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Spatial variations in the microbial community structure and diversity of the human foot is associated with the production of odorous volatiles
Abstract and Figures
The human foot provides an ideal environment for the colonization and growth of bacteria and subsequently is a body site associated with the liberation of odour. This study aimed to enumerate and spatially map bacterial populations' resident across the foot to understand any association with odour production. Culture-based analysis confirmed that Staphylococci were present in higher numbers than aerobic corynebacteria and Gram-positive aerobic cocci, with all species being present at much higher levels on the plantar sites compared to dorsal sites. Microbiomic analysis supported these findings demonstrating that Staphylococcus spp. were dominant across different foot sites and comprised almost the entire bacterial population on the plantar surface. The levels of volatile fatty acids, including the key foot odour compound isovaleric acid, that contribute to foot odour were significantly increased at the plantar skin site compared to the dorsal surface. The fact that isovaleric acid was not detected on the dorsal surface but was present on the plantar surface is probably attributable to the high numbers of Staphylococcus spp. residing at this site. Variations in the spatial distribution of these microbes appear to be responsible for the localized production of odour across the foot.
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... Moreover, a clinical study by Stevens et al. have explored the spatial distribution of bacterial populations and related VOCs using various sampling techniques, with PDMS patch type sampling being one of them [40]. In this study, PDMS patches were used for VOC sampling. ...
Biological surfaces such as skin and ocular surface provide a plethora of information about the underlying biological activity of living organisms. However, they pose unique problems arising from their innate complexity, constant exposure of the surface to the surrounding elements, and the general requirement of any sampling method to be as minimally invasive as possible. Therefore, it is challenging but also rewarding to develop novel analytical tools that are suitable for in vivo and in situ sampling from biological surfaces. In this context, wearable extraction devices including passive samplers, extractive patches, and different microextraction technologies come forward as versatile, low-invasive, fast, and reliable sampling and sample preparation tools that are applicable for in vivo and in situ sampling. This review aims to address recent developments in non-invasive in vivo and in situ sampling methods from biological surfaces that introduce new ways and improve upon existing ones. Directions for the development of future technology and potential areas of applications such as clinical, bioanalytical, and doping analyses will also be discussed. These advancements include various types of passive samplers, hydrogels, and polydimethylsiloxane (PDMS) patches/microarrays, and other wearable extraction devices used mainly in skin sampling, among other novel techniques developed for ocular surface and oral tissue/fluid sampling.
... Certain bacteria such as Staphylococcus epidermidis and Bacillus subtilis contribute to foot odor by breaking down branched-chain of amino acids (leucine or valine) in sweat into isovaleric acid at the plantar skin site. The human foot provides an ideal environment for the colonization of these bacteria due to its high nutrients and humidity (Stevens et al., 2015). ...
Foot odor or bromhidrosis occurs due to the activity of bacteria that convert leucine in sweat into isovaleric acid which results in unpleasant odors. Honey pineapple skin (Ananas comosus [L.] Merr) is generally waste, whereas honey pineapple skin is known to contain antibacterial compounds. The aim of this study is to determine the potential of honey pineapple peel as an active ingredient in footspray based on the results of phytochemical screening and physical evaluation. Honey pineapple peel was extracted by maceration method using ethanol 70% then phytochemical test. Footspray preparations were made with various extract concentrations of 0%, 25%, 35% and 45% then tested for organoleptic, pH, specific gravity, viscosity, homogeneity, spreadability, and dry time during storage period of 0, 7, 14 and 21 days at room temperature. This study showed that honey pineapple peel extract contained flavonoids, tannins, phenols and alkaloids. The footspray has brown color with honey pineapple scent, pH of 5.71-6.37, specific gravity 1.05-1.09 g/mL, viscosity 7.2-13.2 cP, spreadability 6.67-7.60 cm, and the dry time is 4-5 minutes. Footspray containing honey pineapple peel extract with concentrations of 25%, 35% and 45% has a pH value that is safe for the skin, with good specific gravity, viscosity, homogeneity and spreadability, also stable during storage. Formula 1 (25% extract concentration) tends to be preferred because its texture is soft and not too sticky when applied to the skin when compared with formula 2 and 3.
