What’s that smell? Uncovering the mechanisms and bacteria behind body odor in pre-pubescent children and teenager

Background:

Body odor is a biological process that affects all humans. Many animals have scent glands and body odors that serve different purposes, and humans are no different. It is believed that human body odors might signal familial recognition and communication regarding sexual attraction and reproduction (Hoover, K. 2010). While some human-produced scents may be inoffensive or appealing at best, others are found to be entirely unpleasant (body malodor). These unpleasant aromas are created through interactions between the microbes that live on our skin and substances created by our bodies. Metabolic pathways facilitated by our skin bacteria result in the breakdown of lactic, acetic, and other acids that leave our bodies through sweat, which, by itself, is odorless (Barzantny, H. et al 2011).

Because adults generally experience body malodor at a more extensive level than other age groups (Lam, T. et al 2018), abundant research has been conducted on microbial communities that are at the base of the broader metabolic mechanisms producing bad odor in adults. The armpit (axilla) is universally recognized as one of the worst offenders for odor, so a large proportion of this research is focused towards axillary microbiomes (communities of microorganisms living together in a particular area of the body). Skin bacteria’s role in fatty acid metabolism (James, A.G. et al 2004) and the bacterial species Corynebacterium, Staphylococcus, and Cutibacterium (Callewaert, C. et al 2013, Barzantny, H. et al 2011, Li, M. et al 2019) have been the most widely indicated factors in malodor, but Anaerococcus and Peptoniphilus species have also been found to be key components of the axillary microbiome and general acid metabolism as well (James, A.G. 2020). However, there have been very few, if any, studies done on microbial communities behind body malodor in children and teenagers. Having not yet fully gone through puberty, children have different skin physiology than adults; their sebaceous and apocrine glands (which secrete oil and sweat, respectively) have not completely matured (Lam, T. et al 2018). This means children’s sweat has a different composition than the sweat of adults, which may cause different bacterial interactions and metabolic pathways to occur on their skin, causing body odor.

Compared to adults, not much is known about the differences in children and teenagers’ microbial communities and mechanisms of body odor production. A group of researchers in South Asia decided to conduct a study on children and teenagers in the Philippines to put together some baseline research on the microbiomes of children. More specifically, the microbiomes of the underarm, head, and neck regions, which are the main sources of malodor in children. 

Central Research Question:

What are the key bacterial taxa and malodor-associated pathways behind body malodor production in children and teens, and are there significant differences between pre-pubescent children and teenagers?

Results and Evidence:

For sample collections, researchers used 2 groups, a children’s group and a teenager’s group. Both groups took a shower or bath using a standard bar of soap with no perfumes or antimicrobial ingredients, and had samples and scent determinations taken one hour after bath. After the hour mark, children and teens exercised for approximately five hours to generate sweat and then had samples and scent determinations taken at the 8 hour mark. Scent determinations were made by a professional perfumer (an individual who undergoes intensive scent training, usually working in the perfume industry) to categorize aromas: sulfurous, sour, greasy, etc.

Figure 1: Sampling protocol schematic from Lam et al. study 2018.

Microbiome samples were taken by tape stripping, in which strips of tape are applied to an area of skin (Lam, T. et al 2018),  from the scalp, back of neck, and axilla from each child both one hour after their bath and after 5 hours of physical activity, at the 8-hour mark. Sweat samples were also collected during exercise. After samples were taken, the tape strips and sweat samples were processed, and DNA was extracted and sequenced in a lab to determine what types of bacteria and chemical compounds were present. Researchers found that the main three culprits behind body odor in children and teens were bacterial species from the genera Staphylococcus, Malassezia, and Cutibacterium. For teenagers, a main player in underarm odor was the genus Corynebacterium, which was found in significantly higher numbers than in pre-pubescent children (Corynebacterium is one of the main three genera behind adult body odor (Callewaert, C. et al 2013)). One genus, Acinetobacter, might be associated with malodor resistance; pre-pubescent children that had lower levels of body odor seemed to have higher levels of Acinetobacter species. The key malodor-associated pathways that researchers found for children and teenagers were the metabolism of isovaleric and acetic acids. These acids are produced in the sweat during exercise, and are broken down by bacteria (Staphylococcus, Malassezia, and Cutibacterium) into components that are associated with bad odor. 

