Probiotics for treating eczema

Robert John Boyle; Fiona J Bath‐Hextall; Jo Leonardi‐Bee; Dedee F Murrell; Mimi LK Tang

doi:10.1002/14651858.CD006135.pub2

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Analysis 1.1

Comparison 1 Probiotic vs Placebo, Outcome 1 Participant or parent‐rated symptoms of eczema (SCORAD part C) at the end of treatment.

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Analysis 1.2

Comparison 1 Probiotic vs Placebo, Outcome 2 Participant or parent‐rated global change in eczema symptoms during treatment.

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Analysis 1.3

Comparison 1 Probiotic vs Placebo, Outcome 3 Parent or participant‐rated eczema severity (SCORAD part C) (Long term).

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Analysis 1.4

Comparison 1 Probiotic vs Placebo, Outcome 4 Global eczema severity score (Total SCORAD) (Short term).

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Analysis 1.5

Comparison 1 Probiotic vs Placebo, Outcome 5 Global eczema severity score (Total SCORAD) ‐ Sensitivity analysis ‐ Change score.

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Analysis 1.6

Comparison 1 Probiotic vs Placebo, Outcome 6 Investigator‐rated eczema severity (SCORAD parts A/B) (Long term).

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Analysis 1.7

Comparison 1 Probiotic vs Placebo, Outcome 7 Participant/parent‐rated symptoms of eczema (SCORAD part C)(Short term)‐Stratified by Age group.

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Analysis 1.8

Comparison 1 Probiotic vs Placebo, Outcome 8 Participant/parent‐rated global change in symptoms of eczema (Short term) ‐ Stratified by Age.

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Analysis 1.9

Comparison 1 Probiotic vs Placebo, Outcome 9 Global eczema severity score (Total SCORAD) (Short term) ‐ Stratified by Age group.

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Analysis 1.10

Comparison 1 Probiotic vs Placebo, Outcome 10 Global eczema severity score (Total SCORAD) (Short term) ‐ Stratified by Presence of Atopy.

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Analysis 1.11

Comparison 1 Probiotic vs Placebo, Outcome 11 Global eczema severity score (Total SCORAD) (Short term) ‐ Stratified by Challenge‐Proven Food Allergy.

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Analysis 1.12

Comparison 1 Probiotic vs Placebo, Outcome 12 Global eczema severity score (Total SCORAD) (Short term) ‐ Stratified by Eczema Severity.

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Analysis 1.13

Comparison 1 Probiotic vs Placebo, Outcome 13 Global eczema severity (Total SCORAD) (Short term)‐Stratified by Probiotic.

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Analysis 1.14

Comparison 1 Probiotic vs Placebo, Outcome 14 Adverse events (Short term).

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Table 1. Terms used to categorise trial participants with eczema

Forms of eczema included	Forms of eczema excluded
Atopic eczema	Seborrheic eczema
Atopic dermatitis	Contact eczema
Besnier's prurigo	Allergic contact eczema
Neurodermatitis atopica (German)	Irritant contact eczema
Flexural eczema/ dermatitis	Discoid/ nummular eczema
Periorbital eczema	Asteatotic eczema
Childhood eczema	Varicose/ stasis eczema
Infantile eczema	Photo‐/ light‐sensitive eczema
'Eczema' unspecified	Chronic actinic dermatitis
Constitutional eczema	Dishydrotic eczema
Endogenous eczema	Pompholyx eczema
Chronic eczema	Hand eczema
Neurodermatitis	Frictional lichenoid dermatitis
Neurodermatitis (German)	Lichen simplex
	Occupational dermatitis
	Prurigo

Table 1. Terms used to categorise trial participants with eczema

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Table 2. Methodological quality of included studies

