A review of clothing microbiology: the history of clothing and the role of microbes in textiles

Abstract

Humans have worn clothing for thousands of years, and since its invention, clothing has evolved from its simple utilitarian function for survival to become an integral part of society. While much consideration has been given to the broad environmental impacts of the textile and laundering industries, little is known about the impact wearing clothing has had on the human microbiome, particularly that of the skin, despite our long history with clothing. This review discusses the history of clothing and the evolution of textiles, what is and is not known about microbial persistence on and degradation of various fibres, and what opportunities for the industrial and environmental application of clothing microbiology exist for the future.

1. Introduction

In the context of the spread of the virus that causes COVID-19, the global public has become hyper-aware of one instance in which clothing and microbes are related, the use of masks to prevent pathogens (in the case of COVID-19, viruses) from travelling from one person to another. Laundering, along with the rising interest in maintaining the efficacy of laundering for the removal of soils and microorganisms, while minimizing its environmental impacts by means such as reducing water temperatures, is another instance in which people have become acquainted with the notion of microbes in textiles. However, the relationship between clothing and microbes is far broader. Each garment worn by a person since the very first garment is likely to have hosted some microbes, served as a mechanism for the transfer of others and, simultaneously, created conditions on the body that have favoured still other microbes. The relationship between microbes and clothing is of great significance to palaeo-history, history, fashion, medicine and public health. Its consequences ramify. But perhaps because of this ramification, it is a topic that has never been reviewed. Here, we examine what is and is not known about the microbiology of clothing. We do so with an eye to the possibility of future studies, but also with regard to the applications of clothing microbiology to archaeology, medicine and modern textiles.

2. Origin of clothing

For the purposes of this review, clothing is defined as items worn to enclose or cover the body and does not include body modifications [1]. Clothing provides a barrier between the skin and the external environment and serves a variety of functions, which include protection from harmful UV rays, social and cultural purposes, and thermoregulation. The oldest well-documented clothing is surprisingly recent and comes in the form of clothing carved onto Palaeolithic figures [2,3], and remnants of clothing found at archaeological sites [4]. These bits of clothing are associated with early modern humans in Europe. However, because the clothing materials were invariably subject to deterioration, it is likely that the first clothing considerably pre-dates these pieces of evidence. Recent scholarship suggests that Neanderthals (Homo neanderthalensis) likely began to use clothing when they spread into cold habitats in Europe several hundred thousand years ago [5,6]. In the most often cited scenario, Neanderthals used skins of animals, with the fur still attached, as loose-fitting cloak-like clothing [6]. Multi-layered clothing is then hypothesized to have been invented by early modern humans (Homo sapiens) with their own migration into cold realms [7]. However, it is also possible that clothing use is much older and began not in cold realms but instead with simple coverings in warm habitats that are sometimes cool. Cross-culturally, the use of clothing, even if piecemeal, is widespread not only in cold regions but also in most warm regions. Regardless, it is clear that the relationship between clothing and microbes is at least a hundred thousand years old and potentially much more ancient.

3. Evolution of textiles

Animal hides were undoubtedly one of the first articles of clothing worn by humans. Those who argue that Neanderthals wore clothes tend to suggest that they relied on animal hides [5–7]. However, it is of note that woven plant material has recently been discovered at a Neanderthal site and may have been used in clothing production as well as for other applications [8]. Early modern humans developed more specialized cold-weather clothing, typically involving layers that provided much better insulation as they moved into glacial Europe. Early humans also made clothing from plant fibres, especially those of flax and cotton. Flax, Linum angustifolium and Linum usitatissimum, was one of several crops in the ‘Neolithic package’ that were domesticated approximately 10 000 years ago [9] and may be the first plant used for fibre by Homo sapiens. The oldest textile fibre found to date is a flax fibre estimated to be 34 000 years old [4,10]. For the purposes of this review, fibre is defined as a filament that, whether natural or anthropogenic, forms the basic element of fabrics or other textiles [11]. ‘Cotton’ refers to any one of four main species in the genus Gossypium (G. arboretum, G. barbadense, G. herbaceum and G. hirsutum). Cotton was first cultivated as early as 3500 BC in the Indus River Valley of what is now Pakistan [12–14].

