You are on page 1of 7

Infectious Diseases

Treating Bugs with Bugs: The Role of Probiotics as Adjunctive


Therapy for Helicobacter pylori
Sheila M Wilhelm, Jennifer L Johnson, and Pramodini B Kale-Pradhan

elicobacter pylori is a spiral-shaped,


gram-negative bacterium that reOBJECTIVE: To review the literature on the role of probiotics as adjunctive therapy
sides between the mucous layer and surin the treatment of Helicobacter pylori infections.
face epithelial cells in the stomach or inDATA SOURCES: Literature was accessed through MEDLINE (1966-March 2011)
testines.1 It colonizes the gastrointestinal
using the terms H. pylori, probiotic, Lactobacillus, Bifidobacterium, Saccharomyces,
Bacillus clausii, and Propionibacterium. Article references were hand-searched for
lining when the mucosal integrity has been
additional relevant articles and abstracts.
compromised by environmental factors
STUDY SELECTION AND DATA EXTRACTION: All English-language articles published
such as increased acid production, pharin full were evaluated. Randomized, double-blind, placebo-controlled trials
maceutical agents (nonsteroidal antiinassessing the use of probiotics combined with standard eradication therapy of H.
flammatory drugs, aspirin, selective seropylori infection in adults were included in the review.
tonin reuptake inhibitors), dietary toxins,
DATA SYNTHESIS: Various probiotics, including Lactobacillus spp., Saccharomyces
or stress.2,3 H. pylori infects 30-40% of the
spp., Bifidobacterium spp., and B. clausii, reduce adverse effects such as nausea,
population in developed countries like the
taste disturbance, diarrhea, and epigastric pain, and increase tolerability of H.
pylori eradication therapy. Based on the studies reviewed, probiotics do not affect
US.3 H. pylori infection is more common
H.
pylori eradication rates.
in lower socioeconomic conditions and is
CONCLUSIONS
: Probiotics may be beneficial in reducing adverse effects and
prevalent in about 80-90% of the populaincreasing
tolerability
of H. pylori eradication regimens. They may especially be
4
tion in developing countries. This colohelpful in patients with recurrent H. pylori infection and a history of gastrointestinal
nization leads to ulcerations in the mucosadverse effects with antibiotics. Pharmacists can play an important role in
al lining and causes peptic ulcer disease in
educating patients regarding probiotic use during H. pylori eradication therapy.
up to 20% of infected individuals.5 SympKEY WORDS: Bifidobacterium, H. pylori, Lactobacillus, probiotic, Saccharomyces.
toms of peptic ulcer disease include abAnn Pharmacother 2011;45:960-6.
dominal pain, nausea, reflux symptoms,
Published Online, 21 Jun 2011, theannals.com, DOI 10.1345/aph.1Q104
and vomiting; it is the most common
cause of upper gastrointestinal bleeding
and perforation.2 Symptoms and complitamine receptor antagonist, and bismuth.3 Table 1 includes
cations associated with peptic ulcer disease lead to job absenthe first-line recommendations for H. pylori eradication
teeism, reduced work productivity, and lower health-related
recommended
by the American College of Gastroenteroloquality of life. Direct costs related to outpatient and inpatient
3
gy.
Treatment
will fail in approximately 10-35% of pavisits and medication costs are a burden to the health-care
2
tients, and H. pylori will remain resulting from several facsystem and to patients.
tors, including nonadherence related to adverse effects or
One of the main treatment goals for peptic ulcer disease
6
complicated dosing regimens, high prescription costs, and
is H. pylori eradication. Treatment of H. pylori consists of
antibiotic resistance.7,8
triple or quadruple therapy that includes antimicrobials and
Probiotics are microorganisms that help maintain normal
acid suppressive therapy with a proton pump inhibitor, hisgut flora and prevent colonization by pathogenic organisms
via a number of mechanisms, including competitive inhibiAuthor information provided at end of text.
tion of gut wall adhesion of pathogenic microorganisms and

960

The Annals of Pharmacotherapy

2011 July/August, Volume 45

Copyrighted material. Reproduo proibida.

