Cleanliness in context: reconciling hygiene with a modern microbial perspective

Abstract

The concept of hygiene is rooted in the relationship between cleanliness and the maintenance of good health. Since the widespread acceptance of the germ theory of disease, hygiene has become increasingly conflated with sterilization. In reviewing studies across the hygiene literature (most often hand hygiene), we found that nearly all studies of hand hygiene utilize bulk reduction in bacterial load as a proxy for reduced transmission of pathogenic organisms. This treatment of hygiene may be insufficient in light of recent microbial ecology research, which has demonstrated that humans have intimate and evolutionarily significant relationships with a diverse assemblage of microorganisms (our microbiota). The human skin is home to a diverse and specific community of microorganisms, which include members that exist across the ecological spectrum from pathogen through commensal to mutualist. Most evidence suggests that the skin microbiota is likely of direct benefit to the host and only rarely exhibits pathogenicity. This complex ecological context suggests that the conception of hygiene as a unilateral reduction or removal of microbes has outlived its usefulness. As such, we suggest the explicit definition of hygiene as "those actions and practices that reduce the spread or transmission of pathogenic microorganisms, and thus reduce the incidence of disease."

Keywords: Hand hygiene; Hygiene; Microbial ecology; Microbiome; Microbiota; Skin.

Fig. 1

a Diversity of the hand microbiome is variable, with different studies finding different dominant groups (though Proteobacteria and Actinobacteria are common members of the hand microbiome across studies): data presented from [52, 54, 57]. Interactions between taxa may modulate their ecological roles, and community variation across a range of ecological traits may be altered by changes in community membership or structure [124]. b Pre-hand hygiene intervention. Both resident and transient microbes are abundant on the hands (in this conceptualization, colored dots represent individual microbes: many colors are used to show the diversity of microbes present on the hands). c Hand hygiene intervention, such as washing with soap and water, reduces the total number of microbes (microbial load) present on the hands. d Cultivation-dependent detection (CDD) is commonly used to study aspects of hand hygiene; cultivation yields data showing changes in the numbers of colony-forming units (counts), though many microbes are not detectable using this methodology (represented as non-colored, open circles). Some studies identify colonies using morphological or molecular methods, yielding limited taxonomic information. e Cultivation-independent detection, including high-throughput DNA sequencing, is commonly used to study the microbial ecology of the skin. Using these methods, it is possible to quantify alterations in relative abundance of bacterial populations with treatment (such as handwashing), to obtain deep, comprehensive taxonomic diversity estimates. Depending on technique, it may also be possible to also obtain information on functional metabolic pathways (using metagenomics and metatranscriptomics)

Fig. 2

Conceptual illustration of important ecological factors impacted by hygienic practice. a Dispersal is the movement of organisms across space; a patch of habitat is continuously sampling the pool of available colonists, which vary across a variety of traits (dispersal efficiency, rate of establishment, ex host survivability, etc.) [125]. b Environmental filtering works on the traits of dispersed colonists—microbes that can survive in a given set of environmental conditions are filtered from the pool of potential colonists [125]: the resources and conditions found there permit the survival/growth of some organisms but not others. c Protective mutualisms function through the occupation of niche space; harmful microorganisms are excluded from colonization via saturation of available habitat by benign, non-harmful microbes [126]. d Host/microbe feedbacks occur via the microbiota’s ability to activate host immune response and the host immune system’s ability to modulate the skin microbiota [106, 127, 128]. Such feedbacks between host immune response and the skin microbiota are thought to be important to the maintenance of a healthy microbiota and the exclusion of invasive pathogenic microbes [87]. All of these ecological factors are affected by features of the e skin habitat, which includes appendages such as hair follicles, sebaceous glands, and sweat glands; microbes (bacteria, fungi, virus particles, and skin mites) reside not only on the surface but deeply within glands and the roots of hairs, as well as within the squamae of the epidermis (illustration redrawn from [53])