This article originally appeared in the December 2019 issue of Healthcare Hygiene magazine.
By Kelly M. Pyrek
The average adult has about 22 square feet of skin. As the human body’s largest organ, skin’s expansive real estate allows for numerous microorganisms to reside and multiply on the epidermis. Researchers have established that microorganisms can survive for a range of hours to months on surfaces without any kind of intervention, and the skin is no different. Studies indicate that microbes can flourish on hands for hours, and they can number as low as 2 million to as high as 10 million or more on fingertips, hands, forearms and elbows.
Specifically, total aerobic bacterial counts can range from more than 1 × 106 colony forming units (CFU)/cm2 on the scalp, 5 × 105 CFUs/cm2 in the axilla, and 4 × 104 CFU/cm2 on the abdomen to 1 × 104 CFU/cm2 on the forearm. Total bacterial counts on the hands of HCWs have ranged from 3.9 × 104 to 4.6 × 106 CFU/cm2. Fingertip contamination ranged from 0 to 300 CFU when sampled by agar contact methods. Investigators documented that although the count of transient and resident flora varies considerably among individuals, it is often relatively constant for any given individual.
Skin can be understood as its own “ecosystem” according to Fredricks (2001), who explains, “There are multiple niches within the ecosystem of the skin. The axilla may be as different from the trunk as a tropical rain forest is from a desert. The various regions of the skin are noted to have different populations of microbial inhabitants, reflecting their different niches. Colony counts of aerobic bacteria from moist areas such as the axilla or toe web spaces can reach 107 bacteria per cm2, whereas dry areas such as the forearm or trunk may harbor 102 or fewer bacteria per cm2. Anaerobic bacteria are also present on human skin, with colony counts up to 106 bacteria per cm2. In addition, skin structures within a specific skin zone may harbor unique microbes. The stratum corneum, cellular layer, hair shaft and follicle, eccrine, apocrine, and sebaceous glands may each have associated microflora.”
The hands carry a mix of good bacteria along with potentially pathogenic microorganisms, so the importance of washing one’s hands in the clinical setting cannot be overstated, but let’s examine the issue from a microbiological perspective, to gain a better understanding of exactly what is on our hands in the first place.
The Hand Microbiome
Through the wonders of microbial sequencing and typing, there may come a time when it will be possible to tell from the bacteria on an object which individuals have touched it. For example, Seong, et al. 2017 emphasized the significance of bacterial flora found on the surface of the skin and its application in personal identification. In particular, hand surface can be an environment of primary interest, as it harbors higher level of microbial diversity than other parts of the skin. In this study, diversity of microbial communities inhabiting the palms of different individuals was explored using culture-based methods A total of 686 bacterial strains were obtained and identified based on 16S rRNA gene sequence analysis. Among the isolates, the genera Staphylococcus, Micrococcus and Enhydrobacter were recovered as major taxa. Twenty strains could be recognized as candidates for novel species, as the 16S rRNA gene sequence similarities with known species were around 97 percent. Variations in the bacterial composition among individuals could be observed, the researchers found, and say their data confirmed a high potential of palm microbial flora in the forensic application for personal identification.
Before the microbiome became the center of the health data universe, Fierer, et al. (2008) studied the influence of sex, handedness, and washing on the diversity of hand-surface bacteria. The researchers examined the palm surfaces of the dominant and nondominant hands of 51 healthy young-adult volunteers to characterize bacterial diversity on hands and to assess its variability within and between individuals.
By using a novel pyrosequencing-based method, they found that the diversity of skin-associated bacterial communities was surprisingly high; a typical hand surface harbored more than 150 unique species-level bacterial phylotypes, and the researchers identified a 4,742 unique phylotypes across all of the hands examined” “Although there was a core set of bacterial taxa commonly found on the palm surface, we observed pronounced intra- and interpersonal variation in bacterial community composition; hands from the same individual shared only 17 percent of their phylotypes, with different individuals sharing only 13 percent. Women had significantly higher diversity than men, and community composition was significantly affected by handedness, time since last handwashing, and an individual's sex. The variation within and between individuals in microbial ecology illustrated by this study emphasizes the challenges inherent in defining what constitutes a ‘healthy’ bacterial community.”
