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. 2018 Jul 19;84(10):2178–2193. doi: 10.1111/bcp.13662

Table 1.

Summary table of the studies included in the review

Source First author, year [ref] Disease Study design No. of patients Sample collection methods Analysis Key findings Weaknesses Level evidence
Paulino et al . 2006 18 PV Case control
3 PV/5 HV
Sterile swabs
Lesional and nonlesional skin
Multiple sampling in one PV and 2 HV
18S rRNA 5.8S rDNA ▪ Malassezia mycobiota substantially different PV vs. HV Small cohort Low
Amaya et al . 2007 19 PV Case control
22 PV/36 AD/30 HV
OpSite® transparent adhesive dressings
Lesional and nonlesional skin
5.8S rDNA ▪ Malassezia species detected in overall sites higher in PV and AD compared to HV Small cohort
PV patients on treatment
Limited analysis
Different skin site collection PV vs. AD and HV
Low
Paulino et al . 2008 20 PV Case control
1 PV/1 HV
Sterile swabs
Lesional and nonlesional skin
Multiple time points
5.8S rDNA Mycobiota relatively stable over time.
No significant dichotomy between PV and HV.
Small cohort
Limited analysis
Low
Gao et al . 2008 21 PV Case control
6 PV/6 HV
Sterile swabs
Lesional and nonlesional skin
16S rRNA V1‐V9 Firmucutes more abundant in lesional skin PV vs. nonlesional skin and HV.
Actinobacteria less abundant in lesional skin PV vs. nonlesional skin and HV.
Small cohort
No serial sampling
Low
Fahlen et al . 2011 22 PV Case control
10 PV/12 HV
2‐mm skin punch biopsies 16S rRNA V3‐V4 Most common phyla in PV and HV: Firmicutis, Proteobacteria, Actinobacteria.
Staphylococci and Propionibacteria were less common in psoriatic lesions
Small cohort
No serial sampling
Variation in skin sample sites
Low
Alekseyenko et al . 2013 23 PV Case control & Prospective longitudinal cohort study
CC: 54 PV/37 HV
PC: 17 PV/15 HV
Sterile swabs
Lesional and nonlesional skin
HV matched sites
Multiple sampling
16S rRNA V1‐V3 Most common phyla in PV and HV: Firmicutis, Proteobacteria, Actinobacteria.
Combined relative abundance of Corynebacterium, Streptococcus and Staphylococcus was increased in psoriatic skin, compared to unaffected skin and healthy control skin
Some patients on active treatment
Mainly severe patients
Low to moderate
Statnikov et al . 2013 24 PV Case control
54 PV/37 HV
Sterile swabs
Lesional and nonlesional skin
HV matched sites
16S rRNA V1‐V3 and V3‐V5 Microbiome signatures could be used to diagnose psoriasis No serial sampling Low to moderate
Takemoto et al . 2015 25 PV Case control
12 PV/12 HV
PV: psoriatic scales by tweezer
HV: OpSite® transparent adhesive dressings
26S rRNA D1 – D2 Psoriatic lesions exhibited significantly greater diversity compared to HV
▪ Malassezia restricta levels were significantly higher in psoriatic lesions, compared to healthy controls
Small cohort
No serial sampling
Only male patients
Different sample method PV and HV
Low
Salava et al . 2017 26 PV Case control
13 PV
Sterile swabs
Lesional and nonlesional skin
16S rRNA V1‐V3 No significant differences microbial diversity between lesional and nonlesional skin Small cohort
No serial sampling
Variation in skin sample sites
Low
Tett et al . 2017 27 PV Case control
28 PV
Sterile swabs
Lesional and nonlesional skin
WMS sequencing Plaques at the ear had a significant decrease in microbial diversity, and increase in Staphylococcus abundance
At species level, no differences between lesional and nonlesional skin were observed
Small cohort
No serial sampling
Some patients on active treatment
Low
Ring et al . 2017 28 HS Case control
30 HS
24 HV
Biopsies
Lesional and nonlesional skin
16S rRNA V3‐V4
18S rDNA V3‐V4
Microbiome in HS significantly different from HV in lesional and nonlesional skin
Five microbiome types identified
Lesional skin consisted predominantly of Corynebacterium species (type I) and Peptoniphilus species (type IV)
▪ Propionibacterium showed a significant higher abundance in HV
Small cohort
No serial sampling
Low
Guet‐Revillet et al . 2017 29 HS Prospective cohort
65 HS
Sterile swabs
