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Mycobiome and Microbiome in Seborrheic Dermatitis

Dong Heon Lee ,Hye Jung Jung
10.17966/JMI.2022.27.1.9 Epub 2022 March 31

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Abstract

Seborrheic dermatitis (SD) is a chronic inflammatory skin disease in which scaling and erythema occur on various body parts, such as the scalp, eyebrows, nasolabial folds, and ears. Although it is a common skin disease, its pathogenesis remains unclear. It has various causes, including microorganisms and immune and nervous system abnormalities that act in a complex manner. The skin mycobiome/microbiome, an important factor in SD occurrence, is being actively studied. Among the skin microorganisms related to SD, Malassezia and Cutibacterium have been extensively studied. Recently, it was revealed that various microorganisms are related in several ways. The study of changes in mycobiome/microbiome involves comparing types and abundances of microorganisms and degrees of microbial diversity; patients and healthy individuals; the lesion and nonlesion areas; and affected body parts. Several studies on the mycobiome/microbiome associated with SD have shown relatively consistent results; however, some have revealed different outcomes. These variations occur because of differences in individuals, study groups, and sampling/study methodology. Therefore, further research is needed for the application the results of these studies in the treatment of SD.



Keywords



Microbiome Mycobiome Seborrheic dermatitis



INTRODUCTION

Seborrheic dermatitis (SD) is a chronic inflammatory skin disease that causes flakes and erythema on the scalp, eyebrows, nasolabial folds, glabella, and ears. Although it is a common skin disease, its cause is still unclear1. Previous studies have reported on the associations between immune response and inflammation, microorganisms, abnormal skin lipids, epidermal hyperkeratosis, and neurotransmitter abnormalities. Climate, medications, malnutrition, and genetic factors may also cause SD1.

SD pathogenesis due to Malassezia, a fungi, and Cuti- bacterium, a bacteria, have been well studied. Several studies have reported that Malassezia furfur weakens the skin barrier function by producing indoles, which are ligands for aryl hydrocarbon receptors, or using oleic and arachidonic acids generated as sebum metabolites2. Cutibacterium acnes and Malassezia have lipolytic ability, converting triglycerides into free fatty acids3. Recently, with the development of the micro- biome concept in all fields of dermatology, SD research has expanded to investigate the involvement of mycobiome/ microbiome.

SEBORRHEIC DERMATITIS MYCOBIOME

Several studies have confirmed the α- and β-mycobiome diversity in patients with SD. The patient's Shannon index of α diversity has been reported to decrease as well as increase4,5. Several reports have stated that no difference exists between the lesion and nonlesion areas and according to the body parts4,6. Another study reported a decrease in the Chao and Simpson indexes7.

Regarding β diversity, study results indicating that it is possible to distinguish between the patient and healthy individual as well as those indicating that they cannot be distinguished exist. Further, results regarding the lesion and nonlesion areas are heterogenous4,7-10. A previous report stated the absence of any difference in diversity according to disease severity10 (Table 1).

 

Subject

 

Mycobiome

Microbiome

Lin et al.
(2020)4

Scalp

SD/healthy

Lesional/
non-lesional

α

Decreased Shannon diversity in SD

No significant changes in
lesional/non-lesional

No significant changes between SD/healthy

No significant changes in lesional/
non-lesional

β

PCoA could distinguish SD/healthy

No significant changes in
lesional/non-lesional

PCoA could distinguish SD/healthy

No significant changes in lesional/
non-lesional

Grimshaw
et al. (2019)
9

Scalp

SD/healthy

Lesional/
non-lesional

α

N/A

N/A

β

NMDS plots showed no distinct community clustering between SD/heathy

NMDS plots showed distinct community
clustering between lesional/non-lesional

Saxena et al.
(2018)5

Scalp

SD/healthy

α

Significantly higher Shannon
diversity in SD

No significant changes between
SD/healthy

β

N/A

UniFrac distances showed significant difference between SD/healthy

Park et al.
(2017)11

Scalp

SD/healthy

α

Significantly lower richness (Chao1)
and lower evenness (Simpson's
index) in SD

Significantly higher richness (Chao1) and lower evenness (Simpson's index) in SD

β

PCoA and MDS plots showed
distinct community clustering
between SD/healthy

PCoA and MDS plots showed distinct community clustering between
SD/healthy

Soares et al.
(2016)8

Scalp, Forehead

SD/healthy

Lesional/
non-lesional

α

Significantly increased Shannon diversity in SD

Significantly increased Shannon diversity in SD scalps and forehead compared to
healthy controls

β

ANOSIM and NMDS plots showed distinct community clustering

Scalp/Forehead

lesional/non-lesional in SD

ANOSIM and NMDS plots showed distinct community clustering according to
body sites and between lesional
and non-lesional

Tanaka et al.