A major transition occurred in clothing with the invention of woven fabric. Fabric is defined as a two-dimensional plane-like structure made of textile materials created through knitting, weaving or bonding [15]. Archaeological evidence suggests that humans were weaving plants together into baskets and garments at least 23 000 years ago [2,3]. Since then, the technology associated with fabric production has rapidly diversified and advanced. A brief summary of the evolution of textile use throughout human history is displayed in figure 1. Weaving became mechanized during the Industrial Revolution, which allowed the quick production of inexpensive cloth [16]. Artificial fibres would not make their way onto the scene until the nineteenth century, with the first semisynthetic fibre being artificial silk, or ‘rayon’, which was invented in the 1800s [17]. Since their inception, synthetic fibres have revolutionized the textile industry. In 2018, there was a global production volume of 66.6 million metric tonnes (Mt) of synthetic fibre, accounting for about 62% of global fibre production [18]. Polyester alone accounted for 55.1 million Mt, 51.5%, of global fibre production [18]. By contrast, cotton and wool only had global production volumes of about 26.05 and 1 million Mt, respectively, in 2018 [18].

Figure 1.

A brief timeline of the evolution of textiles throughout human history. (Online version in colour.)

4. Impact of textiles on skin

It would be impossible to discuss the impact of textiles on the human microbiome without discussing skin. Skin is the largest organ on the human body; it is also a habitat. The stratum corneum is the horny outer layer of skin and constitutes the essential structure of the skin barrier, as it interacts the most with the environment. The acidity of its surface pH of 4.5–5 [19] helps create unfavourable growth conditions for many pathogenic microorganisms [20] while simultaneously favouring the growth of commensal bacteria such as Staphylococcus spp. and Corynebacterium spp., which themselves may aid in preventing the growth of pathogenic microorganisms [21,22]. Commensal skin microbes tend to be species from a subset of taxa that are tolerant of acidity and have mechanisms that allow them to subsist on the nutrient-deficient resources available in sweat, sebum and the stratum corneum [23].

The primary interaction between clothing and skin is mechanical. Two of the main forces at play are friction and pressure. Skin friction of textiles largely depends on factors such as fibre and fabric structure, material, and textile quality [24,25]. Friction has been implicated in skin ailments such as keratosis follicularis and can exacerbate conditions such as atopic dermatitis [25], while prolonged pressure on various body parts can cause superficial abrasions and tissue deformation [24]. These conditions may potentially favour some bacteria species over others. Additionally, fibre dyeing and finishing can cause skin irritation [26–28], which may lead to allergic contact dermatitis and might also affect skin microbial composition. Moisture management, air permeability and heat transfer regulation of particular fabrics are strongly affected by fibre type and might impact the skin microclimate [29,30], which could alter microbial community structure. Finally, skin occlusion by clothing may elevate the skin pH, compromising skin barrier function, which could favour the growth of pathogenic bacteria such as Staphylococcus aureus and Streptococcus pyogenes [31,32].

Studies of skin microbes often find that only a small proportion of differences in microbial composition from one person to the next can typically be explained by age, diet, genetic background and other factors [33–35]; we suspect that some of the unexplained variation is due to differences in clothing type, clothing use and clothing effects. Clothing may favour microclimates and species that were uncommon prior to its invention and use. It seems likely that microbes associated with humans wearing clothes are very different from those of humans that do not regularly wear clothes. Here, the study of the microbiomes of modern nudists would be revealing.

5. Microbial adhesion to clothing

Clothing can alter skin and its microhabitat, but it can also form a microhabitat in and of itself. That fibres can provide habitat to microbes (and their effects) has long been known. Arguably, aspects of this effect were understood before microbes had even been discovered. For example, the idea that clothes of sick individuals could, themselves, cause disease, was understood before the elaboration of germ theory [36,37]. The first scientific demonstration of the relationship between textiles and disease was made by Joseph Lister, who in 1867 demonstrated that treating bandages with an antiseptic could prevent the infection of wounds [38].