theannals.com

generalized immune system enhancement because of the


ability of probiotics to bind to epithelial cells.9-11 When probiotics bind to epithelial cells, they release substances that prevent the growth of pathogens and modulate intestinal permeability.
Data Sources and Selection
This review examines the role of probiotics in the treatment of H. pylori infection. A literature search using
MEDLINE (1966-March 2011) was completed to identify
randomized, double-blind, placebo-controlled trials published in full in English assessing the use of probiotics
combined with standard eradication therapy of H. pylori
infection. The search included some of the most common
and familiar strains of probiotics used in gastrointestinal
disorders: Helicobacter pylori, probiotic, Lactobacillus, Bifidobacterium, Saccharomyces, Bacillus clausii, and Propionibacterium. The search was further limited to adults.
Bibliographies of recent review articles and systematic reviews were hand-searched for relevant trials.
Clinical Studies
Four randomized, double-blind, placebo-controlled trials assessing the use of probiotics combined with standard
eradication therapy of H. pylori infection were identified
(Table 2).12-15 In all 4 trials, participants were healthy and,
although they were asymptomatic, the results of H. pylori
cultures were positive. All trials assessed antibiotic-associated adverse effects and treatment tolerability as the primary outcome. H. pylori eradication rate was the secondary
outcome in each of the trials.
In the first trial, 60 participants were treated with triple
antibiotic therapy on days 1-7 and Lactobacillus GG on

days 1-14.12 Probiotics significantly improved symptoms,


including nausea (10% vs 36.6%; RR 0.3; 95% CI 0.1 to
0.9), taste disturbance (23.3% vs 50%; RR 0.5; 95% CI 0.2
to 0.9), and diarrhea (3.3% vs 26.6%; RR 0.1; 95% CI 0.1
to 0.9); however, epigastric pain (33.3% vs 30%; RR 1.1;
95% CI 0.5 to 2.3) did not significantly improve during
eradication treatment. These effects were not seen during
the week following the completion of antibiotic therapy.
Eradication rates did not differ significantly between the
groups (83.3% vs 80%).
In the second trial, 97 individuals were randomized to
receive Lactobacillus GG, Saccharomyces boulardii, Lactobacillus acidophilus, Bifidobacterium lactis, or placebo
on days 1-14, with H. pylori treatment on days 1-7.13 Probiotics significantly improved symptoms, including taste disturbance (RR 0.15; 95% CI 0.05 to 0.46; p = 0.0027) and
diarrhea (RR 0.16; 95% CI 0.04 to 0.56; p = 0.018); however, nausea (p = 0.75) and epigastric pain (p = 0.7) did not
significantly improve during H. pylori treatment. These effects were seen during the treatment week and were not
maintained following the completion of antibiotic therapy.
All of the differences were noted between the probiotics
and placebo. None of the probiotics was superior to another. Eradication rates were not significantly different among
the 4 groups receiving probiotics.
In the third trial 47 patients were studied using a milkbased fruit drink containing Lactobacillus GG, Propionibacterium, Bifidobacterium, or placebo on days 1-28 and
triple antibiotic therapy days 1-7.14 Probiotics did not significantly improve symptoms, including nausea (13% vs
21%; mean difference 8%; 95% CI 32 to 16), taste disturbance (70% vs 67%; mean difference 3%; 95% CI 24
to 30), diarrhea (17% vs 8%; mean difference 9%; 95% CI
12 to 32), and epigastric pain (17% vs 29%; mean difference 12%; 95% CI 36 to 14). Eradication rates did not

Table 1. First-Line Regimens for Helicobacter pylori Eradication3


Regimen

Medications

Duration
(days)

Eradication
Rates

Triple therapy (clarithromycin-based)

Proton pump inhibitora


Clarithromycin 500 mg po bid
Amoxicillin 1000 mg po bid or metronidazole 500 mg po bid

10-14

70-85%

Quadruple therapy (bismuth-based)

Proton pump inhibitor or ranitidine 150 mg po bid


Bismuth subsalicylate 525 mg po qid
Metronidazole 250 mg po qid
Tetracycline 500 mg po qid

