Towards a bacterial treatment for armpit malodour
Abstract
Axillary malodour is a frustrating condition for many people. It can lead to significant discomforts and various psychological effects. The underarm microbiome plays a major role in axillary malodour formation. Not only the bacteria on the epidermis, but also and especially those living in the sweat glands, sweat pores and hair follicles play a pivotal role in malodour development. To treat underarm malodour, this viewpoint article envisions a bacterial treatment. Replacing the autochthonous malodour-causing microbiome with a non-odour-causing microbiome, through an armpit bacterial transplantation or direct application of probiotics/non-odour-causing bacteria, could resolve the condition. Selective steering of the microbiome with prebiotics, biochemicals or plant extracts can likewise greatly help in improving the underarm odour. Elimination/inhibition of the “bad bugs” and application/stimulation of the “good bugs” will be part of the future treatment for axillary body odour.
1 Bacteria and Underarm Odour
Fresh sweat does not smell. Bacteria inhabiting the underarm niche have a huge impact on odour formation. Apocrine secretions in the axillae contain long-chain fatty acids, fatty acids bound to amino acids, sulphur-containing amino acids and hormones, which are too large to become volatile. The bacterial degradation of these compounds leads to smaller compounds, which become volatile and have an odour. Depending on the type of bacteria living in the axillary region, that odour can smell foul. The microbiology of malodourous armpits is currently a topic of investigation. Mainly two genera are abundant in the axillary region: Staphylococcus and Corynebacterium spp.1 Recent research shows that Staphylococcus hominis, Corynebacterium tuberculostearicum and Anaerococcus spp. are important and abundant contributors to typical armpit malodour.2, 3 More corynebacteria correlate with more body odour. Low-abundant species contribute likewise; however, it is still unclear which species and to what extent. As compared to the primate axillary microbiome, the human axillary microbiome is much less diverse, probably due to human hygiene habits. Repeated exposure to water, soaps, detergents and underarm cosmetics decrease the microbial load and diversity to a point where only the most adjusted bacterial genera survive.
2 Bacteria Underneath the Axillary Skin Surface
It is still under debate whether bacteria can live underneath the skin surface, that is the sweat glands, hair follicles, sweat ducts, amongst others. There are nonetheless a number of reasons why living bacteria are present in these deeper skin regions. First, sweat glands and hair follicles are in contact with the outer skin epidermis through invagination, pores and dermal ducts. The sweat glands and hair follicles are large enough, warm and nutritiously rich to permit microbial activity. It is thus plausible that the degradation of the odour precursors starts from there. Second, bacteria were found with molecular techniques in the deeper layers of the stratum corneum of the epidermis. The microbiome of the deeper layers determined the recolonization process after skin barrier disruption.4 Next to this, bacteria were microscopically observed in the duct of eccrine sweat glands in biopsy studies. A recent molecular investigation also detected bacteria in the dermis and even in the dermal adipose tissue of the skin.5
Third, the axillary microbiome is quite stable over time. The armpits are regularly washed, and it would therefore be logic that the armpit microbiome shows much more variation over time. Without a microbiome living in the sweat glands and hair follicles, this would indeed be the case. Fourth, many facultative or obligate anaerobic bacteria are found in the axillary region, proving that these bacteria are present in the deeper skin region where the oxygen level and reduction potential is lower. And fifth, a substantial share of the patients suffering from malodourous armpits indicates that the malodour immediately returns after cleaning the armpit skin or taking a shower (Callewaert, personal observation). Even when all bacteria are removed using antibacterial soaps, an odour can emanate from the armpit skin. Figure 1 represents a section of the axillary skin with the distribution of the bacteria as proposed in this viewpoint. The apocrine glands, hair follicles, sebaceous sweat glands and sweat pores represent an area that is larger than the epidermis and is an underestimated area for bacterial growth and malodour generation.
2.1 Why stress sweat is different
Stress sweat refers to the sweat production when the subject is under emotional stress, which comes with anxiety, fear, stress or pain. For many people, stress sweat smells distinctly different and more unpleasant than normal sweat. No real cause was identified for this. The main reason pointed out in this viewpoint relates to the apocrine sweat glands and the high concentration of bacteria living in there. The apocrine sweat glands, together with the hair follicles, provide a more anaerobic environment, rich in nutrients, fatty acids, amino acids and hormones. For people prone to body odour, these areas are occupied by malodour-causing bacteria. It is the “mother nest of body odour” from where the lipid-rich secretion is degraded into volatile and malodourous compounds. Emotional stress selectively stimulates the apocrine sweat glands. As such, the content of the apocrine sweat gland is secreted via the hair follicle onto the epidermis, along with the already degraded substrates, causing a sudden malodour.
The reason why stress sweat smells more unpleasant goes back to the animal kingdom. The oily secretions of apocrine sweat have emulsifying properties for the skin, hair or fur. They have a water repellent and a surfactant function for eccrine secretions. It is thought that these secretions were important in mammals when hunting or escaping, decreasing friction and preventing slipping when running or climbing.6 Animals that were hunted upon have a selective advantage when they are more slippery and can thus escape faster. The release of a sudden malodour, thus being less attractive for its predator, gives an additional selective advantage for the animal.