Today, it is well known that textiles can support the growth of bacteria and fungi as they have been found to degrade natural fibres, and to a lesser extent, synthetic fibres. Textile-degrading taxa include the fungal genera Aspergillus, Penicillium and Microsporum and bacterial genera Bacillus, Streptomyces and Pseudomonas [39]. Microbial growth on textiles can cause unpleasant odours, physical irritation, and the loss of tensile strength and decolorization of the fabric [39,40]. Synthetic fibres are often resistant to microbial attack because microbial enzymes tend to have difficulty breaking their carbon linkages due in part to their hydrophobic nature [41–43] and poor adsorbing capacity [44]. Biodegradation of synthetic fibres is often facilitated by physical damage, chemical decomposition due to microbial metabolites or enzymatic attacks [45]. By contrast, natural fibres are more susceptible to microbial attack because they tend to have high moisture retention properties and their polymer linkages can be more readily accessed by microbial enzymes [46], especially after fabric processing in which their protective layers are removed. Additionally, natural fibres can provide nutrients and energy sources for microbes in the form of carbohydrates or proteins [43]. Characteristics of the fabric itself (i.e. woven, nonwoven, knitted, thickness, etc.) can also impact moisture and heat retention properties of the fabric [47,48], which may in turn affect resident microorganisms.

For bacteria, adhesion is the precursor to the colonization of a clothing surface. It precedes proliferation and subsequent biofilm formation [49]; bacteria that do not adhere to textiles are readily washed off. Different bacteria species appear to differ in their ability to adhere to various textile types. For instance, Staphylococcus spp. were observed to adhere to cotton, polyester and their blends far better than Escherichia coli [50].

Bacteria–fabric contact conditions also have a large impact on bacterial adhesion to fabric. Agitation, fabric water absorbency and saturated wetting seem to increase the interactions between bacterial cells and the fibre of interest, therefore increasing bacterial adherence on the fibre [50,51]. Hydrophobicity also plays a significant role in bacterial adherence because bacteria with hydrophobic properties tend to adhere better to hydrophobic surfaces, while those with hydrophilic properties tend to adhere better to hydrophilic surfaces [52].

Like a forest or any other habitat, clothing has texture and topography that affect which species survive and how well. Generally, bacteria tend to adhere to rough surfaces better than smooth surfaces [53]. Rough surfaces have a larger surface area and more depressions, which increase the likelihood of colonization [54,55]. Scanning electron microscopy (SEM) micrographs from a study by Bajpai et al. corroborate this, as they demonstrate that bacterial cells do not cover the entire fabric surface uniformly—their numbers tend to be higher near rough surfaces of the fibre [56]. Additional studies have also observed that adherent bacteria preferentially attach along the creases of fibre surfaces [57].

It seems likely that the ability of microbes to colonize and live in clothing allowed the evolution of species able to depend on this new habitat, perhaps sometimes with negative consequences for the clothing-wearer. Whether this has been the case for microbes is not yet well-studied, but we know it from slightly larger organisms—lice. Body lice (Pediculus humanus corporis or Pediculus humanus humanus) are obligate human ectoparasites that live in clothing and feed on the body, in contrast with head lice (Pediculus humanus capitis), which both live and feed exclusively on the scalp. Recently, it has been shown that body lice are not a single species, but instead many lineages that have independently evolved from head lice, and vice versa [58–60]. The origin of the first body lice lineage is often thought to have occurred with the advent of clothing [58]. However, more germane to our topic, the fact that both head and body lice have evolved repeatedly to take advantage of clothing suggests that the same is almost certainly true for even faster-reproducing, faster-evolving organisms such as bacteria and fungi.

6. A blurred line between clothing microbes and skin microbes

When most clothes were made from animal skins, it seems likely that microbes associated with clothing would have been strongly influenced by the microbes that colonize the living animal itself. This microbial community may also have been affected by animal hide processing, such as ancient leather tanning and fur dressing methods primarily meant to prevent hide decay. Ancient animal skin processing involved various materials, including salts, urine, fats and vegetable tannins [61], which could have impacted not only the microbial community of the processed clothing but also that of the wearer. It then follows that when humans were wearing clothes from animal skins, there were opportunities not only for microbes on those skins to continue to grow, but also for those microbes to make the ‘jump’ to human skin.