10-14

75-90%

Alternative therapy not validated in the US

First 5 days:
proton pump inhibitor
amoxicillin 1000 mg po bid
Last 5 days:
proton pump inhibitor
clarithromycin 500 mg bid
tinidazole 500 mg bid

10

>90%

Standard doses for proton pump inhibitors are as follows: esomeprazole 40 mg/day po, lansoprazole 30 mg po bid, omeprazole 20 mg po bid, pantoprazole 40 mg po bid, rabeprazole 20 mg po bid.

theannals.com

The Annals of Pharmacotherapy

2011 July/August, Volume 45

Copyrighted material. Reproduo proibida.

961

962

The Annals of Pharmacotherapy

Copyrighted material. Reproduo proibida.

2011 July/August, Volume 45

UBT

Lansoprazole 30 mg bid,
clarithromycin 500 mg bid,
amoxicillin 1 g bid days
1-7

Rabeprazole 20 mg bid,
clarithromycin 500 mg bid,
amoxicillin 1 g bid days
1-7

Bacillus clausii 2 109


cfu/mL tid days 1-14
(Enterogermina, SanofiSynthelabo OTC, Milan,
Italy)

Rabeprazole 20 mg bid,
clarithromycin 500 mg
bid, tinidazole 500 mg bid
days 1-7

Rabeprazole 20 mg bid,
clarithromycin 500 mg bid,
tinidazole 500 mg bid
days 1-7

Regimen

Lactobacillus GG,
Propionibacterium
freudenreichii ssp.
shermanii, L. rhamnosus,
Bifidobacterium breve
1 109 cfu/mL bid for 7
days, then daily for 21
days (milk-based fruit
drink; Valio Ltd., Helsinki,
Finland)

Group 1:
Lactobacillus GG bid
(Giflorex, Errekappa
Euroterapici S.p.A,
Milan, Italy)
Group 2:
Sacchromyces boulardii
bid (Codex, Smith Kline
Beecham, Milan, Italy)
Group 3:
Lactobacillus acidophilus
and Bifidobacterium
lactis bid (Ferzym,
Specchiasol, Milan, Italy)
Group 4: placebo bid
All groups given treatment
on days 1-14

Lactobacillus GG 6 109
cfu/mL bid days 1-14
(Giflorex, Errekappa
Euroterapici S.p.A,
Milan, Italy)

Antibiotic
Regimen

ITT = intention to treat; NS = not significant; UBT = 13C-urea breath test.

N = 114
M/F: 55/59
Mean age:
treatment group
46 y,
placebo group
43 y
H. pylori positive,
asymptomatic

Nista
(2004)15

UBT

Serology; UBT

N = 97
M/F: 43/54
Mean age: not
provided
H. pylori positive,
healthy,
asymptomatic

Cremonini
(2002)13

UBT, serology

Probiotic
Methods

Myllyluoma N = 47
(2005)14
M/F: 18/29
Mean age: 55.6 y
H. pylori positive,
healthy,
asymptomatic

N = 60
M/F: 25/35
Mean age: 40 y
H. pylori positive,
healthy,
asymptomatic

Diagnostic
Patients

Armuzzi
(2001)12

Author

Primary: antibioticassociated adverse


effects and treatment
tolerability
Secondary: eradication
rate

Primary: antibioticassociated adverse


effects and treatment
tolerability
Secondary: eradication
rate

Primary: antibioticassociated adverse


effects and treatment
tolerability
Secondary: eradication
rate

Primary: antibioticassociated adverse


effects and treatment
tolerability
Secondary: eradication
rate

Measurement
Outcomes

Side effect diary/


questionnaire;
vial count; UBT
(at 6 wk)

Questionnaire;
tablet count;
UBT (at 4 wk);
serology (at 4 mo)

Questionnaire;
tablet count;
UBT (at 5-7 wk)

Questionnaire;
tablet count;
UBT (at 6 wk)

Tools

Results
(Probiotic vs Control)