Fierer, et al. (2008) explain that the skin is “a body habitat with complex regional variations in cellular architecture and environmental exposures, where bacterial density may be as high as 107 cells per square centimeter. Many of these bacteria are not simply passive or transient colonizers of the skin surface, but rather appear to be adapted to the specific rigors associated with living in different regions of the skin including frequent skin shedding, antimicrobial host defenses, exposure to soaps and detergents during washing, exposure to UV radiation, and low moisture availability.”
Researchers have found, through culture-based and molecular approaches, that there may be a core set of bacterial taxa commonly found on skin surfaces, but there is a significant amount of variability in the composition of skin-associated bacterial communities that are not well understood.
Fierer, et al. (2008) selected to study the palms because they characterized them as “likely one of the more dynamic skin microbial habitats, given the nearly constant and varied exposure to environmental surfaces and the frequency of perturbations caused by handwashing. In addition, pathogens may inhabit the palmar surface, and efforts to reduce disease transmission by handwashing are a key public health concern.”
The researchers note, “The average palm surface harbors >150 distinct species-level bacterial phylotypes [a species is defined here as organisms sharing 97 percent identity in their 16S rRNA gene sequences. Not surprisingly, this number of unique phylotypes exceeds the number of bacterial types typically cultivated from the skin surface by at least an order of magnitude 8, confirming that culture-based surveys of the skin surface, like surveys conducted in many other microbial habitats, dramatically underestimate the full extent of bacterial diversity. The average phylotype richness observed on a single palm surface was also more than three times higher than the richness observed in a molecular survey of forearm skin and elbow skin. Although we would expect the hand surface to have higher levels of diversity than other skin surfaces because of the more frequent contact with potential inocula from the environment, this discrepancy in observed bacterial diversity is more likely a result of the depth of our sampling, which allowed us to survey even those rare bacterial taxa present on the skin surface.”
The researchers add that the total diversity of bacteria on the hand surface appears to meet or exceed the levels of bacterial diversity found in other human-associated microbial habitats, including the mouth and at specific sites within the lower intestine.
Three phyla (Actinobacteria, Firmicutes, and Proteobacteria) accounted for 94 percent of the sequences, report Fierer, et al. (2008). The most abundant genera (Proprionibacterium, 31.6 percent of all sequences; Streptococcus, 17.2 percent; Staphylococcus, 8.3 percent; Corynebacterium, 4.3 percent; and Lactobacillus, 3.1 percent) were found on nearly all palm surfaces sampled. According to the researchers, these genera have previously been found to be abundant in other molecular surveys of skin bacteria and are considered to be common skin residents, yet they still represented less than 65 percent of all of the identified sequences. They observe that the average palm surface has a large number of rare taxa that may be either transient, short-term colonizers of skin or more persistent, longer-term residents of the skin surface that are simply present at relatively low abundances or whose abundance is determined by specific characteristics of individual hand surfaces.
The researchers report that qualitatively, the bacterial communities found on the hand surfaces appear to be more similar to the communities found on forearm skin than to the communities found on the forehead or inner elbow, suggesting that skin bacterial communities are not uniform across the body and that skin surfaces closer in proximity may harbor more similar bacterial communities.
What’s fascinating is that Fierer, et al. (2008) found that handedness significantly influenced bacterial communities, in that dominant hands have similar overall levels of diversity as nondominant hands, but the composition of the bacterial communities on the dominant and nondominant hands from the same individual was significantly different. Taxa with relative abundances more than 50 percent greater on the dominant hand than the nondominant hand included members of the Enterobacteriales, Lactobacillaceae, Peptostreptococcaceae, and Xanthomonadales groups. T
“The influence of handedness on palm bacterial communities is likely due either to differences in skin environmental conditions (e.g., sebum production, salinity, hydration) or to the dominant hand coming into contact with different types of environmental surfaces than the nondominant hand,” say Fierer, et al. (2008). “Although dominant and nondominant hands harbor distinct bacterial communities, the communities on left and right hands from the same individual were more similar than we would expect by chance. However, these communities still shared only 17 percent of their phylotypes on average, indicating that there is an enormous amount of heterogeneity in skin bacterial communities within an individual.”
Equally interesting is that men and women harbor significantly different bacterial communities on their hand surfaces, the researchers say. Taxa that were shared by both men and women but were more abundant on the skin of 1 sex included members of the following groups: Proprionibacterium (37 percent more abundant on men), Corynebacterium (80 percent more abundant on men), Enterobacteriales (400 percent more abundant on women), Moraxellaceae (180 percent more abundant on women), Lactobacillaceae (340 percent more abundant on women), and the Pseudomonadaceae (180 percent more abundant on women).