... Different body sites exhibit different odor characteristics, with the latter driven by the type of secretory glands present and the unique micro-environmental conditions and microbiomic profile of each area, e.g. axilla, foot, or scalp skin [65,83,133,181]. In terms of their contribution to odor intensity and unpleasantness, contributions by glandular type may be ranked in the following order: apocrine, eccrine, and sebaceous gland [85]. ...
Humans produce odorous secretions from multiple body sites according to the microbiomic profile of each area and the types of secretory glands present. Because the axilla is an active, odor-producing region that mediates social communication via the sense of smell, this article focuses on the biological mechanisms underlying the creation of axillary odor, as well as the intrinsic and extrinsic factors likely to impact the odor and determine individual differences. The list of intrinsic factors discussed includes sex, age, ethnicity, emotions, and personality, and extrinsic factors include dietary choices, diseases, climate, and hygienic habits. In addition, we also draw attention to gaps in our understanding of each factor, including, for example, topical areas such as the effect of climate on body odor variation. Fundamental challenges and emerging research opportunities are further outlined in the discussion. Finally, we suggest guidelines and best practices based on the factors reviewed herein for preparatory protocols of sweat collection, data analysis, and interpretation.
Armpit odors of different individuals were qualitatively and quantitatively collected and analyzed by gas chromatography–mass spectrometry (GC–MS). The results showed that human armpit odor contained 27 substances, including acids, ketones, alcohols, alkanes, and two noticeable odorants of n‐nonaldehyde and dodecanol. A headspace solid‐phase microextraction/gas chromatography–mass spectrometry method determined that both n‐nonaldehyde and dodecanol with distinct characteristic peaks were common chemicals found in the body odors with detection limits at 46.88 and 17.50 ng/L, respectively. The limits of quantitation of both were 156.25 and 59.33 ng/L with relative standard deviation (RSD) less than 5%, and recoveries ranged from 85% to 115%, respectively. The removal of body odor on a moisture‐wicking polyester fabric was quantified through by placement, washing, and deodorant finishing methods. The placement method needs at least 2 days for removing the majority of the odor. Sports washing liquid was the best detergent to remove odors with a removal rate of 76.44% for n‐nonaldehyde and 87.88% for dodecanol. Deodorant finishing is a convenient and efficient method for removing odors with masking effect of added fragrance. The deodorants were able to remove over 85% of n‐nonaldehyde and 75% of dodecanol after drying, indicating that deodorant treatment is an effective method for removing odorous substances. This successful approach in eliminating human odors could offer valuable insights for the advancement of sportswear and hygiene textiles.
Human skin emits a series of volatile compounds from the skin due to various metabolic processes, microbial activity, and several external factors. Changes in the concentration of skin volatile metabolites indicate many diseases, including diabetes, cancer, and infectious diseases. Researchers focused on skin-emitted compounds to gain insight into the pathophysiology of various diseases. In the case of skin volatolomics research, it is noteworthy that sample preparation, sampling protocol, analytical techniques, and comprehensive validation are important for the successful integration of skin metabolic profiles into regular clinical settings. Solid-phase microextraction techniques and polymer-based active sorbent traps were developed to capture the skin-emitted volatile compounds. The primary advantage of these sample preparation techniques is the ability to efficiently and targetedly capture skin metabolites, thus improving the detection of the biomarkers associated with various diseases. In further research, polydimethyl-based patches were utilized for skin research due to their biocompatibility and thermal stability properties. The microextraction sampling tools coupled with high sensitive Gas Chromatography-Mass Spectrometer provided a potential platform for skin volatolomes, thus emerging as a state-of-the-art analytical technique. Later, technological advancements, including the design of wearable sensors, have enriched skin-based research as it can integrate the information from skin-emitted volatile profiles into a portable platform. However, individual-specific hydration, temperature, and skin conditions can influence variations in skin volatile concentration. Considering the subject-specific skin depth, sampling time standardization, and suitable techniques may improve the skin sampling techniques for the potential discovery of various skin-based marker compounds associated with diseases. Here, we have summarised the current research progress, limitations, and technological advances in skin-based sample preparation techniques for disease diagnosis, monitoring, and personalized healthcare applications.
