Efficacy of fermented milk and whey proteins in Helicobacter pylori eradication: A review

Table 2 Studies comparing capsule based probiotic (bacteria only) with placebo or standard therapy plus capsule based probiotic vs standard therapy

Ref.	Type of trial	Evidence grade1	Quality rating2	Subjects	Study design	Study groups/ methods	Outcome variable/s	Results and conclusions
Positive
Canducci et al[27], Italy, 2000	Human	1+	+	120 H. pylori positive patients	RCT	Two groups: RCA (Rabeprazole, Clarithromycin, Amoxycillin) group- triple therapy (n = 60), RCAL group- triple therapy with Lactéol Fort for 7 d	Effect of L. acidophilus could improve the efficacy of a standard anti-H. pylori therapy	In RCA group eradication was successful in 72% at PP analysis or 70% at ITT analysis and in RCAL group eradication was achieved with 88% with PP analysis, 87% with ITT analysis
Negative
Gotteland et al[28], 2005	Human	1+	+	254 children positive for H. pylori	RCT	Three groups: Antibiotics (group Ab)- (n = 57) for 8 d, Lactobacillus acidophilus LB (group Ab)- (n = 63) for 8 wk, Saccharomyces boulardii plus inulin (group Sb1)- (n = 62) 8 wk	To evaluate the capacity of Lactobacillus acidophilus LB and of symbiotic combination of Sb plus inulin to interfere with H. pylori colonization in children	H. pylori was eradicated in 66%, 12% and 6.5% of the children from the Ab, Sb1 and LB groups, respectively. A moderate but significant difference in ∆ DOB was detected in children receiving living Sb1, but not in those receiving LB
Lionetti et al[29], 2006, Italy	Human	1+	++	40 H. pylori positive children	RCT	Two groups: Group A- 10 d sequential therapy plus L. reuteri ATCC 55730, Group B-Placebo with the same therapy	Effect of Lactobacillus reuteri to prevent or minimize the gastrointestinal side-effects	No significant differences were observed between the groups in the success of H. pylori eradication. Treatment was successful in 17 of 20 [85% (95%CI: 68-100)] patients in probiotic supplemented when compared with 16 of 20 patients in placebo group [80% (95%CI: 61–99)] (P = NS)
Nista et al[30], 2004, Italy	Human	1+	++	106 H. pylori positive patients	RCT	Two groups: Group A- triple therapy for 7 d plus Bacillus clausii (probiotic) for 14 d starting from the first day of the treatment (n = 54) Group B- triple therapy plus placebo (n = 52)	Effect of probiotic on incidence and severity of antibiotic-associated side-effects during anti- H. pylori therapy and eradication was evaluated with means of 13C-urea breath test	The H. pylori eradication rate was similar between B. B. clausii and placebo groups. In particular, ITT analysis has shown H. pylori was eradicated in 39 of 54 patients (72.2%) in the B. clausii group and in 37 of 52 patients (71.15%) in the placebo group. In PP population, H. pylori was eradicated in 39 of 50 patients (78%) in the B. clausii group and in 37 of 50 patients (74%) in the placebo group
Myllyluoma et al[31], 2005, Finland	Human	1+	+	47 subjects with H. pylori infection	CCT	Two groups: Group A –probiotic drink (n = 23), group B- Placebo (n = 24) during H. pylori eradication and for 3 wk following the treatment	Effect of probiotic therapy on symptoms associated with the recommended H. pylori eradication treatment. As a secondary end-point to find out whether this therapy could improve the eradication rate	The H. pylori eradication rate was non-significantly higher in the group receiving probiotic therapy (91% vs 79%, P = 0.42)
Cindoruk et al[32], 2007, Turkey	Human	1+	+	124 patients with H. pylori infection	RCT	Two groups: Group A- triple therapy plus S. boulardii, Group B- triple therapy plus placebo for 14 d	Efficacy and safety of S. boulardii in the prevention of side effects and the eradication success of anti-H. pylori therapy	H. pylori eradication rate, although higher in the treatment group, was statistically similar in treatment and control groups: 71% (44/62) vs 59.7% (37/62), respectively (P > 0.05)
Armuzzi et al[33], 2001, Italy	Human	1+	+	60 healthy asymptomatic subjects screened positive for H. pylori infection	CCT	Two groups: Group A- triple therapy for 7 d plus Lactobacillus GG for 14 d during and the week after eradication therapy, Group B- triple therapy plus placebo	Effect of probiotic Lactobacillus GG to minimize or to prevent the occurrence of gastrointestinal side effects	H. pylori eradication rates in group A was 83.33% (25/30) and in group B was 80% (24/30). H. pylori eradication rate had no significant difference
Guo et al[34], China, 2004	Human	FT NA	FT NA	97 H. pylori positive symptomatic patients	CCT	Two groups: treatment group (triple therapy plus Bifid triple viable capsule containing Bifidobacteria longum, faecal streptococci, Lactobacillus acidophilus) (n = 47) control group: triple therapy (n = 50)	Efficacy of probiotic in the treatment of H. pylori	Eradication rate was 93.6% (44/47) in treatment group and 88% in control group (44/50). H. pylori eradication rate had no significant difference
Armuzzi et al[35], 2001, Italy	Human	FT NA	FT NA	120 healthy asymptomatic subjects screened positive for H. pylori infection	CCT	Two groups: Group A- triple therapy for 7 d plus Lactobacillus GG for 14 d during and the week after eradication therapy, Group B- triple therapy plus placebo	Effect of probiotic Lactobacillus GG to minimize or to prevent the occurrence of gastrointestinal side effects.	H. pylori eradication rates in group A was 80% (48/60) and in group B was 76.67% (46/60). H. pylori eradication rate had no significant difference
Cremonini et al[36], Italy, 2002	Human	FT NA	FT NA	85 H. pylori positive, asymptomatic patients	CCT	Four groups- received both during and for 7 d after a 1 wk-triple therapy Group I- Lactobacillus GG (n = 21), group II-Saccharomyces boulardii (n = 22), group III-lactobacillus spp. And bifidobacteria (n = 21), group IV-placebo (n = 21)	Efficacy of probiotic in the eradication of H. pylori infection	The H. pylori eradication rate was almost identical between the probiotic and placebo groups
Tursi et al[37], 2004, Italy	Human	FT NA	FT NA	70 patients with persistent H. pylori infection	CCT	Two groups- group A- quadruple therapy plus bacteria lactobacillus casei subsp. casei DG or group B- quadruple therapy only	Effect of probiotic supplementation on the effectiveness and tolerability of a new second-line 10 d quadruple therapy	H. pylori was negative in 33/34 group A patients (PP: 97.05% ITT: 94.28%) and 30/32 Group B patients
Cao et al[38], China, 2005	Human	FT NA	FT NA	128 H. pylori positive symptomatic patients	CCT	Two groups: Group A -quadruple therapy plus Clostridium butyricum group B- quadruple therapy	Effect of treatment given in eradication of H. pylori	Eradication rates in group A 96.88% (62/64) and group B 92.19% (59/64) was not significantly different