The palms of women were also found to harbor significantly greater bacterial diversity than those of men, whether diversity was assessed by examining the overall phylogenetic structure on each hand or the average number of phylotypes per hand. The researchers observe, “We do not know what drives these differences in overall diversity, but differences in skin pH may be influential. Men generally have more acidic skin than women, and work from other microbial habitats has shown that microbial diversity is often lower in more acidic environments. Other explanations for why men and women appear to harbor distinct hand bacterial communities may include differences in sweat or sebum production, frequency of moisturizer or cosmetics application, skin thickness, or hormone production.”
Clinicians take note – the time since the last handwashing also had a significant effect on skin community composition, Fierer, et al. (2008) emphasize: “Most notably, bacteria belonging to the Proprionibacteria, Neisseriales, Burkholderiales, and Pasteurellaceae taxa were relatively more abundant with time since last handwashing, whereas other bacteria in the Staphylococcaceae, Streptococcaceae, and Lactobacillaceae groups showed the opposite pattern and were relatively more abundant on hands that had been recently washed. Although handwashing altered community composition, overall levels of bacterial diversity were unrelated to time since last handwashing. Either the bacterial communities rapidly reestablish after handwashing, or washing (as practiced by the students included in this study) does not remove the majority of the bacterial taxa found on the skin surface.”
Eight years after Fierer, et al. (2008) published their research, Kumar, et al. (2019) assessed the ability of skin microbes to physically interact (co-aggregate) intergenically. The bacterial flora from the hands (palm area) of similar age group students was isolated. The predominant isolates were selected and identified using 16s rRNA gene sequencing. A total of 27 bacteria were isolated from the skin (palm area-fingers) of 10 individuals. The researchers report these isolates belong to seven bacterial genera and 10 different species; among 27 isolates, Staphylococcus haemolyticus had highest co-aggregation partners of 17 followed by Acinetobacter spp. and Pseudomonas spp. with 15 partners each. The study indicates that few microbes have high potential to influence coaggregation among distinct genera isolated from the skin; however, the researchers say further studies are needed to understand the ability of these bacteria to co-aggregate, their influence in interpersonal transmission and shaping of microbial ecology of the host skin.
Why does this matter? Kumar, et al. (2019) explain that the presence of more number of co-aggregating bacteria in individuals may facilitate the inter-personal transfer among individuals who are having hand contacts very often: “These bacteria are recently known to acquire multidrug resistance and can be transferred rapidly, surviving desiccation and persisting in the environment for a long time. Thus, these bacteria could pose significant concern among the interacting population, especially the vulnerable human population. Co-aggregation is common among Pseudomonas species; Doring, et al. demonstrated the transfer of P. aeruginosa and Burkholderia cepacia by handshaking of individuals, where these bacteria were detected up to 30 minutes to 180 minutes. Numerous studies have documented that the subungual area of the hand harbor high concentration of bacteria, most frequently coagulase-negative Staphylococci, Pseudomonas spp., Corynebacteria, and yeasts.”
Edmonds-Wilson, et al. (2015) connects the dots for us in their review of human hand microbiome research when they observe, “Human hands are a conduit for exchanging microorganisms between the environment and the body. Hands can harbor pathogenic species, including methicillin-resistant Staphylococcus aureus or Escherichia coli; particularly within high risk environments, such as healthcare and food-handling settings. Product use can impact the hand microbiome, with greater pathogen hand carriage on people using a high level of hand hygiene products, while other studies have demonstrated reduced pathogen carriage and/or infections with use of these products. Frequently washed hands of healthcare workers are colonized with more pathogenic bacteria than those who wash less frequently. … Many studies have demonstrated the beneficial impact of handwashing and/or use of alcohol-based hand rubs for reducing pathogenic bacteria on hands and/or reducing infection rates in various institutional settings. The occurrence of pathogens on hands is well-studied; in contrast, hands are rarely considered a source of beneficial bacteria contributing to our healthy microbiome.”
