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Table 1 Characteristics of the included studies

From: Effect of probiotic supplementation on gastrointestinal motility, inflammation, motor, non-motor symptoms and mental health in Parkinson’s disease: a meta-analysis of randomized controlled trials

Study

Study design

No. of participants

(experimental/control)

Age, yearsa

(experimental/control groups)

Probiotics

Control

group

Frequency

and

duration

Outcome

measure

Main finding

Barichella et al. [9]

Randomized double-blind

clinical trial

80/40

71.8 ± 7.7/69.5 ± 10.3

Fermented milk containing multiple probiotic strains and prebiotic fiber

Pasteurized, fermented,

fiber-free milk

Once daily for 4 weeks

1. Bowel movements

2. Bristol Stool Scale score

3. Treatment satisfaction

4. Treatment continuation

Probiotics were superior to placebo in improving constipation in patients with PD

Borzabadi et al. [10]

Randomized double-blind

clinical trial

25/25

66.7 ± 10.7/

66.9 ± 7.0

Capsule 8 × 109 CFU

Lactobacillus acidophilus

Bifidobacterium bifidum

L. reuteri

Lactobacillus fermentum

(2 × 109 CFU each)

Placebo capsule

Once daily for 12 weeks

1. Gene expression

(IL-1, IL-8, TNF-α, TGF-β, PPAR-γ, VEGF, and LDLR)

2. Biomarkers of oxidative stress

(total glutathione and nitric oxide)

The probiotics group had significantly improved gene expression levels of IL-1, IL-8, TNF-α, TGF-β, and PPAR-γ; however, the gene expression of VEGF and LDLR and the number of biomarkers of inflammation and oxidative stress were unaffected

Du et al. [25]

Randomized clinical trial

23/23

68.39 ± 7.55/66.65 ± 8.66

Capsule

5 × 109 CFU Bacillus licheniformis

1 × 107 CFU

Lactobacillus acidophilus, Bifidobacterium longum,

Enterococcus faecalis

None

Three times daily

for 12 weeks

1. Bowel movements

2. Bristol Stool Scale scores

3. Constipation (PAC-SYM)

4. Quality of life (PAC-QOL)

The probiotics group demonstrated improved bowel movements and improved scores on symptom scales associated with constipation (PAC-SYM scores and PAC-QOL scores)

Georgescu et al. [11]

Randomized controlled clinical trial

20/20

75.6 ± 9.7/69.8 ± 5.6

Capsule 60 mg

Lactobacillus acidophilus Bifidobacterium infantis

Trimebutine

200 mg

three times daily

Twice daily for 12 weeks

1. Abdominal pain

2. Bloating

3. Constipation

Probiotics improved abdominal pain and bloating similar to trimebutine; however, trimebutine was more effective for constipation with incomplete evacuation

Ibrahim et al. [12]

Randomized double-blind

clinical trial

22/26

69.0 ± 5.2/70.5 ± 6.1

Capsule 3 × 1010 CFU

Lactobacillus sp. Bifidobacterium sp.

fructo-oligosaccharides lactose

Fermented milk

Twice daily for 8 weeks

1. Garrigues Questionnaire

2. Gut transit time

3. Quality of life (PDQ39-SI)

4. Motor symptoms (MDS-UPDRS)

5. Non-motor symptoms (NMSQ)

Probiotics led to improved bowel opening frequencies and whole gut transit times in PD

Michela et al. [13]

Randomized double-blind

clinical trial

80/40

N/R/N/R

Fermented milk containing multiple probiotic strains and prebiotic fiber

Pasteurized,

fermented,

fiber-free milk

Once daily for 4 weeks

1. Complete bowel movements

Probiotics were superior to placebo in improving numbers of complete bowel movements

Mehrabani et al. [26]

Randomized double-blind

clinical trial

40/40

68.2 ± 7.7/69.1 ± 8.2

Powder in sachets

5 × 109 CFU

Lactobacillus acidophilus

Lactobacillus rhamnosus Lactobacillus plantarum Bifidobacterium longum Streptococcus thermophilus