(2016)15

Scalp

Lesional/
non-lesional

α

N/A

No significant changes between lesional/non-lesional

β

N/A

PCoA showed clear separation between

lesional/non-lesional

Abbreviations: ANOSIM, analysis of similarities; MDS, metric multidimensional scaling; N/A, not available; NMDS, non-metric multidimensional scaling; PCoA, principal coordinates analysis; SD, seborrheic dermatitis

Table 1. α and β diversity in seborrheic dermatitis

Among the fungi constituting the mycobiome, the most well-known is Malassezia. Additionally, it has been reported that fungi, such as Mycosphaerella, Candida, Filobasidium, Aspergillus, Ganoderma, Exidia, Pilatoporus, and Engyodontium, vary in SD. Currently, heterogeneous results indicate the increase or decrease of each species, but the increase in Malassezia, especially M. restricta, and the decrease in M. golbossa, reveal similar results4-14.

SEBORRHEIC DERMATITIS MICROBIOME

The α-diversity of the SD microbiome showed inconsistent results. Thus, among the outcomes obtained, the relatively consistent one states that no difference between the lesion and nonlesion areas exist7-9. Regarding the β-diversity, the main opinion is that the sample distance is higher in healthy individuals4,5,7-9,15 (Table 1). The members of the microbiome include Staphylococcus, Cutibacterium, Streptococcus, Pseudomonas, Actinobacteria, and Firmicutes. It is considered that Staphylococcus and Streptococcus increase while Cutibacterium and Pseudomonas decrease4-9,12,13,15.

CAUSES OF DISCREPANCIES BETWEEN STUDY RESULTS

Differences between study results arise due to differences between individuals. Moreover, factors such as residence and race of the population, sampling method, and sequencing techniques differ among studies. Sequencing results also vary depending on the target gene, and there are various methods for sequencing, such as cloning and Sanger sequencing, quantitative polymerase chain reaction, amplicon sequencing, and whole metagenome sequencing; however, currently no standardized sampling or experimental method exists. Therefore, the results are bound to be affected2.

THE RELATIONSHIP BETWEEN MYCOBIOME/MICROBIOME AND SEBORRHEIC DERMATITIS SYMPTOMS

For clinically meaningful microbiome changes, it should be confirmed that changes are significantly related to clinical symptoms. However, research is limited on this topic. According to a study by Saxena et al.5, M. globosa, known to decrease mainly in SD, showed a negative correlation with total dandruff and itching and a positive correlation with total Malassezia. Also, a decrease in Pseudomonas and an increase in Staphylococcus were positively correlated with dandruff and itch5. A positive correlation of Staphylococcus and Cutibacterium with TEWL and water content indicates their potential role in skin barrier function12. Moreover, researchers have analyzed the functional pathways of the mycobiome/microbiome. The mycobiome are enriched in pathways involved in cell-host adhesion in the dandruff. Contrastingly, the microbiome was enriched in pathways related to the synthesis and metabolism of amino acids, biotin, and other B-vitamins, which have been reported to be essential for hair growth5.

THE RELATIONSHIP BETWEEN MYCOBIOME/MICROBIOME AND SD TREATMENT

For the application of microbiome research in actual clinical practice, it is necessary to check whether dysbiosis improves after treatment and whether this improvement leads to symptom progression, besides examining the relationship between microorganisms and clinical symptoms. However, there is limited research on this field. Leong et al.16 confirmed the changes in M. restricta and M. globosa in 35 healthy sub- jects before and after using antifungal zinc pyrithione shampoo. On the one hand, M. restricta temporarily decreased after shampooing, but the variation among individuals was large. However, it soon returned to the original state, thus failing to maintain a meaningful change. On the other hand, M. globosa was unaffected by the use of zinc pyrithione sham- poo16. The following results confirmed the changes in patients with SD using selenium-disulfide shampoo. The participants used 2% ketoconazole shampoo for 1 month. The outcomes showed beneficial results, such as the reduction of dandruff and erythema, restoration of Malassezia diversity, reduction of total Malassezia count, and reduction of Staphylococcus. The participants were classified into two groups. The first group maintained treatment using 1% SeS2-based shampoo, and the other group used a vehicle. It was confirmed that the significant response after using ketoconazole shampoo was well maintained in the group using the selenium shampoo17.

