A virus, which survive best at a low to medium RH.36
TABLE 48.1 Examples for survival of pathogens on fomites in the absence of decontamination and duration of time required to reach a noninfectious state
Minimum Infective Dose
ki (Log10 Reduction in Titer/d)
Time Needed for 3 Log10 Reductiona
Time Needed to Get Below MIDb
Adenovirus 40 (Abad et al16)
Feline calicivirus (Doultree et al17)
Hepatitis A virus (Abad et al16)
Rhinovirus 14 (Sattar et al18)
Rotavirus p13 (Abad et al16)
Coronavirus 229E (Warnes et al19)
Influenza virus (Bean et al20)
Mouse hepatitis virus (Casanova et al21)
Transmissible gastroenteritis virus (Casanova et al21)
Acinetobacter species (Otter and French22)
Campylobacter jejuni (Humphrey et al23)
500 organisms (Kothary and Babu24)
Clostridium difficile (Otter and French22)
Escherichia coli (Wilks et al25)
>105 organisms (Kothary and Babu24)
Staphylococcus aureus (Otter and French22)
103-105 organisms (Otter and French22)
Candida albicans (Traoré et al26)
Cryptosporidium parvum (Alum et al30)
10 (oo)cysts (Kothary and Babu24)
1000 organisms (Health Canada Pathogen Safety Data Sheets27)
Giardia muris (Alum et al30)
10 (oo)cysts (Stachan and Kunstýr28)
Abbreviations: ki, inactivation constant; MID, minimum infective dose; TCID50, tissue culture infective dose50.
a The time in days for 1 log10 inactivation = 1 / ki. For the days required to obtain 3 log10 inactivation, multiply the days required for 1 log10 inactivation by 3.
b Assumes an initial burden of 106 pathogens. The log10 reduction needed to achieve a bioburden 1 log10 lower than the lowest MID is divided by ki to arrive at the time required (days).
c Nonporous surfaces include aluminum, stainless steel, and glass.
d Examples of porous surfaces include paper, latex glove, and cloth.