Maltodextrin

Once daily for

12 weeks

1. Biomarkers of oxidative stress

(TAC, TOS, OSI, GSH, MDA)

2. Quality of life (PDQ39)

3. Mental status

(Hospital Anxiety and Depression Scale)

4. Fatigue Severity Scale scores

The probiotics group had increased TAC, reduced MDA levels, and reduced OSI values, and it also had lower levels of depression and displayed improvements in well-being and cognitive impairment

Sun et al. [24]

Randomized double-blind

clinical trial

48/34

66.46 ± 6.98/68.76 ± 6.91

Capsule 3 × 1010 CFU

Bifidobacterium animalis subsp. lactis

Maltodextrin

Once daily for 12 weeks

1. Number of spontaneous defecation incidents

2. Bristol Stool Scale scores

3. Motor symptoms (MDS-UPDRS)

4. Quality of life (PAC-QOL)

5. Hamilton Anxiety Rating Scale scores

6. Hamilton Depression Scale scores

Probiotics improved sleep quality and alleviated anxiety and gastrointestinal symptoms

Tamtaji, O. R., et al. (2019)[14]

Randomized double-blind

clinical trial

30/30

68.2 ± 7.8/67.7 ± 10.2

Capsule 8 × 109 CFU

Lactobacillus acidophilus

Bifidobacterium bifidum

Lactobacillus reuteri

Lactobacillus fermentum

(2 × 109 CFU each)

Placebo capsule

Once daily for 12 weeks

1. Motor symptoms (MDS-UPDRS)

2. High-sensitivity CRP

3. Biomarkers of oxidative stress

(total glutathione,

malondialdehyde)

4. Diabetes markers

(fasting plasma glucose, Insulin, Insulin sensitivity check index)

5. Dyslipidemia markers

(triglycerides, VLDL, LDL, HDL)

Probiotics had useful impacts on MDS-UPDRS scores and some metabolic profiles

Tan et al. [15]

Randomized double-blind

clinical trial

34/38

70.9 ± 6.6/68.6 ± 6.7

Capsule 109 CFU Lactobacillus Acidophilus

Lactobacillus reuteri

Lactobacillus gasseri

Lactobacillus rhamnosus

Bifidobacterium bifidum Bifidobacterium longum Enterococcus faecalis

Enterococcus faecium

Placebo capsule

Once daily for 4 weeks

1. Bowel movements per week

2. Average stool consistency

3. Quality of life (PAC-QOL)

4. Constipation severity scores

Probiotics were effective for relieving constipation in patients with PD

Yang et al. [16]

Randomized double-blind

clinical trial

63/59

N/R/N/R

Fermented milk

containing 109 CFU Lactobacillus casei strain

Placebo capsule

Once daily for 12 weeks

1. Quality of life (PDQ39)

2. Non-motor symptoms (NMSQ)

3. Hamilton Anxiety Rating Scale scores

4. Hamilton Depression Rating Scale scores

Probiotics may be a useful approach in managing the non-motor symptoms of PD

  1. N/R, not recorded; CFU, colony-forming units; IL, interleukin; TNF, tumor necrosis factor; TGF, transforming growth factor; PPAR, peroxisome proliferator-activated receptor; VEFG, vascular endothelial growth factor; LDLR, low-density lipoprotein receptor; PAC-SYM, Patient Assessment of Constipation Symptoms; PAC-QOL, Patient Assessment of Constipation Quality of Life, UPDRS, Unified Parkinson's Disease Rating Scale; NMSQ, Non-Motor Symptoms Questionnaire; PDQ-39, Parkinson's Disease Questionnaire; PDSS, Parkinson’s Disease Sleep Scale; TAC, total antioxidant capacity; TOS, total oxidant status; OSI, oxidative stress index; GSH, glutathione; MDA, malondialdehyde; CRP, C-reactive protein; VLDL, very-low-density lipoprotein; LDL, low-density lipoprotein; HDL, high-density lipoprotein
  2. aMean age ± standard deviation