Rather than regulating existing microbes, some treatments involve supplementation with beneficial microorganisms. Hence, strains known to be helpful against atopic dermatitis in patients with SD can be used, as patients with SD also suffer from barrier damage and skin immune abnormalities, such as atopic dermatitis18. Vitreoscilla filiformis is a gram-negative bacterium that stimulates regulatory T cells and does not affect the survival of microorganisms constituting the microbiome19. It has been reported that when applied to patients with atopic dermatitis, it helps to moisturize the skin20. Therefore, when vitreoscilla biomass was applied to SD patients, symptom improvement, such as itching, was observed21. The application of the Lactobacillus biomass (Lactobacillus sporogene or Lactobacillus rhamnosus) also appeared to be beneficial in the improvement of both psor- iasis and SD22,23. Furthermore, another study investigated the reaction after oral ingestion rather than microbial application. SD symptoms, such as dandruff, improved when Lactobacillus paracasei NCC 2461 ST11 was taken once daily24.

CONCLUSION

In conclusion, SD mycobiome/microbiome diversity can be considered controversial, and presently, this research has relatively decreased. It is possible that the difference between the lesion and nonlesion areas is not significant, and there is a change in species and quantity. Malassezia (esp., restricta), Staphylococcus, and Streptococcus increased in abundance, whereas M. globosa, Cutibacterium, and Pseudomonas de- creased. There are possible correlations between SD symptoms and changes in the microbiome and its metabolic pathways.



References


1. 1. Wikramanayake TC, Borda LJ, Miteva M, Paus R. Seb- orrheic dermatitis-Looking beyond Malassezia. Exp Dermatol 2019;28:991-1001
Google Scholar 

2. 2. Tao R, Li R, Wang R. Skin microbiome alterations in seborrheic dermatitis and dandruff: A systematic review. Exp Dermatol 2021;30:1546-1553
Google Scholar 

3. 3. Adalsteinsson JA, Kaushik S, Muzumdar S, Guttman-Yassky E, Ungar J. An update on the microbiology, immunology and genetics of seborrheic dermatitis. Exp Dermatol 2020;29:481-489


4. 4. Lin Q, Panchamukhi A, Li P, Shan W, Zhou H, Hou L, et al. Malassezia and Staphylococcus dominate scalp micro- biome for seborrheic dermatitis. Bioprocess Biosyst Eng 2021;44:965-975
Google Scholar 

5. 5. Saxena R, Mittal P, Clavaud C, Dhakan DB, Hegde P, Veeranagaiah MM, et al. Comparison of healthy and dandruff scalp microbiome reveals the role of com- mensals in scalp health. Front Cell Infect Microbiol 2018; 8:346


6. 6. Clavaud C, Jourdain R, Bar-Hen A, Tichit M, Bouchier C, Pouradier F, et al. Dandruff is associated with disequi- librium in the proportion of the major bacterial and fungal populations colonizing the scalp. PLoS One 2013;8: e58203
Google Scholar 

7. 7. Park T, Kim HJ, Myeong NR, Lee HG, Kwack I, Lee J, et al. Collapse of human scalp microbiome network in dandruff and seborrhoeic dermatitis. Exp Dermatol 2017; 26:835-838
Google Scholar 

8. 8. Soares RC, Camargo-Penna PH, de Moraes VC, De Vecchi R, Clavaud C, Breton L, et al. Dysbiotic bacterial and fungal communities not restricted to clinically affected skin sites in dandruff. Front Cell Infect Microbiol 2016;6:157
Google Scholar 

9. 9. Grimshaw SG, Smith AM, Arnold DS, Xu E, Hoptroff M, Murphy B. The diversity and abundance of fungi and bacteria on the healthy and dandruff affected human scalp. PLoS One 2019;14:e0225796
Google Scholar 