We do not know of any studies of transfer of skin microbes from dead skin (the clothing) to living skin (the wearer), but the transfer of microbes, including non-pathogenic microbes, from the skin of one person to another is well-established [62], as is transfer from dogs to humans [62]. We hypothesize that the consistent wearing of animal skins and plants is likely to have led to the transfer of microbes from those animals and plants to human skin. It is possible that such transfers left a persistent legacy on the human skin microbiota, which is an intriguing, yet unexplored question. Recent work has shown that skin microbes of mammals tend to reflect the evolutionary history of those mammals [63,64]. This might be expected both because of vertical inheritance of microbes (from mother and father to child) and because more closely related mammals have more similar skin habitats [63]. The probability of transfer might also depend on the frequency of contact. It is noteworthy that studies of mammal skin microbiomes have found relatively similar microbes on some domestic mammals and humans, perhaps as an indication of ancient transfers [63].

One route to the study of changes in skin microbiomes associated with wearing clothing is through the use of ancient DNA and protein to study skin of the long dead. Recent studies of mummies have revealed some intact skin microbiota [65,66]. It seems likely that in the coming years many more studies of ancient DNA on old textiles will be carried out. When they are, we will gain a better understanding of both ancient clothing microbiology and, perhaps to some extent, ancient skin microbes, as well as the exchanges between skin and clothing.

While we are uncertain whether animal microbes on clothing permanently colonized human skin, or vice versa, we do know that microbes can generally transfer from clothing to skin and back over shorter time periods. This transfer may promote selective bacterial enrichment, that is, when a habitat selects for the growth of certain microbes above others, and so these particular microbes are enriched in numbers compared with their non-selected neighbours. Bacterial enrichment promotes the creation of another microbiome within the textile, which may differ in composition from that of the original skin microbiome [67].

Bacterial enrichment on textiles largely depends on the community living on the skin, the bacterial species, the bacteria–fabric contact conditions and the physico-chemical properties of the clothing textile [50]. Textile dyes and finishes can also have a significant impact on the susceptibility of textiles to microbial attack and may either promote or hinder fabric degradation [68,69]. The three main bacterial phyla found in textiles (Firmicutes, Actinobacteria and Proteobacteria) are also of known importance to the human skin microbiome [67,70]. Like the skin microbiome, the textile microbiome appears to be dominated by Staphylococcus and Micrococcus spp. [67], with the precise species that are present, and their composition, mainly affected by the individual wearing the textile [67,71]. The axillary microbiome, however, is generally dominated by Staphylococcus and Corynebacterium [72]. Some studies have found Corynebacterium spp., one of the main odour-causing microorganisms of the axillae [73], to be undetectable in clothing textiles [67], while others have demonstrated its presence in the textile microbiome [71,74]. These differences may relate to study design. For instance, culture-based methods may miss many species found on samples (whether of skin or textiles). Propionibacterium spp. and Corynebacterium spp. are frequently underestimated in culture-based studies [75]. In addition, the length of time that clothing is worn may also have an effect. In the study that found Corynebacterium spp. on clothing, the clothing was worn for a longer period of time and fabric samples were taken directly from the axillary region. This may have facilitated the transfer of lipids from the apocrine glands to clothing, thus providing support for the growth of Corynebacterium spp. [76]. The native community of various textiles, prior to being worn or washed, must also be taken into account. One study has shown that the native microbiome of cotton textiles is largely dominated by Acinetobacter [71]. These bacteria may originate from fabric processing and manufacturing [71]. Future research should investigate the source of native textile microbiomes, how textile microbiomes differ between fabric types as well as garment types (e.g. shirts, pants, etc.) and their impacts on human skin microbial community structure.

7. Microbial biodegradation of natural and synthetic fibres

Along with the growth of bacteria on fabric comes the inevitable possibility of microbial degradation, the process of which is explained in electronic supplementary material, figure S1. Microbes have the potential to survive on or adapt to nearly any living condition or substrate. As such, it is not surprising that bacteria and fungi have been identified that are associated with the degradation of various fibre materials, as shown in table 1. Surface structures of each fibre discussed below are illustrated in figure 2.

Table 1.