Solid Phase Microextraction (SPME) is a flexible and convenient sampling and sample preparation technique that extracts different kinds of analytes, including both volatile and non-volatile, without the use of a solvent. The technique facilitates fast, simple and automated determination of target analytes in a range of matrices. As it offers a green methodology, it is growing in popularity as an alternative tool in analytical chemistry to traditional methods. This book follows on in spirit from the editors’ previous title, Applications of Solid Phase Microextraction and will introduce the reader to breakthrough methodologies and cutting edge applications. Although it assumes a good degree of SPME knowledge, an overview of the fundamentals is given before taking the reader through an update of the field.
The reader will learn the basic principles and advantages of different SPME formats including the stir bar extraction techniques, thin film SPME, Bio-SPME, and new trends in different coatings. Applications in complex media, including food analysis, drug residues and bioanalysis are covered.
Bringing together leading sample preparation academics from around the world, the editor has put together an informative new book, suitable for analytical chemists and practitioners utilising SPME tools in their research.
Solid Phase Microextraction (SPME) is a flexible and convenient sampling and sample preparation technique that extracts different kinds of analytes, including both volatile and non-volatile, without the use of a solvent. The technique facilitates fast, simple and automated determination of target analytes in a range of matrices. As it offers a green methodology, it is growing in popularity as an alternative tool in analytical chemistry to traditional methods. This book follows on in spirit from the editors’ previous title, Applications of Solid Phase Microextraction and will introduce the reader to breakthrough methodologies and cutting edge applications. Although it assumes a good degree of SPME knowledge, an overview of the fundamentals is given before taking the reader through an update of the field.
The reader will learn the basic principles and advantages of different SPME formats including the stir bar extraction techniques, thin film SPME, Bio-SPME, and new trends in different coatings. Applications in complex media, including food analysis, drug residues and bioanalysis are covered.
Bringing together leading sample preparation academics from around the world, the editor has put together an informative new book, suitable for analytical chemists and practitioners utilising SPME tools in their research.
Introduction
Sebum-based metabolomics (a subset of “sebomics”) is a developing field that involves the sampling, identification, and quantification of metabolites found in human sebum. Sebum is a lipid-rich oily substance secreted by the sebaceous glands onto the skin surface for skin homeostasis, lubrication, thermoregulation, and environmental protection. Interest in sebomics has grown over the last decade due to its potential for rapid analysis following non-invasive sampling for a range of clinical and environmental applications.
Objectives
To provide an overview of various sebum sampling techniques with their associated challenges.
To evaluate applications of sebum for clinical research, drug monitoring, and human biomonitoring.
To provide a commentary of the opportunities of using sebum as a diagnostic biofluid in the future.
Methods
Bibliometric analyses of selected keywords regarding skin surface analysis using the Scopus search engine from 1960 to 2022 was performed on 12th January 2023. The published literature was compartmentalised based on what the work contributed to in the following areas: the understanding about sebum, its composition, the analytical technologies used, or the purpose of use of sebum. The findings were summarised in this review.
Results
Historically, about 15 methods of sampling have been used for sebum collection. The sample preparation approaches vary depending on the analytes of interest and are summarised. The use of sebum is not limited to just skin diseases or drug monitoring but also demonstrated for other systemic disease. Most of the work carried out for untargeted analysis of metabolites associated with sebum has been in the recent two decades.