In their review, Edmonds-Wilson, et al. (2015) found that overall, the data on hands is limited compared to other body sites, and most studies were conducted on young adults, often students or professionals, in the United States. Most studies contained a small sample size (≤10) and/or assessed microbial composition at a single time-point. Most studies reported between eight and 24 families of bacteria on hands. Bacteria were found from four phyla across all studies (most to least relative abundance): Firmicutes, Actinobacteria, Proteobacteria, and Bacteroidetes. There were considerable differences in the types of bacteria found among the studies, with Staphylococcaceae, Corynebacteriaceae, Propionibacteriaceae and Streptococcaceae being found in most of the studies. Interestingly, Propionibacteriaceae, when detected, was often quite high in relative abundance.
One study found that bacteria were the most prevalent microorganism (>80 percent relative abundance), then viruses, and fungi being least prevalent (<5% relative abundance) on hands. However, as Edmonds-Wilson, et al. (2015) caution, this finding “may be somewhat biased for greater proportion of bacteria, since the relative size of viral genomes is small, and would therefore be expected to represent proportionally less of the sequence data, even if bacteria and viruses were equally abundant.”
The researchers also note that skin biogeography significantly impacts the composition of the microbiome: “Hands have greater bacterial diversity; and the hand microbiome is more dynamic over time than other skin sites. Palm skin typically harbors more than three times more bacterial phylotypes per individual compared to forearm or elbow skin. Fungal species diversity was intermediate on hands, with feet having greater diversity and core body skin sites having the least diversity. Microbial communities on hands were generally enriched with different bacterial taxa compared with other body sites and acquired a larger pool of total bacterial species through time. The interpersonal variation of the hand microbiome was less than the variation between different body sites on the same individual. Temporal stability of the microbiome is dependent on physiological conditions of the skin; with moist, warm, and nutritionally rich skin sites harboring a more stable microbiome than hands which are dry and continually exposed to varying environments. Additionally, individuals with more variable hand bacterial communities have greater variability at other skin sites, indicating microorganisms may be transferring between skin sites.”
Of note for patient hand hygiene, Edmonds-Wilson, et al. (2015) found that immune function and other health factors likely impact the bacterial composition of hand skin: “A study found different bacterial composition on the hands of healthy controls compared with those of immune-compromised individuals; with healthy populations having greater proportions of Staphylococcus spp., Fusobacterium spp. and Prevotella spp., and the immune-compromised having a greater proportion of Acinetobacter spp.”
Extrinsic factors impacting hand microbiome composition was challenging to discern, as no studies in this review by Edmonds-Wilson, et al. (2015) directly evaluated the impact of hand hygiene or other product use on the hand microbiome. However via self-reported survey data, the researchers attempted to correlate hand hygiene practices, including the type of products used and the frequency of use, to changes in the hand microbiome. They observe, “Healthcare workers likely have greater exposure to hand hygiene products than the rest of the population; however the overall microbial diversity on hands was unchanged with alcohol-based handrub use or handwashing, with the exception that overall diversity was lower in those that reported more than 40 handwashing with soap and water events per shift. The length of time since the last handwashing event impacted bacterial composition, with Propionibacteria, Neisseriales, Burkholderiales and Pasteurellaceae more abundant with time since handwashing, and Staphylococcaceae, Streptococcaceae, and Lactobacillaceae more abundant on recently (more than two hours) washed hands. While there were changes in bacterial composition with time since last handwashing, there was no impact on the overall level of diversity on the hands. Another study found no impact on hand microbiome composition when handwashing occurred within one hour of sampling. Frequency of handwashing on the day prior to sampling did not correlate with changes in bacterial composition. Use of other topical products was not studied on hands but use of oral antibiotics had a significant impact on the hand microbiome, with the largest shift observable around the time of use.”
Now that we have seen what is living on the human hands, it is imperative to understand that bacteria recovered from the hands can be divided into two categories – resident of transient, emphasizes the World Health Organization (WHO) Guidelines on Hand Hygiene in Health Care (2009), citing Price (1938).
Resident flora (resident microbiota) consists of microorganisms residing under the superficial cells of the stratum corneum and can also be found on the surface of the skin. Staphylococcus epidermidis is the dominant species, and oxacillin resistance is extraordinarily high, particularly among healthcare workers, states the WHO guideline (2009). Resident flora has two main protective functions: microbial antagonism and the competition for nutrients in the ecosystem. In general, resident flora is less likely to be associated with infections, but may cause infections in sterile body cavities, the eyes, or on non-intact skin.
