Inanimate objects in the built environment can serve as reservoirs of microbial matter. Each of these objects is host to an entire community composed of a wide variety of bacterial, viral, archaeal, protistan, and fungal organisms, including potential pathogens and microbial metabolic products harmful to humans.

Microbial Community Ecology on Fomite Surfaces

On indoor surfaces that lack abundant moisture and nutrient availability, most microorganisms that arrive from other environments (such as from human occupants) are generally considered unlikely to survive, and those viable microbes that do survive are generally considered to be inactive or dormant until transferred to other host locations or until they experience an influx of moisture and nutrients that help them proliferate [4••, 50,51,52]. Surveys of fungal communities in indoor environments, conducted using high-throughput molecular sequencing, have shown that they tend to be driven primarily by transport from the local outdoor environment [31]. However, similar surveys of bacterial communities in the built environment have revealed high abundances of skin-associated bacteria (e.g., Propionibacterium acnes, Corynebacterium, and Streptococcus), particularly in buildings and on surfaces with high human occupancy and frequency of interactions [35]. Source-tracking efforts have also provided insight into the origin of the bacteria that reside on various indoor surfaces. For example, urine- and feces-associated bacteria have been shown to be more common on toilet seats and toilet handles than on other surfaces [53]; bacteria associated with fresh produce have been shown to be more common on kitchen countertops and inside refrigerators [54]; and bacteria associated with leaves and soil have been shown to be more common on the interior and exterior trim of doors that open to the outside than other (more interior) home surface locations [55]. Conversely, on surfaces that frequently have high moisture levels, such as those in bathrooms and kitchens (e.g., shower curtains, sinks, and countertops), rich microbial biofilms can form community assemblages that closely resemble those found in plumbing systems and water reservoirs [56,57,58]. Investigating differences both within and between homes, Lax et al. (2014) demonstrated that bacterial communities on different surfaces in an individual home showed strong similarities for some surfaces (e.g., kitchen floors were similar to bedroom floors and both were similar to human feet; and kitchen light switches were similar to the front doorknob, which were also similar to occupants’ hands) but not for others (e.g., kitchen countertops and human noses were distinct from doorknobs) [3••]. Moreover, when a family moved homes, the bacterial community composition on surfaces in the new home rapidly converged toward the composition of bacteria from surfaces in the previous home, suggesting that the new occupants quickly deposited their own unique signatures of human-associated bacteria to the new space.

While much has been revealed about bacterial and fungal communities in indoor environments in recent years, much less is known about viral communities and total viral abundance on surfaces in buildings [59]. However, much has been learned about the presence, abundance, and survival of specific viruses and other potential pathogens that cause concern for infectious disease transmission and other emerging microbial hazards.

Viral Pathogens on Fomite Surfaces

Presence and Abundance

The study of fomites has traditionally involved determining whether the presence of specific potentially pathogenic organisms—primarily those of viruses or bacteria—resided on environmental surfaces. For example, in an early influential survey, Boone and Gerba (1982) sampled over 300 fomites from daycare centers and homes to determine the presence of influenza A virus on each surface [60]. During flu seasons, approximately half of all common building surfaces from both types of indoor environments had measurable levels of influenza virus, suggesting that contaminated fomite surfaces could play a role in influenza transmission.

Since then, numerous similar studies targeting influenza and other viruses have also discovered that, for example:

Norovirus and influenza A virus were found on frequently used fomites (e.g., desktops, faucet handles, and paper towel dispensers) in elementary school classrooms [61].

Widespread norovirus contamination was found on fomite surfaces on houseboats on which an outbreak of norovirus gastroenteritis was suspected [62].

Picornavirus (including rhinovirus and/or enterovirus) was detected on approximately 20% of toys in pediatric office waiting rooms [63].

Human rhinovirus (hRV) was detected on 5% of clothing samples from teachers working in childcare centers [64].