Conclusion
Sebum has a huge potential beyond skin research and understanding how one’s physiological state affects or reflects on the skin metabolome via the sebaceous glands itself or by interactions with sebaceous secretion, will open doors for simpler biomonitoring. Sebum acts as a sink to environmental metabolites and has applications awaiting to be explored, such as biosecurity, cross-border migration, localised exposure to harmful substances, and high-throughput population screening. These applications will be possible with rapid advances in volatile headspace and lipidomics method development as well as the ability of the metabolomics community to annotate unknown species better. A key issue with skin surface analysis that remains unsolved is attributing the source of the metabolites found on the skin surface before meaningful biological interpretation.
Volatile biomarkers play a significant signalling role in communication between biological cells living as individual entities or as mini-societies that sense, respond and adapt to changes in their environment. In this process, volatile biomarkers can leak into the blood, from which they can be secreted into most body fluids (blood, breath, skin, urine, saliva, feces, etc.), from which sensing devices can capture and interpret their chemical fingerprint to reflect any association with health disorders in a fast, easy, and minimally non-invasive manner.
This book introduces the concept of biomarkers within the body in terms of basic and translational sciences. It starts with a comprehensive review of the expression and mechanistic pathways involving volatile biomarkers at single cell and (micro)organism levels, cell-to-cell and cell-to-organism communications, and their secretion into body fluids. It discusses several ways for discovering and detecting the secreted biomarkers using mass spectrometry and other spectroscopic techniques. This is followed by an appraisal and translation of the accumulating knowledge from the laboratory to the Point-of-Care phase, using selective sensors as well as desktop and wearable artificial sensing devices, e.g., electronic noses and electronic skins, in conjugation with AI-assisted data processing and healthcare decision-making in diagnostics. The book offers an outlook into the challenges in the continuing development of volatile biomarkers and their wider availability to healthcare, which can be substantially improved. It should appeal to research groups in universities, start-up and large-scale industries associated in all aspects of biomedicine.
Volatile biomarkers play a significant signalling role in communication between biological cells living as individual entities or as mini-societies that sense, respond and adapt to changes in their environment. In this process, volatile biomarkers can leak into the blood, from which they can be secreted into most body fluids (blood, breath, skin, urine, saliva, feces, etc.), from which sensing devices can capture and interpret their chemical fingerprint to reflect any association with health disorders in a fast, easy, and minimally non-invasive manner.
This book introduces the concept of biomarkers within the body in terms of basic and translational sciences. It starts with a comprehensive review of the expression and mechanistic pathways involving volatile biomarkers at single cell and (micro)organism levels, cell-to-cell and cell-to-organism communications, and their secretion into body fluids. It discusses several ways for discovering and detecting the secreted biomarkers using mass spectrometry and other spectroscopic techniques. This is followed by an appraisal and translation of the accumulating knowledge from the laboratory to the Point-of-Care phase, using selective sensors as well as desktop and wearable artificial sensing devices, e.g., electronic noses and electronic skins, in conjugation with AI-assisted data processing and healthcare decision-making in diagnostics. The book offers an outlook into the challenges in the continuing development of volatile biomarkers and their wider availability to healthcare, which can be substantially improved. It should appeal to research groups in universities, start-up and large-scale industries associated in all aspects of biomedicine.
Humans host complex microbial communities believed to contribute to health maintenance and, when in imbalance, to the development of diseases. Determining the microbial composition in patients and healthy controls may thus provide novel therapeutic targets. For this purpose, high-throughput, cost-effective methods for microbiota characterization are needed. We have employed 454-pyrosequencing of a hyper-variable region of the 16S rRNA gene in combination with sample-specific barcode sequences which enables parallel in-depth analysis of hundreds of samples with limited sample processing. In silico modeling demonstrated that the method correctly describes microbial communities down to phylotypes below the genus level. Here we applied the technique to analyze microbial communities in throat, stomach and fecal samples. Our results demonstrate the applicability of barcoded pyrosequencing as a high-throughput method for comparative microbial ecology.