Lesional and nonlesional skin
16S rRNA
V1‐V2
Lesional skin consisted predominantly of anaerobes (Porphyromonas and Prevotella species)
Clinical severity significantly associated with variations in lesional microbiota
Fusobacterium associated with severe HS
Small cohort Low
Dowd et al . 2008 30 UC Prospective cohort
10 VLU/10 DFU/
10 PU
Debridement samples 16S rRNA V4 Major populations include of all wound include: Staphylococcus, Pseudomonas, Peptoniphilus, Enterobacter, Strenotrophomonas, Finegoldia and Serratia species
Each wound type different profile, dependent on oxygen tolerance of the bacterial population
Small study
No serial sampling
Low
Price et al . 2009 31 UC Prospective cohort
7 DFU/7 NU/3 VLU/3 PSU/4 OTH
Wound base curette
Multiple time points
16S rRNA V3 Fastidious anaerobic bacteria of the Clostridiales family XI were the most prevalent bacteria in wounds
Wound microbiota from antibiotic treated patients were significantly different from untreated patients
In diabetic patients, Streptococcus was more abundant
Small study
Sampling time point variable
Patients on wide variety of treatments
Low
Price et al . 2011 32 UC Cross‐sectional
4 DFU/3 NU/3 VLU/2 OTH
Wound base curette
Multiple samples taken
16S rRNA V3‐V4 The 10 most common genera included Staphylococcus, Pseudomonas, Streptococcus, Anaerococcus, Ralstonia, Morganella, Porphyromonas, Peptoniphilus, Janthinobacterium and Corynebacterium
Samples from different sites within individual wounds shared similarities in bacterial community compositions
Samples taken from different wounds were less similar than those taken from different sites within the same wound
Small cohort
Patients on active treatment
No serial sampling
Low
Rhoads et al . 2012 33 UC Cross‐sectional
4 DFU/3 NU/3 VLU/2 OTH
Wound base curette 16S rRNA V1‐V3 The ten most common genera included Staphylococcus, Pseudomonas, Streptococcus, Anaerococcus, Ralstonia, Morganella, Porphyromonas, Peptoniphilus, Janthinobacterium and Corynebacterium
Samples from different sites within individual wounds shared similarities in bacterial community compositions
Samples taken from different wounds were less similar than those taken from different sites within the same wound
Small cohort
Patients on active treatment
No serial sampling
Low
Gjodsbol et al . 2012 34 UC Comparative
46
VLU
Filter paper pad & punch biopsies 16S rRNA V1‐V3 ▪ Staphylococcus aureus most found species
Multiple sampling over time lead to identification of additional species
No difference in outcomes different sample techniques
No controls Low
Gardner et al . 2013 35 UC Cross‐sectional
52
DFU
Sterile swabs 16S rRNA V1‐V3 The most abundant OTU was Staphylococcus, with S. aureus the most common species
Ulcer closing was positively correlated with number of species level OTUs, higher microbial diversity, relative abundance of Proteobacteria, and negatively correlated with relative abundance of Staphylococcus
Ulcer depth was negatively associated with Staphylococcus abundance and positively associated with anaerobic bacteria relative abundance
No serial sampling
No controls
Low
Wolcott et al . 2016 37 UC Cohort
2963
910 DFU/916 VLU/676 DU/370 PSU
Sharp debridement at surface wound bed 16S rRNA V1‐V3 Neither patient demographics (age, gender, race, diabetes status) nor wound type influenced the bacterial composition of the chronic wound microbiome
▪ Staphylococcus and Pseudomonas comprise the most prevalent genera present in the microbiota of chronic wounds, with S. aureus and S. epidermidis the most predominant species
Chronic wounds are frequently colonized by communalistic and anaerobic bacteria, including coagulation‐negative Staphylococcus, Corynebacterium, and Propionibacterium species
Unclear whether patients were on treatment Low to moderate
Smith et al . 2016 36 UC Cohort
20 DFU
Sterile swabs 16S rRNA V4 The most commonly detected bacteria in all ulcers were Peptoniphilus, Anaerococcus and Corynebacterium species