Rotavirus was detected on about 20% of fomite samples in daycare centers, including on telephone receivers, drinking fountains, water-play tables, and toilet handles [65]; and on nearly half of surfaces sampled in a pediatric unit, with higher prevalence on surfaces that are commonly in direct contact with children (e.g., thermometers and play mats) than on other environmental surfaces (e.g., door handles and wash basins) [66].

Severe acute respiratory syndrome (SARS) coronavirus RNA was found on 30% of surface swab samples in hospitals, including in patient rooms, on computer mice at nurse stations, and on the handrail of a public elevator [67].

Human parainfluenza virus 1 (HPIV 1 ) was detected on 37% of a total of 328 fomites from 12 different office buildings, most frequently isolated on desktops [68].

HPIV 3 , HPIV 1 , and norovirus GII RNA were detected on 16 (12%), 7 (5%), and 4 (3%) of a total of 130 surfaces sampled in offices, with computer keyboards, computer mice, telephones, and desktops having significantly higher abundances than other fomite surfaces such as door handles, light switches, or ventilation ducts [5•].

Human adenoviruses (HAdV) were detected from 63 of 141 (45%) fomite samples in an adult intensive care unit (ICU) in a hospital in Rio de Janeiro, Brazil, with viral loads ranging from 2.48 × 10 1 to 2.1 × 10 3 genomic copies per milliliter [69].

Middle East respiratory syndrome coronavirus (MERS-CoV) was detected on 2 of 51 (4%) high-touch surfaces in patient rooms with laboratory-confirmed MERS-CoV patients [70].

These studies and many others confirm that viruses that are known to cause communicable diseases in humans are commonly found on surfaces, but it then must be determined whether they are viable and potentially infectious to humans.

Viability and Survival

Weber and Stilianakis (2008) reviewed numerous studies that investigated the environmental inactivation of influenza A viruses, finding that daily inactivation rate constants differ by several orders of magnitude depending on the nature of surface characteristics and that influenza virus can survive in aerosols for several hours, but only for a few minutes on human hands [71]. As an example from this body of literature, Bean et al. (1982) tracked the survival of laboratory-grown influenza A and B viruses on various surfaces, finding that both viruses survived up to 48 h on hard, non-porous surfaces, such as stainless steel and plastic and up to 12 h on porous surfaces, such as cloth, paper, and tissues [72]. Moreover, fomite transmission of influenza viruses was considered possible because influenza virus could be transferred from stainless steel surfaces to hands for up to 24 h after deposition (and from tissues to hands for up to 15 min after deposition). The viruses then subsequently survived on hands for an additional 5 min after transfer from the tested fomites.

More recently, Greatorex et al. (2011) combined the two main types of approaches commonly used in the literature to evaluate the survival of influenza A and pandemic H1N1 viruses inoculated onto a wide range of surfaces common to work and home environments [73]: (i) molecular (genomic) detection by reverse transcription polymerase chain reaction (RT-PCR), which provides a quantitative measure of presence/abundance of genetic material, and (ii) virus viability by plaque assay (for influenza A) or fluorescent focus assay (for H1N1), which provides a measure of virus survivability. The genome of both viruses was detected on most surfaces up to 24 h after inoculation with minimal decrease in gene copy number (except for unsealed wood surfaces), while virus viability decreased more rapidly to a level below detection on all surfaces at 24 h. However, viruses did survive up to 4 h on most surfaces and up to 9 h on non-porous surfaces. The authors concluded that influenza A transmission via fomites is possible, but it is unlikely if contact occurs after long periods following surface contamination, unless re-inoculation occurs during that time. Similarly, Mukherjee et al. (2012) investigated the viability of H1N1 virus on naturally contaminated hands and household surfaces of 20 individuals with laboratory-confirmed infection, finding that H1N1 has a short period of survival on naturally contaminated skin and fomites, and secretions deposited on hands by coughing or sneezing have a concentration of approximately 20–30 TCID 50 /mL [74].