Symptoms (ITT): nausea (25.9% vs 50%; RR


0.519, 95% CI 0.31 to 0.88), diarrhea (9.3% vs
30.8%; RR 0.301, 95% CI 0.12 to 0.76),
epigastric pain (44.4% vs 65.4%; RR 0.68, 95%
CI 0.48 to 0.97)
Adherence: not reported
Eradication: 72.2% vs 71.15% (p = NS)

Symptoms: no significant difference in any


adverse effects
Adherence: not reported
Eradication: 91% vs 79% (p = 0.42)

Symptoms:
During treatmenttaste disturbance (Group 1 =
9.5%, Group 2 = 5%, Group 3 = 5%, Group 4 =
40%; RR 0.15, 95% CI 0.05 to 0.46); diarrhea
(Group 1 = 5%, Group 2 = 5%, Group 3 = 5%,
Group 4 = 30%; RR 0.16, 95% CI 0.04 to 0.56)
Following treatmentno significant difference
between groups
Adherence: not reported
Eradication: Group 1 = 76%, Group 2 = 81%,
Group 3 = 86%, Group 4 = 80% (p = NS)

Symptoms:
During treatmentnausea (10% vs 36.6%; RR
0.3, 95% CI 0.1 to 0.9); taste disturbance
(23.3% vs 50%; RR 0.5, 95% CI 0.2 to 0.9);
diarrhea (3.3% vs 26.6%; RR 0.1, 95% CI 0.1
to 0.9)
Following treatmentno significant difference
between groups
Adherence: 100%
Eradication: 83.3% vs 80% (p = NS)

Table 2. Randomized, Double-Blind, Placebo-Controlled Trials of Probiotics Plus Eradication Therapy for
Helicobacter pylori Infections12-15

SM Wilhelm et al.

theannals.com

Probiotics as Adjunctive Therapy for H. pylori

significantly differ between the groups (91% vs 79%; p =


0.42).
In an intention-to-treat analysis in the fourth trial, 114
patients were administered B. clausii or placebo on days 114 and triple antibiotic therapy on days 1-7.15 The probiotic
improved nausea (25.9% vs 50%; RR 0.519; 95% CI 0.31
to 0.88), diarrhea (9.3% vs 30.8%; RR 0.301; 95% CI 0.12
to 0.76), and epigastric pain (44.4% vs 65.4%; RR 0.68;
95% CI 0.48 to 0.97); however, it had no effect on taste
disturbance (53.7% vs 59.6%; RR 0.901; 95% CI 0.65 to
1.26) during the first week while patients were receiving
antibiotic therapy. The probiotic continued to improve nausea during week 2 (14.8% vs 32.7%; RR 0.453; 95% CI
0.21 to 0.96). However, this probiotic did not improve
eradication rates (72.2% vs 71.15%; p = NS).
Discussion
The majority of the studies on probiotic therapy during H.
pylori eradication did not have strong designs. To evaluate
the most robust data, only randomized, double-blind, placebo-controlled trials of probiotics and H. pylori eradication
therapy were included in this review. In 3 of the 4 trials, probiotics increased tolerability and reduced adverse effects, particularly nausea, taste disturbance, diarrhea, and epigastric
pain, of H. pylori eradication therapy.12,13,15 This was true of a
variety of probiotic strains such as Lactobacillus spp., Sacchromyces spp., Bifidobacterium spp., and B. clausii. One trial did not find a reduction in adverse effects; however, it was
the smallest of the 4 trials and the only one to use a milkbased probiotic supplement.14 Probiotics did not appear to
have an effect on the eradication rates in any of the 4 trials.
Strengths of the 4 trials consist of the use of objective
data such as the urea breath test and serologic assays such
as the enzyme-linked immunosorbent assay to diagnose H.
pylori in healthy, asymptomatic study subjects. The urea
breath test has an excellent positive and negative predictive
value, regardless of H. pylori prevalence. Although quantitative antibody testing has very good negative predictive
value, the positive predictive value depends on H. pylori
prevalence, and is not recommended for use after therapy.
The urea breath test and serology were used to confirm
eradication between 4 and 7 weeks after eradication therapy, which adds a limitation to the trials with the use of
serologic assays after treatment, but are still considered
valid objective measurements in clinical trials. The first trial used specific and detailed questionnaires to assess symptoms, and patients were also provided verbal and printed
instructions on filling in the questionnaires.12 This most
likely led to increased questionnaire adherence and reliability of the adverse effect data. The second trial included
asymptomatic subjects and used a mandatory run-in period
to prevent a confounding factor of previous gastrointestinal
symptoms.13 Myllyluoma and colleagues used fecal recovtheannals.com