A summary of five primary textiles in use today, their physicochemical characteristics, and the major bacterial and fungal communities that have been isolated from, or associated with the degradation of, the processed and/or raw fibres or fabric. *Organisms from which enzymes have been isolated that have been shown to have PET degradation or hydrolysis capabilities. ** Organisms associated with flax retting.

fibre	fibre type	unprocessed fibre primary composition	unprocessed fibre physicochemical characteristics	major bacterial communities	major fungal communities	references
wool	animal fibre	keratin	extremely cross-linked structure • high concentration of disulfide bridges • surface covered in water-repellent membrane	Bacillus spp. (B. mesentericus, B. subtilis, B. cereus, B. mycoides); Pseudomonas; Streptomyces sp. (Streptomyces fradiae)	Aspergillus spp. (A. cervinus, A. fischeri, A. flavus, A. fumigatus, A. nidulans, A. niger, A. rapier, A. sparsus, A. spinulosus, A. ventii); Chrysosporium sp.; Penicillium spp. (P. canescens, P. cyclopium, P. granulatum, P. lanoso, P. paxilli, P. soopi); Microsporum sp.; Trichopchyton sp.; Fusarium sp.; Rhizopus sp.; Cheatomium sp.; Alternaria sp.; Ulocladium sp.; Stachybotrys chartarum; Scopulariopsis brevicaulis; Acremonium sp.	[40,68]
cotton	vegetable-based fibre	almost purely cellulose	highly fibrillar and crystalline structure • not extensible • fibre is oriented in twists, causing uneven surface structure	Cytophaga sp.; Cellulomonas sp.; Bacillus sp.; Clostridium sp.; Sporocytophaga sp.; Microbispora bispora	Aspergillus spp. (A. versicolor, A. flavus, A. fumigatus, A. niger, A. terreus, A. nidulans, A. ustus, A. fischerii, A. flaschentraegeri); Penicillium spp. (P. notatum, P. citrinum, P. funiculosum, P. cyclopium, P. janthinellum); Cladosporium spp. (C. macrocarpium, C. herbarum); Cheatomimum spp. (C. globusum, C. cochlioides); Alternaria spp. (A. tennuis, A. geophila); Trichoderma spp. (T. viride, T. reesei); Fusarium nivale; Myrothecium sp. Memnoniella sp.; Stachybotrys sp.; Verticillum sp.	[40,77]
silk	animal fibre	fibroin connected by sericin	fibroin has a crystalline structure consisting of 90% alanine, glycine, serine and tyrosine • protein fibres linked by disulfide bridges • hydrogen bonds within and between molecules	Bacillus megaterium; Pseudomomas spp. (P. aureofaciens, P. chlororaphis, P. paucimobilis, P. cepacia); Serratia sp.; Streptomyces sp.; Variovorax paradoxus	Aspergillus spp. (A. flavus, A. niger, A. rapei); Penicillium spp. (P. canescens, P. paxilli); Chaetomium sp.; Cladosporium sp.; Rhizopus sp.	[39,40]
flax	vegetable-based fibre	65–80% cellulose with pectins, hemicellulose, and aromatic compounds in small amounts	bundles of individual fibres encircling the lignified core tissues • noncellulosic carbohydrates present within the cellulosic structure • high moisture regain	**Achromobacter parvulus; **Clostridium spp. (C. beijerinckii, C. saprogenes, C. saccaroacetoperbutylicum, C. perenne, C. felsineum, C. acetobutylicum); **Pseudomonas spp. (P. aeruginosa, P. fluorescens, P. putida); **Micrococcus sp.; **Bacillus spp. (B. amylobacter, B. felsineus, B. comesii rossi, B. mycoides, B. subtilis, B. licheniformis); **Granulobacter pectinovorum; **Erwinia carotovora	**Cladosporium herbarum; **Mucor spp. (M. stolonifer, M. hiemalis, M. plumbens); **Epicoccum nigrum; **Rhizopus sp.; **Botrytis cineria; **Aureobasidium pululans; **Phoma sp.; **Rhizomucor pusillus; Aspergillus spp. (A. flavus, A. fumigatus, **A. niger, A. terreus, A. nidulans, A. ustus, A. fischeri, A. auratus, A. carbonarius, A. proliferans, A. spinulosus); **Penicillium spp. (P. funiculosum, P. rajstrickii, P. biforme, P. soopi); Trichoderma viride; **Alternaria alternata; Cheatomium cochlioides; Fusarium spp. (F. nivale, **F. culmorum)	[40,78–85]
polyethylene terephthalate (PET)	synthetic fibre	terephthalic acid and ethylene glycol linked by ester bonds	consists of non-polar, saturated, high molecular weight hydrocarbons • ability to accumulate electrostatic charges on the surface • combination of crystalline and non-crystalline regions	Ideonella sakaiensis; *Pseudomonas mendocina; *Bacillus spp. (B. subtilis, B. licheniformis); *Thermobifida spp. (T. alba, T. cellulosilytica, T. fusca, T. halotolerans); *Clostridium botulinum; *Saccharomonospora viridis; *Thermomonospora curvata	*Thermomyces spp. (T. insolens, T. lanuginosus); *Penicillium citrinum; *Candida antarctica; *Fusarium spp. (F. solani pisi, F. solani, F. oxysporum); *Aspergillus oryzae	[86–111]