Others have found that influenza virus can survive (i.e., remain viable and/or potentially infectious) much longer on fomite surfaces, using a variety of approaches. Thomas et al. (2008) tested the survival of influenza A viruses on banknotes after intentional contamination, finding viruses could survive up to 3 days after inoculation at high concentrations [75]. Additionally, when the virus was encapsulated in respiratory mucus (which may more realistically reflect human contributes to fomite surfaces), survival was as high as 17 days. And when nasopharyngeal secretions from naturally infected children were used to inoculate banknote surfaces, influenza virus survived at least 2 days in one-third of the test cases. Similarly, Oxford et al. (2014) found that influenza A H1N1sw virus particles survived and remained infectious for up to 48 h on a wooden surface, for 24 h on stainless steel and plastic surfaces, and for 8 h on a cloth surface [76]. Perry et al. (2016) found that two influenza A (H1N1) virus strains deposited on stainless steel surfaces remained infectious over a weeklong period, with a 2-log 10 loss (99%) in infectivity over 7 days [77]. Moreover, infectivity decreased more rapidly over time at higher absolute humidity, which is consistent with other similar studies [78, 79]. Thompson et al. (2017) tested the viability and RNA abundance (via qt-RT-PCR signal) of five influenza strains seeded on three surfaces (cotton, microfiber, and stainless steel) over time, finding that viable virus was detected for up to 2 weeks on stainless steel and up to 1 week on cotton and microfiber samples [6•]. Times to achieve 99% reductions in viability were ~ 18 h for cotton, ~ 34 h for microfiber, and ~ 175 h for stainless steel. Specific to materials used in personal protective equipment (PPE), Sakaguchi et al. (2010) found that the infectivity of influenza A virus was maintained for ~ 8 h on the surface of an N95 particulate respirator, a non-woven fabric surgical mask, a Tyvek gown, a coated wooden desk, and stainless steel, and for ~ 24 h on a rubber glove [80], suggesting that frequent replacement of PPE and clothing worn by healthcare professionals is warranted to minimize cross-infection. While there is high variability among these studies in influenza inactivation rates and survival on fomite surfaces over time (influenced by a combination of material type, environmental conditions, virus strain, inoculation methods, and viral presence/abundance/viability detection methods), there is general consistency in the literature that influenza viruses can survive for up to several days after being deposited on some surface types and in some conditions.

The survival of other viruses on fomites has also been investigated in recent years. For example, in the aforementioned study of HAdV in an ICU unit in Brazil, a subset of 10 samples that were positive for HAdV were selected for viability assessment, and exactly half of those samples were indeed still viable [69]. Boone and Gerba (2007) reviewed prior studies of the viability of numerous respiratory and enteric viruses on surfaces, reporting virus inactivation rates ranging from ~ 0.01–0.1 log 10 per hour for avian influenza and influenza A and B to ~ 0.2–0.6 log 10 per hour for rhinovirus 14, PIV 2 , and respiratory syncytial virus [81]. Inactivation rates for enteric viruses were lower, from ~ 0.002–0.003 log 10 per hour for astrovirus (serotype 4) and rotavirus p13 to ~ 0.01 log 10 per hour for adenovirus 40. van Doremalen et al. (2013) reported that MERS-CoV viability was more stable at low temperature and low humidity conditions and could still be recovered after 48 h, suggesting fomite transmission of MERS-CoV is possible [82].

Bacterial Hazards on Fomite Surfaces

In addition to viruses, bacterial hazards have also been found on fomite surfaces, including potentially pathogenic and antibiotic-resistant bacteria, which are often not mutually exclusive.