Transient flora (transient microbiota), which colonizes the superficial layers of the skin, is more amenable to removal by routine hand hygiene, says the WHO guideline (2009). Transient microorganisms do not usually multiply on the skin, but they survive and sporadically multiply on skin surface. They are often acquired by healthcare workers during direct contact with patients or contaminated environmental surfaces adjacent to the patient and are the organisms most frequently associated with HAIs. The transmissibility of transient flora depends on the species present, the number of microorganisms on the surface, and the skin moisture.
Regardless of the kind of flora, we know that hands get contaminated in the healthcare environment and serve as a significant vector for disease if the conditions are right. But in the zest for cleanliness, is something lost in translation? Larson (2001) had once posed the question, “when is clean too clean?” in the era when the Hygiene Hypothesis – the idea that exposure to microbes helped enhance the immune system, especially in the formative years of children’s development – was still a prominent concept in public health.
As Larson (2001) explained, “For over a century, skin hygiene, particularly of the hands, has been accepted as a primary mechanism to control the spread of infectious agents. Although the causal link between contaminated hands and infectious disease transmission is one of the best-documented phenomena in clinical science, several factors have recently prompted a reassessment of skin hygiene and its effective practice. In industrialized countries, exposure to potential infectious risks has increased because of changing sociologic patterns. Environmental sanitation and public health services, despite room for improvement, are generally good. In addition, choices of hygienic skin care products have never been more numerous, and the public has increasing access to health- and product-related information.
In the early 2000s, the relationship between skin hygiene and infection, as well as the effects of washing on skin integrity, were just beginning to be fully investigated, if not completely understood. Larson, writing within the context of the times, had raised the issue of skin barrier properties and the effects of hand hygiene practices on healthcare workers’ much-washed skin, specifically irritant contact dermatitis. She wrote that, “Damaged skin more often harbors increased numbers of pathogens. Moreover, washing damaged skin is less effective at reducing numbers of bacteria than washing normal skin, and numbers of organisms shed from damaged skin are often higher than from healthy skin.”
Again, in the context of the times, Larson (2001) noted, “Even with use of antiseptic preparations, which substantially reduce counts of hand flora, no reductions beyond an equilibrium level are attained. The numbers of organisms spread from the hands of nurses who washed frequently with an antimicrobial soap actually increased after a period of time; this increase is associated with declining skin health. In a recent survey, nurses with damaged hands were twice as likely to be colonized with S. hominis, S. aureus, Gram-negative bacteria, enterococci, and Candida spp. and had a greater number of species colonizing the hands. The trend in both the general public and among health-care professionals toward more frequent washing with detergents, soaps, and antimicrobial ingredients needs careful reassessment in light of damage done to skin and resultant increased risk for harboring and transmitting infectious agents. More washing and scrubbing are unlikely to be better and may, in fact, be worse. The goal should be to identify skin hygiene practices that provide adequate protection from transmission of infecting agents while minimizing the risk for changing the ecology and health of the skin and increasing resistance in the skin flora.”
Larson (2001) concluded that, “From the public health perspective, more frequent use of current hygiene practices may not necessarily be better (i.e., perhaps sometimes clean is ‘too clean’), and the same recommendations cannot be applied to all users or situations. Future investigation is likely to improve understanding of the interaction between skin physiology, microbiology and ecology and the role of the skin in the transmission of infectious diseases.”
Studies since then have shown that after handwashing, as many as 80 percent of individuals retain some pathogenic bacteria on their hands, and that handwashing removes body's own fatty acids from the skin, which may result in cracked skin that provides an entry portal for pathogens. As Jain, et al. (2016) note, “To overcome the limitations of plain handwashing, hand sanitizers were introduced claiming to be effective against those pathogenic micro-organisms as well as to improve skin condition due to the addition of emollients in it.”
Ellingson, et al. (2014) confirm that irritant contact dermatitis (ICD) is the most frequently occurring adverse reaction to hand hygiene products and impacts a large proportion of the nursing workforce at some point in their careers. Strategies to prevent and manage ICD include: Have a process to manage HCP with ICD; involve staff members in hand hygiene product selection; educate HCP about the relative impact of ABHR versus handwashing in terms of skin damage; promote use of ABHR for routine hand hygiene; wash hands with warm or cold water; provide lotion for use in the workplace and encourage use; promote use of gloves for wet work, which includes extensive patient care.