2.2 Do underarm cosmetics work?
Deodorants and antiperspirants are widely used to avoid armpit malodours. Deodorants reduce the bacterial counts in the axillae and add perfume to mask the malodour formation. Antiperspirants additionally block the eccrine sweat glands to reduce the moisture production. For the general public, underarm cosmetics do the job of reducing bacterial growth and adding perfume and thus reducing underarm odour. Moreover, staphylococci can regrow the fastest when no more underarm cosmetics are used.7
The use of underarm cosmetics leads to an increased diversity. The overall bacterial density is decreased, which opens up space for new species. Overuse of underarm cosmetics is often a flee reaction of people who suffer from malodourous axillae. It is hypothesized in this viewpoint that over usage of these products leads to a selective colonization of malodour-causing microbiota. These bacteria survive in the sweat glands and around the hair roots and are generally more able to withstand the more anaerobic environment. The consumers of underarm cosmetics often do not know the difference between a deodorant and an antiperspirant. Often, antiperspirants are used to combat malodourous axillae. This might be a wrong reaction, as the aluminium salts only have an effect on the eccrine sweat glands.8 The apocrine sweat glands have sweat ducts and pores which are much broader than those of the eccrine sweat glands and moreover open up to the hair follicle and not to the epidermis. The aluminium salts cannot block the apocrine sweat glands and can thus only minimally influence the malodour production originating from the apocrine glands.
2.3 Armpit microbial management to treat axillary osmidrosis
Today, most of the treatment options focus on sweat reduction. These include the usage of antiperspirants, oral medication, iontophoresis, botulinum toxin injection, sympathectomy, excision of axillary skin, axillary liposuction or laser- and microwave-based ablation of the sweat glands. Other treatments focus on the reduction in the axillary bacterial load. These include the usage of deodorants and antiperspirants and the application of topical antibiotics. When the bacterial growth is minimized, fewer bacterial enzymes are present and fewer apocrine sweat secretions are transformed into volatile compounds. Noteworthy to mention is that the bacterial reduction treatments focus on elimination or reduction of all bacterial species. However, bacteria will recolonize the skin niche, on the epidermis surface, as well as beneath it. It is therefore interesting to understand which factors govern the recolonization of the bacterial species. Preferably, the non-odour-causing microbiota occupy the axillary skin, thus, not releasing axillary malodour and preventing the growth of malodour-causing microbiota. It was recently found that more Staphylococcus epidermidis and Propionibacterium acnes correlated with a better underarm odour.2 With this knowledge, novel solutions can be tested to reverse the malodour formation. In this viewpoint, a bacterial treatment is envisioned, as illustrated in Figure 2.
Probiotics have been proposed to combat body odour. Several patent applications were filed using lactic acid bacteria and bacilli on the (axillary) skin, and some mention a reduced axillary malodour. Also non-pathogenic bacteria, such as extracts of Vitreoscilla filiformis spp., have been applied to the skin and resulted in a curative impact on skin disease states. The use of these bacteria can have a beneficial, yet temporary, effect, as they are unable to thrive on the skin niche. The currently known probiotics are mainly designed for food purposes and will be rapidly outcompeted by much better acquainted skin microbiota. Orally supplied probiotics, on the other hand, can also initiate an immune response and lead towards a beneficial effect on the skin. The topical or oral application of living bacteria (or as lysate) can form a valuable and durable alternative for the existing treatments.
The principle of an armpit bacterial transplantation is currently under investigation. The malodour-causing microbiome is removed and replaced with a healthy non-odourous axillary microbiome. It is the principle of pre-emptive colonization, in which the new microbiota occupy space and nutrition and thus prevent other bacteria from colonizing the skin niche. The autochthonous axillary community is removed using antibacterials and antibiotics. Suitable donors are screened and selected. As bacteria are adjusted to the host (different strains and different physiology), the donor is preferably related to the acceptor, to increase the chances of successful bacterial transmission. A high load of donor bacteria is transferred on the clean axillary skin of the acceptor using a cotton swab. Incubation follows, so the microbiome can occupy the epidermis, sweat glands and hair follicles, without external disturbances. Results so far look promising, at least on a short timescale (1 month), but also on a longer timescale (3 months or permanent).
A step further is the topical application and probiotic use of existing skin bacteria, which were previously cultured ex vivo. In this way, a better knowledge of the bacterial content is gained, excluding pathogenic or malodour-causing species. The danger of transmission of viruses, fungi or pathogens is likewise noticed in faecal microbiota transplantations. Instead of stool transplants, a mixture of stool isolates was also capable of resolving antibiotic-resistant Clostridium difficile infection in the gut.9 The application of isolated and cultured non-odour-causing skin residents can antagonize the autochthonous malodour-causing microbiome in a durable way.
An alternative way is to stimulate and/or selectively steer the non-odour-causing bacteria. This can be complemented with a selective inhibition of the malodour-causing species. The axillary skin microbiome contains a wide diversity of bacteria, where both malodour and non-odour-causing bacteria are present. The addition of supplements to the axillae under the form of biochemicals, prebiotics or plant extracts could be an efficient solution. Several patent applications have been filed in this direction. These compounds can be added to the everyday used underarm cosmetics. A recurrent growth stimulus for the “right” bacteria, together with a recurrent inhibition of the “wrong” bacteria, will positively impact the underarm odour on the long term. If this effect can be achieved not only on the epidermis, but also underneath the skin surface, the odour can be improved from inside out. Much is still subject of investigation, but it seems evident that a special attention needs to be given to the bacteria in resolving axillary body odour. A solution is to be found through management of the underarm microbiome.
Acknowledgements
This work has been supported by the Belgian American Educational Foundation and the Research Foundation - Flanders (FWO) with grant FWO15/PDO/033. CC wrote the article, and JL and TVDW contributed knowledge and reviewed the article.
Conflict of Interests
The authors have declared no conflicting interests.