Figure 2.

Scanning electron microscopy micrographs of various fibres. Adapted from micrograph by Leo Barish, Albany International Corporation [112].

(a). Wool

Wool is a natural fibre primarily composed of keratin. It is characterized by an extremely cross-linked structure and has a high concentration of disulfide bridges owing to the high proportion of cysteine residues in keratin [68,113]. The surface of raw wool fibre is covered in a natural, water-repellent membrane. Therefore, under clean, dry conditions, raw wool has a naturally strong resistance to microbial attack [114]. During fabric processing, woollen raw materials undergo rigorous mechanical, chemical and photochemical treatments that increase the susceptibility of the fibres to biodegradation [40]. Not only does this processing remove the protective membrane of the wool, but the high pH conditions during processing make wool more susceptible to breakdown by microbial enzymes [68]. These enzymes chemically reduce the disulfide bonds in wool, then hydrolyse the wool's peptide linkages [68,115]. Biodeterioration of wool is caused by both bacteria and fungi. However, keratin is often degraded to a higher degree by keratinolytic fungi such as species of the genera Microsporum, Trichophyton and Fusarium than by bacteria [39].

(b). Silk

Silk is a natural protein-based fibre produced by silkworms (Bombyx mori) domesticated in China around 2640 BC [116]. Unprocessed silk fabric consists of protein fibres called fibroin that are connected to one another by a rubber-like protein known as sericin [39]. Degummed silk, which lacks sericin, is currently used to produce silk fabric, as sericin is known to turn yellow over time (though degumming makes the fabric more susceptible to light-induced damage). There are conflicting reports about the intrinsic antimicrobial nature of silk, with some studies demonstrating that sericin may have antimicrobial properties [117] while others suggest that bacteria may assimilate sericin easier than fibroin for growth [118,119]. Such opposing reports are likely a result of differences in silk processing as more recent work by Kaur et al. has shown that residual silk processing chemicals may assist in inhibiting or killing bacteria if not removed and may yield misleading results [120].

(c). Cotton

Cotton is a vegetable-based fibre principally composed of cellulose [121]. The proportion of cellulose to other biomolecules in vegetable-based textile fibres is much higher than other plant-derived materials, comprising 90–99% in cotton but only 45% in wood [68]. To use cellulosic fibres as a carbon source, glucose must be released from cellulose through the synergistic efforts of three hydrolytic enzymes: endoglucanases (EC 3.2.1.4), exoglucanases (EC 3.2.1.91) and β-glucosidases (EC 3.2.1.21) [39,122]. This attack is dependent on the breakdown of the natural waxy cuticle, which protects the plant from environmental damage, water loss, and pathogenic invasion [39,123]. However, during the intense processing of raw cotton, the cuticle as well as other impurities are removed. This results in reduced strength of the cotton fibres, making the processed fabric more susceptible to microbial attacks which cause a reduction in the degree of cellulose polymerization and a breakage of fibre structure [40].