Study	Treatment allocation	Blinding	Loss to follow‐up	Clarity of methods	Compliance	Dietary management
Brouwer 2006	Method not described	Unclear	One1 participant lost to follow‐up after randomisation. Available case analysis used, with no exclusions after randomisation and no imputation of data.	Clear	No compliance measures described	Adequate exclusion of other probiotics during study
Gruber 2007	Method not described	Described as 'double blind' but no details given	No loss to follow‐up. Four participants excluded from analysis after randomisation.	Unclear what the placebo was; otherwise clear	92.5% of doses taken by probiotic group; 94.4% by placebo group	Not stated, other than an encouragement to avoid allergens
Isolauri 2000	Method not described	Described as 'double blind' but no details given	Loss to follow‐up not stated. Not clear whether available case analysis was used.	Unclear ‐ dose and duration of probiotic treatment received not clearly described. Severity of participant eczema at baseline not described.	No compliance measures reported	Not stated
Majamaa 1997	Method not described	Described as 'double blind' but no details given	Loss to follow‐up data not given. Not clear whether available case analysis was used. Four participants excluded from analysis after randomisation, based on later negative food challenge.	Unclear ‐ precise dose of probiotic received by participants not stated	No compliance measures described	Not stated
Passeron 2006	Treatment allocated by hospital pharmacy according to a computer generated randomisation sequence.	Participants, clinicians and outcome assessers were all blinded	Nine participants lost to follow‐up. Available case analysis used, with no exclusions after randomisation. A secondary analysis was performed by the authors using imputation of missing data, but was not included in this meta‐analysis.	Clear	No compliance measures described	Not stated
Rosenfeldt 2003	Method not described	Described as 'double blind' but no details given	Fifteen participants excluded from analysis after randomisaton, for reasons including poor compliance, exacerbation of eczema and loss to follow‐up. No available case analysis performed.	Clear	No compliance measures described	Adequate exclusion of other probiotics during study
Sistek 2006	Treatment allocated by a third party according to a computer generated randomisation sequence. Third party not otherwise involved in the study.	Participants, clinician and outcome assessor blind	One study withdrawal. Available case analysis was used, with no exclusions after randomisation and no imputation of data.	Clear	Assessed by two telephone calls	One participant noted to have taken non‐study probiotic
Taniuchi 2005	Method not described	Unclear	Loss to follow‐up not reported. Not clear whether available case analysis was used.	Clear	No compliance measure described	Not stated
Viljanen 2005	Treatment allocated by a remote third party according to a computer generated randomisation sequence.	Participants, clinicians and outcome assessor blinded	Twenty‐two participants were lost to follow‐up. Analysis was by 'treatment received' because four participants who did not tolerate the study formula were excluded from analysis.	Method for diagnosing eczema not described	No compliance measures described	Not stated
Weston 2005	Treatment allocated by hospital pharmacy according to a computer generated randomisation sequence.	Outcome assessor blind, and also stated 'double blind'	Three participants lost to follow‐up. Available case analysis was used, with no exclusions after randomisation and no imputation of data.	Clear	Sachet counts and parent‐completed sachet administration chart. Good compliance.	Adequate exclusion of other probiotics during study
Kirjavainen 2003	Method not described	Described as 'double blind' but no details given	No loss to follow‐up data given. Analysis was by 'treatment received' because five participants who did not tolerate the study formula were excluded from analysis after randomisation.	Unclear ‐ intended duration of study treatment not stated	No compliance measures reported	Not stated
Folster‐Holst 2006	Method not described	Described as 'double blind' but no details given	Six participants lost to follow‐up. Available case analysis was used.	Clear	No compliance measures reported	Not stated

Table 2. Methodological quality of included studies

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Table 3. Quality of Life Measures (Weston 2005)

	Probiotic 8 weeks	Placebo 8 weeks	Probiotic 16 weeks	Placebo 16 weeks
N	26	27	26	27
Median	‐2	‐2	‐2.5	‐3
IQR	‐5 to ‐0.7	‐6 to +2	‐5 to ‐1	‐7.2 to +2

Table 3. Quality of Life Measures (Weston 2005)