Potentially Pathogenic Bacteria

Marks et al. (2014) detected viable Streptococcus pyogenes and Streptococcus pneumoniae in samples from a daycare and then verified in laboratory tests that isolates of both organisms remained viable over extended periods of time and remained infectious in a mouse model when present as a biofilm (rather than as desiccated cells on surfaces) [83]. These findings suggest that fomite transmission in the environment could be an important pathway if fomites are contaminated with oropharyngeal secretions containing biofilm streptococci. Jones and Lutz (2014) measured the mean survival time of Pseudomonas aeruginosa on laminate, glass, and stainless steel surfaces to be 3.75, 5.75, and 6.75 h, respectively [84]. Malcolm et al. (2017) evaluated the growth and survival of the non-tuberculous mycobacterium (NTM) Mycobacterium abscessus in the presence of mineral particles, kaolin, halloysite, silicon dioxide, and house dust. Mycobacterium abscessus interacted with the particulates, with increased survival rates in the presence of house dust, surviving desiccation for as long as 2 weeks [7•]. These studies and others confirm that potentially pathogenic bacteria are present in the built environment and that they can survive on fomites for long periods of time.

Antibiotic-Resistant Bacteria

Antibiotic-resistant bacteria have been studied in even more detail than potentially pathogenic bacteria. In 2013, the US Centers for Disease Control and Prevention (CDC) published an analysis of the major antibiotic-resistant threats in the USA [85]. Davis et al. (2012) reviewed published works about the household transmission of Staphylococcus aureus and other staphylococci, and suggested that household microbial communities might have a role in the transfer of antimicrobial resistance genes and could be reservoirs for recolonization of humans [86]. Public transit environments can also play an important role, as handrails of public buses [87], as well as the hands of bus riders [88], in two cities in Portugal were tested positive for contamination by methicillin-resistant Staphylococcus aureus (MRSA).

Some of the greatest concerns for antibiotic-resistant bacteria transmission occur in healthcare environments where contamination and transmission are possible through numerous fomites, ranging from mobile phones [89] to medical devices [90] to surgical tape [91] to doctors’ handbags [92]. While it has been hypothesized that many of these fomites have been important sources, closer investigation often reveals a more nuanced understanding. For example, Julian et al. (2011) sampled the surfaces of cellular phones carried by personnel at a veterinary hospital for both MRSA and methicillin-resistant Staphylococcus pseudintermedius (MRSP). MRSP was isolated from only 2 of 123 phones, and MRSA was isolated from only 1 of 123 phones [93]. Similarly, Missri et al. (2018) assessed bacterial colonization on healthcare workers’ mobile phones in a hospital that were sampled immediately before and 5 min after sanitization with bactericidal wipes [8•]. All phones were colonized with bacteria, and healthcare workers had higher bacterial colonization than administrative staff. However, potential pathogens were detected on approximately one-third of phones (most commonly by Staphylococcus aureus), while only one phone was colonized with MRSA. No multi-drug resistant bacteria were detected. Smibert et al. (2018) swabbed medical staff personal mobile phones, departmental phones, and ICU keyboards and cultured for 94 multi-drug resistant organisms (MRDOs) that had been previously cultured from ICU patients, including 11 MRSA, 2 VRE, and 81 Gram-negative bacteria [9••]. MRSA was isolated from only two phones, and whole-genome sequencing of mobile phone isolates demonstrated the isolates on mobile phones had different single nucleotide polymorphism (SNPs) compared with the clinical isolates, which suggests that these fomites are unlikely to contribute to hospital-acquired MRDOs. Given the ubiquitous nature of bacteria in the built environment, studies that have characterized bacterial colonization alone tend to be less useful for yielding mechanistic or health-relevant insights than those that have targeted specific pathogens and other microbial hazards.