(d). Flax

Flax (most commonly L. angustifolium and L. usitatissimum) is another vegetable-based fibre and is used to produce the fabric linen. Flax is a bast fibre, meaning it is part of the inner bark of the stem of a dicotyledonous plant, and is composed of a complex mixture of different polymers such as cellulose, hemicellulose, lignin and pectin [124]. Linen fabric has high strength and high moisture retention, likely owing to the presence of noncellulosic carbohydrates within the cellulosic structure [78]. During fabric processing, the flax plant undergoes retting by various means to separate flax fibres from the stem of the plant by degrading pectin and other natural adhesives [125], followed by mechanical treatments to remove non-fibre impurities, then final processing and spinning of the fibres into yarn to produce linen [126]. Raw flax straw that has not been retted requires even more intense decortication and extensive processing to yield fibres that can be spun into yarn [126]. Since the epidermis and woody core of the flax have been removed during processing, the linen no longer has a protective layer of cuticle and waxes and may potentially have weakened cellulose owing to cellulases present during retting, making its cellulosic fibres more vulnerable to microbial attack.

(e). Polyester

Polyester is a human-made fibre defined as a ‘manufactured’ fibre in which the fibre-forming substance is composed of ‘at least 85% by weight of an ester of a dihydric alcohol and terephthalic acid’ [127, p. 191], with the most common polyester used for clothing being polyethylene terephthalate (PET). Polyester fibres used for clothing can be either staple fibres, which are short fibres that are often twisted together to form a yarn, or filament fibres, which are long continuous strands; each of these fibre types has its own unique properties [87]. Polyester filament yarn currently dominates the polyester market, accounting for 44% of the global polyester production in 2016 [128]. Polyester fibres are strong, have low moisture absorption and are resistant to dilute acids, alkalis and organic solvents [87]. Polyester and many other synthetic polymers are difficult for microorganisms to degrade owing to physical limitations imposed by their insolubility in aqueous media, the lack of functional groups and high molecular weights [129]. One study reported that a 100% polyester shirt only suffered a 20% weight loss following a 90-day soil burial test, while processed cotton fabric samples at various levels of finishing treatments suffered a weight loss of between 50 and 77% under the same conditions [130].

8. The downside of microbes in clothing

While the presence of microbes in clothing is as old as clothing itself, it may sometimes cause problems for human health. Healthcare-associated infections (HCAIs) are among the leading causes of death in the USA [131]. These infections are caused by the transmission of harmful microorganisms from an infected patient, healthcare worker or environmental source to another individual in any setting in which patients receive healthcare. Though hygiene is one factor contributing to the prevalence of HCAIs, another potential source for transmission is hospital coats worn by doctors and other medical professionals, as microbes have the potential to persist within the textile. Several studies have found potentially pathogenic bacteria in hospital staff uniforms, some of which were drug-resistant organisms such as methicillin-resistant S. aureus (MRSA) and vancomycin-resistant enterococci (VRE) [132–135]. One investigation linked a cluster of three cases of Gordonia bronchialis infection to a nurse anaesthetist who tested positive for the bacterium [136,137]. After decontamination, including disposal of her household washing machine, she tested negative for G. bronchialis, and the outbreak eventually ceased. This supports the notion that eradication programmes aimed at identifying bacterial reservoirs, including clothing and washing machines, and using directed infection control practices are highly effective in reducing HCAIs [138].

Industrial laundry procedures, which tend to be preferred in hospitals over home laundering of uniforms, are generally sufficient to remove microbial contaminants from garments. However, recontamination has been shown to occur quickly [139], with one study by Burden et al. discovering that uniforms that were almost sterile prior to use accumulated almost 50% of their 8 h measured colony-forming unit (CFU) count after only 3 h of wear [140]. While home laundering is permitted for non-contaminated uniforms that are not considered personal protective equipment [141,142], its effectiveness in reducing microbial contamination is dependent on personnel compliance with established guidelines [136]. Laundering must be combined with other control practices for maximum effectiveness [136].

9. Future perspectives

One challenge as we consider the clothing of the future relates to sustainability. On a global scale, an estimated 48 million tonnes of clothes are discarded annually, approximately 75% of which are either sent to landfills or incinerated; only about 20% is recycled [143]. Since most synthetic textiles are not readily biodegradable, considerable environmental pollution can occur as a result, with synthetic clothing contributing about 35% of the global release of microplastics into oceans [144].