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Table 4. Non‐parametric analyses of SCORAD scores

	Majamaa 1month LGG	Majamaa 1month Place	Majamaa 2mo LGG	Majamaa 2mo Placebo	Isolauri 2mo LGG	Isolauri 2mo Bb12	Isolauri 2mo Placebo
N	13	14	13	14	9	9	9
Median	15	19	16	14	1	0	13.4
IQR	7‐28	13‐31	6‐25	2‐38	0.1‐8.7	0‐3.8	4.5‐18.2
IQR = Interquartile range

Table 4. Non‐parametric analyses of SCORAD scores

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Table 5. Assessments of need for topical corticosteroid treatment during study

	Rosenfeldt Probiotic	Rosenfeldt Placebo	Gruber Probiotic	Gruber Placebo	Weston Probiotic	Weston Placebo	Folster‐H Probiotic	Folster‐H Placebo
N	39	39
Median grams hydrocortisone butyrate applied	7.8	6.0
Range	0 to 67	0 to 59
Mean grams 1% hydrocortisone applied			0.8	3.5
Standard deviation			45.0	29.8
Median change in topical corticosteroid use score					0.25	‐1.0
IQR for change in corticosteroid score					‐6.7 to +7.0	‐8.0 to +0.7
Mean applications per week							3.0	3.2
Standard deviation							0.6	0.9

Table 5. Assessments of need for topical corticosteroid treatment during study

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Comparison 1. Probiotic vs Placebo

Outcome or subgroup title	No. of studies	No. of participants	Statistical method	Effect size
1 Participant or parent‐rated symptoms of eczema (SCORAD part C) at the end of treatment Show forest plot	5		Mean difference (Random, 95% CI)	‐0.90 [‐2.84, 1.04]

1.1 Parallel group trials	4		Mean difference (Random, 95% CI)	‐0.68 [‐3.07, 1.71]
1.2 Cross‐over trials	1		Mean difference (Random, 95% CI)	‐1.80 [‐3.59, ‐0.01]
2 Participant or parent‐rated global change in eczema symptoms during treatment Show forest plot	3		Odds ratio (Random, 95% CI)	0.40 [0.14, 1.15]

2.1 Parallel group trials	2		Odds ratio (Random, 95% CI)	0.70 [0.27, 1.77]
2.2 Cross‐over trials	1		Odds ratio (Random, 95% CI)	0.18 [0.05, 0.60]
3 Parent or participant‐rated eczema severity (SCORAD part C) (Long term) Show forest plot	2	102	Mean Difference (IV, Random, 95% CI)	‐2.27 [‐3.97, ‐0.58]

4 Global eczema severity score (Total SCORAD) (Short term) Show forest plot	7		Mean difference (Random, 95% CI)	‐2.46 [‐7.45, 2.53]

4.1 Parallel group studies	6		Mean difference (Random, 95% CI)	‐1.68 [‐7.15, 3.80]
4.2 Cross‐over studies	1		Mean difference (Random, 95% CI)	‐6.27 [‐11.21, ‐1.32]
5 Global eczema severity score (Total SCORAD) ‐ Sensitivity analysis ‐ Change score Show forest plot	5		Mean difference (Random, 95% CI)	‐2.47 [‐4.72, ‐0.21]

5.1 Parallel group trial	4		Mean difference (Random, 95% CI)	‐2.15 [‐4.64, 0.34]
5.2 Cross‐over trial	1		Mean difference (Random, 95% CI)	‐3.93 [‐9.25, 1.40]
6 Investigator‐rated eczema severity (SCORAD parts A/B) (Long term) Show forest plot	2	102	Mean Difference (IV, Fixed, 95% CI)	‐8.11 [‐13.14, ‐3.09]

7 Participant/parent‐rated symptoms of eczema (SCORAD part C)(Short term)‐Stratified by Age group Show forest plot	5		Mean difference (Random, 95% CI)	Subtotals only