My questions:

Question 1: 

Why didn’t the researchers in this study differentiate the groups by male and female? It makes sense to leave the pre-pubescent children (ages 5-9) in one category, but I would postulate that there are already several key physiological differences between male and female teenagers (ages 15-18) that are making a difference in microbiome composition and gland maturity. Sebaceous and apocrine glands are high contributors to sweat, and are associated with hair follicles. Since males often have more body hair than females, and as adults produce more sweat than females (Kaciuba-Uscilko, H. et al 2001). There are probably differences in the axillary microbiome; not necessarily in species but in species abundance,which could affect the metabolism of fatty acids produced by sweat.. Also, if more sweat is being produced, then there are more acids for bacteria to metabolize, causing more malodor. It makes sense if researchers were just trying to get a baseline knowledge on the differences between fully developed mature adults compared to teenagers, but nonetheless I think it would make for an interesting study. 

Question 2: 

How do deodorants and antiperspirants play a role in the microbial community in the armpit? It is known that antiperspirants cause a decrease in colonies of culturable bacteria (Urban, J. et al 2016), but what are the effects of this? Are there negative repercussions from having a lower diversity of microorganisms in the axillary microbiome, or is there no impact on bacterial abundance/diversity?

Further readings and videos:

  • This Ted Talk gives a really good breakdown of body odor and the armpit microbiome! It dives a little deeper into the science of body odor.
  • Here’s another good video (this one’s a little shorter) by Popular Science, that gives a more basic breakdown of B.O.
  • This article is short and sweet, and has some really cool pictures of bacteria cultures taken from human armpits.
  • Here is the link to the paper this blog post was written about. 

    References:

  • Barzantny, Helena, I. Brune, A. Tauch. “Molecular basis of human body odour formation: insights deduced from corynebacterial genome sequences”International Journal of Cosmetic Science Vol 34 Issue 1: pg. 2-11 (2012).
  • Callewaert C, Kerckhof F-M, Granitsiotis MS, Van Gele M, Van de Wiele T, Boon N. “Characterization of Staphylococcus and Corynebacterium Clusters in the Human Axillary Region.” PLoS ONE 8(8): e70538 (2013).
  • Hoover, Kara C. “Smell with inspiration: The evolutionary significance of olfaction.” American Journal of Physical Anthropology Vol 143 Issue S51: pg 63-74 (2010). 
  • James, Alexander Gordon. “The Axillary Microbiome and its Relationship with Underarm Odor.” Skin Microbiome Handbook: From Basic Research to Product Development: Chapter 5 (2020).
  • James, A., Casey, J., Hyliands, D. et al. “Fatty acid metabolism by cutaneous bacteria and its role in axillary malodour.” World Journal of Microbiology and Biotechnology 20, 787–793 (2004).
  • Kaciuba-Uscilko, H., R. Grucza. “Gender differences in thermoregulation.” Current Opinion in Clinical Nutrition and Metabolic Care Vol 4 Issue 6: pg 533-536 (2001). 
  • Lam, T.H., Verzotto, D., Brahma, P. et al. “Understanding the microbial basis of body odor in pre-pubescent children and teenagers.” Microbiome Vol 6, Issue 213 (2018). 
  • Li, M., Budding, A., van der Lugt‐Degen, M. et al. “The influence of age, gender and race/ethnicity on the composition of the human axillary microbiome.” International Journal of Cosmetic Science Vol 41, Issue 4: pg 371-377 (2019).
  • Urban, J., D. Fergus, A. Savage, M. Ehlers et al. “The effect of habitual and experimental antiperspirant and deodorant use on the armpit microbiome.” PeerJ. (2016).