ery of Lactobacillus and Propionibacterium to show adherence in the treatment group and probiotic abstinence in
the placebo group.14 The first and fourth trials analyzed
symptoms individually, and categorized them weekly.12,15
This provided specific information regarding adverse
events and effective timing of probiotics.
Even though these are well-designed trials, they do have
limitations. They used differing eradication regimens. Two
of the trials12,13 used a tinidazole-based regimen, which is
not considered first-line therapy in the US.3 All 4 trials
used a 7-day eradication regimen, which is shorter than the
recommended 10- to 14-day regimens3; this may have had
an effect on eradication rates and tolerability. Small sample
sizes further limited the studies. In addition, subjects completed questionnaires and symptom diaries to report adverse effects and treatment tolerability, which may have
skewed the results because of the subjective nature of adverse effect reporting, and the inevitable variability in patient response to adverse effects. While all 4 trials assessed
adherence, rates were not reported. This may be an issue
because of the high pill burden of H. pylori eradication
therapy with additional probiotic doses. One trial included
participants from a group of educated health-care
providers, which does not necessarily represent the population most affected by H. pylori disease.12 Adverse effects
might be tolerated differently in this population, and the diets of the participants may be more rich in fruits, vegetables, and dairy compared to subjects in other trials. None
of the studies controlled for subjects intake of dietary probiotics such as yogurt or other probiotic supplements. It is
unclear whether any geographic differences existed, since
the 3 trials that showed improvement in tolerability were
conducted in Italy,12,13,15 whereas the fourth trial was conducted in Finland.14 Finally, all trials used different probiotics.
Conflicting evidence exists regarding the efficacy of
probiotics for the reduction of adverse effects and increase
in tolerability of H. pylori eradication therapies. Some trials indicate that probiotics are effective for reducing adverse effects and increasing eradication rates of H. pylori
therapy.16,17 Other trials showed increased eradication rates,
with increases or no change in adverse effects.18,19 While
some trials report probiotics have no effect on adverse effects or eradication rates,20,21 others report that probiotics
reduce adverse effects without affecting eradication rates.22
Probiotics may have a role as adjunctive therapy for H.
pylori eradication. They have been shown to improve gastrointestinal adverse effects such as nausea, taste disturbance, diarrhea, and epigastric discomfort. By reducing the
adverse effects, patients may adhere to H. pylori eradication therapy, thereby increasing eradication rates. This is
supported by a study that showed the use of a yogurt probiotic preparation resulted in a higher completion rate than
eradication therapy alone.17 An increase in the eradication

The Annals of Pharmacotherapy

2011 July/August, Volume 45

Copyrighted material. Reproduo proibida.

963

SM Wilhelm et al.