7.1 Age under 2 years	2		Mean difference (Random, 95% CI)	‐0.13 [‐4.18, 3.91]
7.2 Age 2‐12 years	1		Mean difference (Random, 95% CI)	0.33 [‐1.94, 2.60]
7.3 Age not categorised	2		Mean difference (Random, 95% CI)	‐2.23 [‐3.71, ‐0.74]
8 Participant/parent‐rated global change in symptoms of eczema (Short term) ‐ Stratified by Age Show forest plot	3		Odds ratio (Random, 95% CI)	Totals not selected

8.1 Age under 2 years	1		Odds ratio (Random, 95% CI)	0.0 [0.0, 0.0]
8.2 Age 2‐ 12 years	1		Odds ratio (Random, 95% CI)	0.0 [0.0, 0.0]
8.3 Age not categorised	1		Odds ratio (Random, 95% CI)	0.0 [0.0, 0.0]
9 Global eczema severity score (Total SCORAD) (Short term) ‐ Stratified by Age group Show forest plot	7		Mean difference (Random, 95% CI)	Subtotals only

9.1 Age under 2 years	3		Mean difference (Random, 95% CI)	0.74 [‐5.06, 6.54]
9.2 Age 2 ‐ 12 years	1		Mean difference (Random, 95% CI)	‐3.28 [‐13.78, 7.22]
9.3 Age not categorised	3		Mean difference (Random, 95% CI)	‐5.66 [‐14.82, 3.50]
10 Global eczema severity score (Total SCORAD) (Short term) ‐ Stratified by Presence of Atopy Show forest plot	7		Mean difference (Random, 95% CI)	Subtotals only

10.1 Participants with atopy	2		Mean difference (Random, 95% CI)	‐5.50 [‐23.87, 12.87]
10.2 Participants with unknown atopic status	5		Mean difference (Random, 95% CI)	‐1.73 [‐7.29, 3.83]
11 Global eczema severity score (Total SCORAD) (Short term) ‐ Stratified by Challenge‐Proven Food Allergy Show forest plot	6		Mean Difference (IV, Random, 95% CI)	Subtotals only

11.1 Food allergy present	1	120	Mean Difference (IV, Random, 95% CI)	1.15 [‐3.20, 5.50]
11.2 Unknown food allergic status	5	300	Mean Difference (IV, Random, 95% CI)	‐3.19 [‐10.59, 4.20]
12 Global eczema severity score (Total SCORAD) (Short term) ‐ Stratified by Eczema Severity Show forest plot	4		Mean Difference (IV, Random, 95% CI)	Subtotals only

12.1 Severe eczema (SCORAD over 40)	3	70	Mean Difference (IV, Random, 95% CI)	‐7.00 [‐15.34, 1.34]
12.2 Moderate eczema (SCORAD 15‐40)	4	175	Mean Difference (IV, Random, 95% CI)	‐3.45 [‐10.34, 3.45]
12.3 Mild eczema (SCORAD under 15)	1	8	Mean Difference (IV, Random, 95% CI)	‐5.53 [‐15.29, 4.23]
13 Global eczema severity (Total SCORAD) (Short term)‐Stratified by Probiotic Show forest plot	7		Mean difference (Random, 95% CI)	Subtotals only

13.1 Lactobacillus rhamnosus GG, either alone or in combination with different probiotic bacteria	3		Mean difference (Random, 95% CI)	3.37 [0.55, 6.20]
13.2 Other Lactobacillus strains, either alone or in combination with different probiotic bacteria	4		Mean difference (Random, 95% CI)	‐7.64 [‐11.65, ‐3.62]
14 Adverse events (Short term) Show forest plot	5		Odds Ratio (M‐H, Random, 95% CI)	Subtotals only

14.1 Gastrointestinal symptoms	5	304	Odds Ratio (M‐H, Random, 95% CI)	1.57 [0.78, 3.15]

Comparison 1. Probiotic vs Placebo

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