Traditional culture-based methods have incompletely defined the microbial landscape of common recalcitrant human fungal skin diseases, including athlete's foot and toenail infections. Skin protects humans from invasion by pathogenic microorganisms and provides a home for diverse commensal microbiota. Bacterial genomic sequence data have generated novel hypotheses about species and community structures underlying human disorders. However, microbial diversity is not limited to bacteria; microorganisms such as fungi also have major roles in microbial community stability, human health and disease. Genomic methodologies to identify fungal species and communities have been limited compared with those that are available for bacteria. Fungal evolution can be reconstructed with phylogenetic markers, including ribosomal RNA gene regions and other highly conserved genes. Here we sequenced and analysed fungal communities of 14 skin sites in 10 healthy adults. Eleven core-body and arm sites were dominated by fungi of the genus Malassezia, with only species-level classifications revealing fungal-community composition differences between sites. By contrast, three foot sites-plantar heel, toenail and toe web-showed high fungal diversity. Concurrent analysis of bacterial and fungal communities demonstrated that physiologic attributes and topography of skin differentially shape these two microbial communities. These results provide a framework for future investigation of the contribution of interactions between pathogenic and commensal fungal and bacterial communities to the maintainenace of human health and to disease pathogenesis.
A single nucleotide polymorphism (SNP), 538G→A, leading to a G180R substitution in the ABCC11 gene results in reduced concentrations of apocrine derived axillary odour precursors.
Determine the axillary odour levels in the SNP ABCC11 genotype variants and to investigate if other parameters associated with odour production are affected.
Axillary odour was assessed by subjective quantification and gas chromatography headspace analysis. Metabolite profiles, microbiome diversity and personal hygiene habits were also assessed.
Axillary odour in the A/A homozygotes was significantly lower compared to the G/A and G/G genotypes. However, the perception-based measures still detected appreciable levels of axillary odour in the A/A subjects. Metabolomic analysis highlighted significant differences in axillary skin metabolites between A/A subjects compared to those carrying the G allele. These differences resulted in A/A subjects lacking specific volatile odourants in the axillary headspace, but all genotypes produced odoriferous short chain fatty acids. Microbiomic analysis revealed differences in the relative abundance of key bacterial genera associated with odour generation between the different genotypes. Deodorant usage indicated a high level of self awareness of axillary odour levels with A/A individuals less likely to adopt personal hygiene habits designed to eradicate/mask its presence.
The SNP in the ABCC11 gene results in lower levels of axillary odour in the A/A homozygotes compared to those carrying the G allele, but A/A subjects still produce noticeable amounts of axillary odour. Differences in axillary skin metabolites, bacterial genera and personal hygiene behaviours also appear to be influenced by this SNP.
Although foot malodour is a common consumer problem, the range of products available to combat the condition is fairly limited. In part, this is due to an incomplete understanding of how the key odorants are generated by microorganisms resident on the skin. The aim of these studies was to identify the key chemical components of foot malodour, the organisms and metabolic pathways responsible for their production, and to develop model systems to study these processes in vitro. Using gas chromatography with simultaneous mass spectrometry and sniff port detection, volatile fatty acids were implicated as foot malodorants, with isovaleric acid particularly prominent. l-Leucine was identified as the likely substrate, and the source of this branched amino acid postulated to be the degradation of foot callus. An in vitro assay was employed to screen a library of isolated foot bacteria for their ability to generate isovaleric acid from l-leucine. Staphylococcus species were found to be the main producers, while some Brevibacterium, Micrococcus and Kytococcus isolates fully catabolized isovaleric acid and l-leucine, indicating the dynamic nature of odour production. The degradation of foot callus by Kytococcus sedentarius was investigated, and an in vitro ‘foot malodour model’ developed, demonstrating the generation of isovaleric acid using a combination of partially purified K. sedentarius keratinases and a Staphylococcus species. The results of these studies provide new understanding on the microbiological and biochemical origins of foot malodour which, in turn, should lead to the development of novel deodorant systems for this part of the body. Copyright © 2012 John Wiley & Sons, Ltd.