In new ulcers, the most commonly detected bacteria were the above and Staphylococcus species
The majority of OTUs residing in both new and recurrent ulcers (>67%) were mostly Gram‐positive cocci (Staphylococcus, Streptococcus, Anaerococcus, Peptoniphilus and Finegoldia
Lower HbA1c values and shorter duration of diabetes correlated with higher diversity within the ulcer
Small cohort
No serial sampling
No controls
Low
Kalan et al . 2016 38 UC Prospective longitudinal cohort
100 DFU
Sterile swabs
Multiple time point sampling
ITS1 rRNA Fungal microbiome was highly heterogeneous over time and between subjects
Fungal diversity increased with antibiotic administration
The proportion of the phylum Ascomycota were significantly greater at the beginning of the study in wounds that took >8 weeks to heal
No controls
Most patients on active treatment
Low to moderate
Loesche et al . 2017 39 UC Prospective longitudinal cohort
100 DFU
Sterile swabs
Multiple time point sampling
16S rRNA V1‐V3 The most abundant genus identified was Staphylococcus, followed by Streptococcus, Corynebacterium and Anaerococcus
The major OTU attributed to Staphylococcus was S. aureus
Ulcer microbiota was highly dynamic, with community type transitions occurring approximately every 3.52 weeks
Microbiota community instability was associated with faster healing and improved outcomes
Exposure to systemic antibiotics destabilize wound microbiota, rather than altering overall diversity or relative abundance of specific taxa
No controls
Most patients on active treatment
Low to moderate
Kuk Park et al . 2012 40 SD/PC Case control
4 PC
3 HV
Sterile swabs 26S rRNA D1‐D2 ▪ P. meleagrinum and P. chrusogenum detected on dandruff scalp
▪ Malassezia spp. 2 times more abundant on dandruff scalp
Small cohort
No serial sampling
Low
Clavaud et al . 2013. 41 SD/PC Case–control
29 PC
20 HV
Sterile swabs
In 20 PC patients lesional and nonlesional sampling
16S
28S‐ITS
▪ M. restricta major fungal species on scalp PC and HV
▪ M. restricta and s. epidermidis significantly more abundant on PC scalp
▪ Propionibacterium acnes significantly less abundant on PC scalp
▪ M. restricta/P. acnes ratio significantly higher in PC scalp
Small cohort
No serial sampling
Low
Soares et al . 2015 42 SD/PC Case control
9 SD (5 mild, 4 severe)
5 HV
Sterile swabs
Scalp, forehead chin, shoulder and interface samples
5.8S/ITS2 rDNA In general, no association between Malassezia mycobiota and SD was found
Higher m. globosa abundance was found in nonscalp lesions of severe SD patients
Small cohort
No serial sampling
Low
Park et al . 2017 43 SD/PC Case control
29 SD
28 PC
45 HV
Sterile swabs
Scalp samples
16 s rRNA V4‐V5
ITS1 rDNA
Higher abundance of Staphylococcus sp. and m. restricta, and lower abundance of Propionibacterium associated with scalp disease No serial sampling Low
Bek‐Thomsen et al . 2008 44 AV Case control
5 AV/3 HV
Cyanoacrylate biopsy
AV acne lesion face
HV nose area
16S rRNA V1‐V9 Acne skin higher diversity, P. acnes and S. epidermidis most common species Small cohort
Only moderate to severe patients
No serial sampling
No nonlesional patient sampling
Low
Fitz‐Gibbon et al . 2013 45 AV Case control
49 AV/52 HV
Bioré® Deep Cleansing Pore strips
Nose area
16S rRNA V1‐V9 No difference relative abundance P. acnes AV in HV.
Association specific P. acnes strain and acne.
Some patients on active treatment
No serial sampling
No nonlesional patient sampling
Low
Barnard et al . 2016 46 AV Case control
38 AV/34 HV
Bioré® Deep Cleansing Pore strips
Nose area
WMS sequencing Association specific P. acnes strain and acne. Some patients on active treatment
No serial sampling
No nonlesional patient sampling
Low
Dreno et al . 2017 47 AV Single‐center, randomized‐controlled, double‐blind
Erythromycin 4%
OR
Dermatocosmetic
26 AV
Sterile swabs
Lesional and nonlesional skin
Multiple time points
16S rRNA V4 Different microbiota profiles on different sites.
Erythromycin treatment reduced the number of Actinobacteria, and dermocosmetic reduced Actinobacteria and Staphylococcus spp.