¹Levels of evidence: 1++ High quality meta-analysis, systematic reviews of RCTs, or RCTs with a very low risk of bias; 1+ Well conducted meta-analysis, systematic reviews of RCTs or RCTs with a low risk of bias; 1- Meta-analysis, systematic reviews or RCTs or RCTs with a high risk of bias; 2++ High quality systematic reviews of case-control or cohort studies or high quality case-control or cohort studies with a very low risk of confounding, bias, or chance and a high probability that the relationship is causal; 2+ Well conducted case control or cohort studoes with a low risk of confounding, bias, or chance and a significant risk that the relationship is not causal; 3 Non-analytic studies, e.g., case reports, case series; 4 Expert opinion.

²Quality rating for individual studies: ++ Applies if all or most criteria from the checklist are fulfilled; where criteria are not fulfilled the conclusions of the study or review are thought very unlikely to alter; + Applies if some of the criteria from the checklist are fulfilled; where criteria are not fulfilled or are not adequately described, the conclusions of the study or review are thought unlikely to alter; - Applies if few or no criteria from the checklist are fulfilled; where criteria are not fulfilled or are not adequately described, the conclusions of the study or review are thought likely or very likely to alter. H. pylori: Helicobacter pylori; RCT: Randomised controlled trial; CCT: Controlled clinical trial; CT: Clinical trial; NR: Not reported; NS: Not significant.