In addition to MRSA, other major microbial hazards in healthcare environments include Clostridioides difficile (C. diff), carbapenem-resistant Enterobacteriaceae, vancomycin-resistant Enterococcus (VRE), and a number of single- and multi-drug-resistant organisms [85]. Haun et al. (2016) reviewed 72 studies that assessed contamination of fomites in healthcare settings and found high variability in contamination rates by fomite type, by microbial agent (including MRSA, Gram-negative rods, enterococci, and C. diff), and by microbiological sampling and analysis technique [10•]. Grimmond et al. (2018) sampled for C. diff on 50 disposable and 50 reusable sharps containers in seven hospitals, finding that 8% and 16% of containers had detectable, albeit sub-infective, levels of C. diff, suggesting that sharps containers are not likely to pose a risk of C. diff transmission [94]. Jackson et al. (2019) sampled the bacterial burden on body sites of ICU patients who were colonized with vancomycin-resistant Enterococcus (VRE) and the healthcare workers (HCWs) who tended to those patients [11••]. HCW contamination on gloves and gowns (i.e., personal protective equipment or PPE) was associated with the VRE burden on body sites of patients with VRE, including perianal, stool, and skin swab samples, suggesting that ICU patients with a higher bacterial burden were more likely to transmit VREs to HCWs via their PPE.

A number of methods for controlling antibiotic-resistant bacteria and other microbial hazards on fomite surfaces have been investigated, including UV light, disinfectant cleaners, material coatings, and others. For example, Mitchell et al. (2019) quantified the doses of UV light that are required to inactivate MRSA, VRE, C. diff, and murine norovirus on stainless steel and Formica laminate fomite surfaces [95]. Reitzel et al. (2014) characterized the ability of a novel chlorhexidine and gentian violet antiseptic coating to kill bacterial and fungal pathogens on the surface of disposable medical gloves, finding that the coating eradicated MRSA, VRE, and multi-drug-resistant Pseudomonas aeruginosa, among others [96]. Despite the effectiveness of antimicrobial cleaners, other studies suggest that caution should be practiced in their use. For example, Hartmann et al. (2016) identified antibiotic resistance genes (ARGs) in settled dust from athletic and educational facilities, and found that ARG abundance was positively correlated with the concentration of antimicrobial chemicals found in the same dust samples [12••]. Similarly, Mahnert et al. (2019) compared the microbial communities and their resistomes (the total antibiotic resistance gene profile of a community) on surfaces of clinical settings using metagenomic genome and plasmid reconstruction, where they found that the microbiome of highly maintained built environments has a different resistome compared with other built environments, as well as a greater diversity of resistance genes [13••]. How these results are best applied is still an active area of research, as ARGs are also natural components of environments rich with bacteria (e.g., soils), and their role in shaping bacteria in indoor environments is not yet well understood.

One promising area of research that has emerged in recent years may offer an alternative to traditional cleaning methods. Unlike antimicrobials that kill microbes, probiotic cleaners that contain spores from Bacillus species (i.e., B. subtilis, B. pumilus, and B. megaterium) are thought to work primarily through biological competition to prevent the survival and proliferation of pathogenic bacteria [97, 98]. Probiotic cleaners have been found to be more effective than traditional cleaning methods, with several studies demonstrating that their use decreased pathogen load on surfaces by an average of 90% more than conventional chemical cleaners (ranging from 70 to 99%; [99, 100]). Furthermore, Caselli et al. (2019) showed that in hospitals where probiotic cleaners were used, the abundance of antibiotic resistance genes on treated surfaces was reduced by up to 99% [101]. Importantly, Caselli et al. (2016) confirmed their safety for use in healthcare facilities by measuring the infection rate from over 30,000 patients across seven facilities and found no evidence of infection by Bacillus spp., regardless of whether patients were at high risk for infection by opportunistic pathogens [102]. Safe sterilization or eradication of antibiotic-resistant bacteria on fomite surfaces remains an active area of study.

The aforementioned studies confirm that not only do pathogenic viruses, non-pathogenic viruses, and bacteria deposit and exist on fomites in the built environment they can also remain viable for hours, or even days, dependent upon the fomite material, microorganism type, and indoor environmental characteristics. From there, are they transmitted to humans and, if so, what are the implications of fomites for human health?