10. 10. Soares RC, Zani MB, Arruda AC, de Arruda LH, Paulino LC. Malassezia intra-specific diversity and potentially new species in the skin microbiota from Brazilian healthy sub- jects and seborrheic dermatitis patients. PLoS One 2015; 10:e0117921
Google Scholar 

11. 11. Park HK, Ha MH, Park SG, Kim MN, Kim BJ, Kim W. Characterization of the fungal microbiota (mycobiome) in healthy and dandruff-afflicted human scalps. PLoS One 2012;7:e32847
Google Scholar 

12. 12. Wang L, Clavaud C, Bar-Hen A, Cui M, Gao J, Liu Y, et al. Characterization of the major bacterial-fungal populations colonizing dandruff scalps in Shanghai, China, shows microbial disequilibrium. Exp Dermatol 2015;24:398-400
Google Scholar 

13. 13. Xu Z, Wang Z, Yuan C, Liu X, Yang F, Wang T, et al. Dandruff is associated with the conjoined interactions between host and microorganisms. Sci Rep 2016;6:24877
Google Scholar 

14. 14. Tajima M, Sugita T, Nishikawa A, Tsuboi R. Molecular analysis of Malassezia microflora in seborrheic dermatitis patients: comparison with other diseases and healthy subjects. J Invest Dermatol 2008;128:345-351
Google Scholar 

15. 15. Tanaka A, Cho O, Saito C, Saito M, Tsuboi R, Sugita T. Comprehensive pyrosequencing analysis of the bacterial microbiota of the skin of patients with seborrheic der- matitis. Microbiol Immunol 2016;60:521-526
Google Scholar 

16. 16. Leong C, Wang J, Toi MJ, Lam YI, Goh JP, Lee SM, et al. Effect of zinc pyrithione shampoo treatment on skin commensal Malassezia. Med Mycol 2021;59:210-213
Google Scholar 

17. 17. Massiot P, Clavaud C, Thomas M, Ott A, Guéniche A, Panhard S, et al. Continuous clinical improvement of mild-to-moderate seborrheic dermatitis and rebalancing of the scalp microbiome using a selenium disulfide-based shampoo after an initial treatment with ketoconazole. J Cosmet Dermatol 2021;doi:10.1111/jocd.14362
Google Scholar 

18. 18. Mottin VHM, Suyenaga ES. An approach on the potential use of probiotics in the treatment of skin conditions: acne and atopic dermatitis. Int J Dermatol 2018;57:1425-1432
Google Scholar 

19. 19. Benyacoub J, Bosco N, Blanchard C, Demont A, Philippe D, Castiel-Higounenc I, et al. Immune modulation pro- perty of Lactobacillus paracasei NCC2461 (ST11) strain and impact on skin defences. Benef Microbes 2014;5: 129-136
Google Scholar 

20. 20. Guéniche A, Dahel K, Bastien P, Martin R, Nicolas JF, Breton L. Vitreoscilla filiformis bacterial extract to improve the efficacy of emollient used in atopic dermatitis symp- toms. J Eur Acad Dermatol Venereol 2008;22:746-747
Google Scholar 

21. 21. Guéniche A, Cathelineau AC, Bastien P, Esdaile J, Martin R, Queille Roussel C, et al. Vitreoscilla filiformis biomass improves seborrheic dermatitis. J Eur Acad Dermatol Venereol 2008;22:1014-1015


22. 22. Vijayashankar M, Raghunath N. Pustular psoriasis re- sponding to probiotics-a new insight. Our Dermatol 2012; 3:326-329
Google Scholar 

23. 23. Navarro-López V, Martínez-Andrés A, Ramírez-Boscá A, Ruzafa-Costas B, Núñez-Delegido E, Carrión-Gutiérrez MA, et al. Efficacy and safety of oral administration of a mixture of probiotic strains in patients with psoriasis: A randomized controlled clinical trial. Acta Derm Venereol 2019;99:1078-1084


24. 24. Reygagne P, Bastien P, Couavoux MP, Philippe D, Renouf M, Castiel-Higounenc I, et al. The positive benefit of Lactobacillus paracasei NCC2461 ST11 in healthy volun- teers with moderate to severe dandruff. Benef Microbes 2017;8:671-680
Google Scholar 

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