As we have seen, hand-hygiene products have improved over the decades to recognize and address the problem of skin that has been scrubbed and rubbed in the quest for clean in the healthcare environment. Which begs the question, can hands ever be too clean? Focus has been placed on the historically low rates of hand hygiene in many institutions, but few investigators have ever attempted to define what is optimal and what is excessive cleanliness, knowing that microbes can quickly re-populate hands, notwithstanding the residual antimicrobial effects of some hand-hygiene products.
The mechanism of handwashing and handrubbing influences the cleanliness of the hands – or does it? There seems to be some disagreement as to how effective technique can be, and unlike the levels of cleanliness for medical devices that can be established through sterility parameters, we are at a disadvantage when it comes to microorganisms on skin and ascertaining exactly how "clean" hands are after they have been washed in the real-world setting.
“This is what the guidelines and recommendations are for, so there is no reason to invent another definition of what “clean” is,” says Didier Pittet, MD, MS, CBE, professor of medicine, hospital epidemiologist, and director of the infection control program at the University of Geneva Hospitals. “There is are standard that qualifies the log reduction in bacteria needed to prevent cross transmission In the U.S. it’s ASTM standards, in Europe it’s the EN ones. We do not need hands to be sterile (have zero bacteria on them) in order to prevent cross transmission.”
“I am not aware of fast, reliable, easy-to-use point-of-care technology to answer the fundamental question we have for healthcare workers before and after each patient encounter: Did you wash your hands, and did you do it properly?” says Paul Pottinger, MD, FACP, FIDSA, professor of medicine in the Division of Allergy & Infectious Diseases at the University of Washington Medical Center in Seattle. “The best answer seems to be training our clinicians in proper technique, right from the start, how (including how long) to wash their hands,” adds Pottinger, who is also director of the Infectious Diseases Training Program, and co-director, of the UWMC Antimicrobial Stewardship Program.
“Part of that training can include application of a fluorescent hand-rub product that will reveal under special light just how well someone has done,” he continues. “This can have a real impact on getting everyone's technique up to snuff before they hit the wards. As for whether they sustain this best practice... well, that's another matter. For us, success depends on a supportive healthcare environment, where team members are encouraged, empowered, and expected to call each other out if they forget to perform diligent, effective hand hygiene.”
“In the real world, there are products like GloGerm to aid the visualization of washing technique, but is this enough?,” asks Pittet. “Such products can help, but behavior change is a complex field. So as long as hand hygiene compliance remains suboptimal, I think the answer to everything will be ‘no, it’s not enough.’ But such innovations can be useful tools in the WHO multimodal strategy (https://www.who.int/gpsc/news/simple_guideline/en/).”
Pittet adds, “Hand hygiene, when performed correctly, results in hands that are more than clean enough to prevent cross-transmission from the hands of that person. The issue is not making hand hygiene more effective microbiologically -- that part is okay. What is difficult is making sure people perform hand hygiene well, and at all of the moments where there is a risk of infecting the patient with contaminated hands. That is why we developed the 5 moments for hand hygiene for the World Health Organization (https://www.who.int/gpsc/5may/background/5moments/en/).”
Pittet continues, “If we are talking about is it enough for healthcare workers to ‘wash in’ and ‘wash out’ when they go into and leave a patient room, the answer is absolutely not. If we are talking about the WHO 5 Moments for Hand Hygiene, they are enough if it is followed well (we aim for 80 percent compliance but even improvements resulting in far lower levels of compliance have caused large reductions in healthcare-associated infections).”
Pottinger emphasizes, “Current handwashing protocols from CDC and APIC are excellent. They do not include microbiological testing of hands to see just how clean they are, probably because such testing is not practical and not necessary, so long as hands are washed in the correct way and at the correct opportunities. Specifically, hands should be clean during patient encounters. Using an alcohol-based hand rub is appropriate if hands are visibly clean before the product is applied, but nothing replaces good old soap and water when they are visibly soiled. Nothing too fancy is required to do a great job: get hands wet, rub them together with plenty of soap, make sure the entire hand is soaped up (including the backs, between fingers... everywhere), and keep on scrubbing. After 15-20 seconds, the bioburden should be so low that risk of carrying or transmitting germs by hand is exponentially reduced. If that protocol is followed, it is plenty robust.”
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