Small cohort
Multiple samples excluded due to insufficient bacterial material
Moderate
Kelhala et al . 2017 48 AV Single‐centre, controlled study
isotretinoin 0.4–0.6 mg kg–1
or
lymecycline 300 mg twice daily
17 isotretinoin
11 lymecycline
16 HV
Sterile swabs
Predose and after 6 weeks
Cheek, back and armpit
16S rRNA V1‐V3 Positive correlation Propionibacterium abundance and acne severity grade
Both treatments reduced clinical acne grades
▪ Propionibacterium decreased in cheek samples after both treatments
▪ Propionibacterium decreased in back samples after lymecycline, but not isotretinoin treatment
Diversity increased after treatment
Small cohort
No nonlesional patient sampling
Moderate
Sugita et al . 2004 58 AD Case control
13 AD/12 HV
OpSite® transparent adhesive dressings
Lesional skin
HV matched sites
26S and 5S rRNA intergenic spacer region 1 ▪ M. restricta colonizes both AD and HV Small cohort
No serial sampling
Limited analysis
Patients on active treatment
Low
Dekio et al . 2007 49 AD Case control
13 AD/10 HV
Sterile swabs
Forehead skin
16S rRNA In both AD and HV there was a high rate of Streptococcus species
In AD Strenotrophomonas maltophilia was significantly more common
Small cohort
No serial sampling
Patients on active treatment
Low
Kaga et al. 2009 50 AD Case control
56 AD/32 HV
OpSite® transparent adhesive dressings
Lesional skin AD
Face HV
26S and 5S rRNA intergenic spacer region 1 In mild and moderate AD, M. restricta was predominant over M. globose
In patients with severe AD, proportions of M. restricta and M. globose were almost identical
Limited analysis
No serial sampling
Variation in skin sample sites
Patients possibly on active treatment
Low to moderate
Yim et al . 2010 51 AD Prospective cohort
60
Sterile swabs
5 body sites
26S There were no significant differences between positive Malassezia culture, Malassezia species, and severity of AD Limited analysis
Patients on emollient treatment
Low to moderate
Akaza et al . 2010 52 AD Case control
67
Sterile swabs
Lesional and nonlesional skin
Face and trunk
26S For the total number of Malassezia species, there were no significant differences between lesional and nonlesional areas No serial sampling
Patients on active treatment
Low to moderate
Kong et al . 2012 60 AD Prospective cohort
12 AD/11 HV
Sterile swabs
Multiple time points
Baseline, flare, post‐flare
16S rRNA V1‐V9 Flare ups were associated with an increased proportion of Staphylococcus sequences, particularly S. aureus, and correlated with disease severity
Increases in Streptococcus, Propionbacterium, and Corynebacterium species were observed following therapy
Small cohort
Only moderate to severe patients
Different treatments regimens during flare
Low to moderate
Seite et al . 2014 54 AD Prospective cohort
Emolliens treatment
46
Sterile swabs
Lesional and nonlesional skin
Multiple time points
16S rRNA V1‐V2 Affected skin harboured a greater relative abundance of Staphylococcus, and in particular S. epidermis, compared to healthy skin
Responders had increased microbial diversity and decrease in Staphylococcus species
Large time between first and second sample
Only moderate patients
Low to moderate
Chng et al . 2016 55 AD Case control
19 medical history AD/15 HV/5 positive skin prick
Tape stripping anti‐cubital fossa 16S rRNA V3‐V6
WMS
Nonflare, baseline skin microbiome signatures enriched for Streptococcus and Gemella in AD prone skin versus normal skin
Increased percentage of S. aureus carriers noted in AD cohort over control subjects
Small cohort
No serial sampling
No lesional samples
Low
Gonzalez et al . 2016 56 AD Randomized, placebo‐controlled, single‐blinded
Topical steroid
or
Topical steroid + dilute bleach bath
21 AD/14 HV
Sterile swabs
Lesional and nonlesional skin
Multiple time points
16S rRNA V4 Affected skin harboured a greater relative abundance of S. aureus
Microbial diversity at all lesional sites inversely correlated with overall EASI Index score
Taxonomic normalization occurred on lesional following treatments
Bacterial communities on lesional skin resemble nonlesional skin but remain distinct from healthy control skin
Small study Moderate
Seite et al . 2017 57 AD Double‐blind, Randomized, comparative
Emollient A
or
Emollient B
53
Sterile swabs
Lesional and nonlesional skin
Multiple time points
16S rRNA V1‐V2 Significant increased levels of Xanthomonas genus in patients treated with emollient A
Levels of Staphylococcus genus increased between Day 1 and Day 28 in patients treated with emollient B
Only moderate patients
No wash‐out other treatments
Moderate
Kim et al . 2017 59 AD Prospective cohort
Wet dressings
Topical steroids
Antihistamines
Antibiotics
27 AD
6 HV
Saline soaked gauzes 16S rRNA V1‐V3 Proportion of Staphylococcus significantly decreased after treatment
Diversity (Shannon Index) significantly increased after treatment
Small study
Patients on wide variety of treatments
No nonlesional skin analysis
Low to moderate

AD, atopic dermatitis; AV, acne vulgaris; DFU, diabetic foot ulcer; HS, hidradenitis suppurativa; NU, neuropathic ulcer; OTH, other; OTU, operational taxonomic unit; PSU, post‐surgical ulcer; PU, pressure ulcer; PV, psoriasis vulgaris; SD/PC, seborrhoeic dermatitis/pityriasis capitis; UC, ulcus cruris; VLU, venous leg ulcer