With this in mind, the notion of a circular model of textile production rather than the current linear economy model has begun to gain traction over the past several years. In the linear model, resources are extracted, processed, distributed, consumed and ultimately discarded as waste. Not only does the process generate massive amounts of waste and environmental pollution, but it also loses the industry money—an estimated 500 billion US dollars globally per year [145]. By contrast, the circular model aims for an economy in which textiles are maintained at their highest value during use and re-enter the economy after use to reduce waste [145]. This model supports the use of renewable resources in the event virgin inputs are required and aims to reduce toxic chemical usage and microfibre release into the environment through a complete overhaul of current processes [145]. Several companies have already taken the first steps towards this goal. For example, H&M collected over 17 000 tonnes of clothing and footwear for recycling in 2017 [146], while Nestlé announced in early 2020 that they would invest $2.1 billion towards reducing their use of virgin plastics in favour of recycled plastics [145].

Investigating microbes with the ability to persist on synthetic fibres, or use synthetic polymers, may reveal mechanisms that have industrial applications or that can be used to degrade these products in the environment. For example, an enzyme with polyethylene terephthalate-hydrolysing properties, designated a PETase, was recently isolated from Ideonella sakiensis and has shown promising results when used in a photosynthetic microalga to produce and express an engineered version of the PETase into the surrounding media [86,147].

Another challenge relates to the desire for antimicrobial textiles. Antimicrobial textiles have been used for thousands of years, with even ancient Egyptians using herbs and spices to preserve mummy wraps and prevent the growth of bacteria [148]. Antimicrobial substances can be used to diminish both the transient and resident skin flora to reduce the risk of pathogenic infection and transmission [30]. In recent years, increased consumer demand for hygienic clothing and athletic wear, as well as the need to reduce HCAIs, has made the antimicrobial textile industry one of the fastest-growing markets in the textile sector [149]. However, recent work has demonstrated that antimicrobial fabrics alone may not be enough to reduce overall contamination, and factors such as fluid repellency must be considered in order to increase the efficacy of the antimicrobial agent [136]. Further, the long-term effects of antimicrobial clothing on the body are not yet clear. Some antimicrobial textiles show promise for combating skin conditions such as atopic dermatitis and atopic eczema [30]. However, many of the compounds used in antimicrobial clothing [150] are likely to have negative effects on beneficial skin microbes in addition to their target effects on pathogens. While several studies have concluded that antimicrobial clothing had no adverse effects on healthy skin microflora [151,152], the studies were short term and we are only beginning to understand which microbes should be present on healthy skin (and hence which might be missing [153]).

10. Conclusion

Human lifestyles have changed dramatically since the invention of clothing. The nature of clothing has evolved from animal skins to complex blends of synthetic fibres over the course of thousands of years. While it seems likely that clothing has strongly influenced the human microbial community, more work must be done to definitively understand the effects of clothing on the human microbiome, especially the skin microbiome. Rapid technological advances now provide the opportunity to potentially explore the microbial communities of well-preserved prehistoric animal and human specimens, which may offer key insight into the evolution of the human microbiome. Advances in DNA extraction protocols and sequencing sensitivity will enable a more accurate identification of the textile microbiome. Further research should be done to elucidate the microbiome of a wider variety of textiles so as to better understand the relationship between microbes, textile fabrics and human skin. Opportunities for novel research abound as we seek not only to better understand our microbial neighbours, but also to use that understanding to improve upon our current production of textiles while mitigating the impacts of textile production on the environment.

Data accessibility

This article has no additional data.

Authors' contributions

D.S. and R.R.D. conceived the presented idea. D.S. took the lead in writing the manuscript, with support from R.R.D. and A.G. R.R.D. and A.G. provided critical feedback and helped shape the content of the manuscript. All authors discussed the presented information, contributed to and approved the final manuscript, and agree to be held accountable for all aspects of the work.

Competing interests

We declare we have no competing interests.

Funding

We would like to thank NIH MBTP (1T32GM133366-01 and 5T32GM008776-20) and HanesBrands, Inc. (MRA-20170213) for providing support to D.S.