rate of H. pylori during antibiotic therapy may decrease the


chance of recurrence and may result in reduced bacterial
resistance.
Probiotics are not often used as adjunctive therapy for
patients with H. pylori infections. This provides the pharmacist with an important role in discussing the option of
probiotic use in combination with H. pylori eradication
therapy. A pharmacist should, however, take into account
the economic burden of these products before recommending them. A typical regimen of probiotics would begin in
conjunction with the H. pylori eradication therapy and may
be continued for a week following completion of the eradication therapy. Many probiotics are readily available in the
community, and choosing an appropriate product could be
an important factor in treating the patient. Unfortunately,
the products used in these studies are not typically sold in
the US, which makes selecting a probiotic supported by
evidence difficult. Even though a specific strain of Lactobacillus supported by evidence may not be available in the
US, it may be reasonable to extrapolate the effects of that
strain to other types of Lactobacillus when product selections are limited. Table 3 contains a noninclusive list of
probiotic preparations available in the US.
Probiotics are most commonly recommended for use on
an outpatient basis to healthy patients without many comorbid conditions. This population represents most of the
patients in the clinical trials that were reviewed. Probiotics
are freely used because of their dietary supplement status,
which limits the amount of safety data reported, and also because of their perceived lack of serious complications. However, there have been case reports of fungemias caused by
Saccharomyces cerevisiae and S. boulardii with and without
probiotic supplementation.23 Patients who acquire invasive
Saccharomyces infections have at least one risk factor, including intravenous catheter use, intensive care unit hospital-

ization, and immunocompromised status. There have been


other case reports linking Lactobacillus spp. and Bacillus
subtilis to invasive bacterial infections in patients taking probiotic supplements.24-26 This is contradictory to clinical trials
showing Lactobacillus to be safe for use in immunocompromised populations, but is still an alarming finding. This may
be important to consider when recommending probiotics to
patients who might be at a higher risk of acquiring bloodborne infections, especially the immunocompromised or patients with central catheters.
Summary
Probiotics may be beneficial in reducing adverse effects
and increasing tolerability of H. pylori eradication regimens. They may especially be helpful in patients with recurrent H. pylori and history of gastrointestinal adverse effects with antibiotics. Pharmacists can play an important
role in educating their patients regarding probiotic use during H. pylori eradication therapy.
Sheila M Wilhelm PharmD BCPS, Assistant Professor, Wayne
State University, and Harper University Hospital, Detroit, MI
Jennifer L Johnson PharmD, PGY 1 Resident, Harper University
Hospital
Pramodini B Kale-Pradhan PharmD, Associate Professor, Wayne
State University; and St. John Hospital and Medical Center, Detroit,
MI
Correspondence: Dr. Kale-Pradhan, pkale@wayne.edu
Reprints/Online Access: www.theannals.com/cgi/reprint/aph.1Q104

Conflict of interest: Authors reported none

References
1. Valle JD. Peptic ulcer disease and related disorders. In: Fauci AS, Braunwald E, Kasper DL, et al., eds. Harrisons principles of internal medicine.
17th ed. New York, NY: McGraw-Hill Companies, Inc., 2008:1855-71.

Table 3. Noninclusive List of Available Probiotics in the US


Product

Manufacturer

Probiotic

CFU

Cost
(US $)

Capsules
(n)

Align

Procter and Gamble

Bifidobacterium infantis 35624 (bifantis)

1 109

27.99

28

Culturelle

Amerifit Brands

Lactobacillus GG, inulin

1 1010

24.99

30

Flora Q

Kenwood Therapeutics

Lactobacillus acidophilus
Bifidobacterium
Lactobacillus paracasei
Streptococcus hermophilus

Not stated

29.99

30

Floranex

Rising

L. acidophilus
Lactobacillus bulgaricus

2 106

11.99

50

Florastor

Biocodex

Saccharomyces boulardii

Not stated

46.99
11.99

50
10

Lactinex (refrigerated)

Becton, Dickinson, and Co.

L. acidophilus
L. bulgaricus

1 108

13.99

12 (packets)

Phillips Colon Health

Bayer

L. acidophilus
Bifidobacterium bifidum
Bifidobacterium longum

1.5 109

15.99

30

Systenex

Ganeden Biotech

Bacillus coagulans (GanedenBC)

2 109

16.99

30

964

The Annals of Pharmacotherapy

2011 July/August, Volume 45

Copyrighted material. Reproduo proibida.

theannals.com

Probiotics as Adjunctive Therapy for H. pylori


2. Barkun A, Leontiadis G. Systematic review of the symptom burden,
quality of life impairment and costs associated with peptic ulcer disease.
Am J Med 2010;123:358-66.e2.
3. Chey WD, Wong BC. American College of Gastroenterology guideline
on the management of Helicobacter pylori infection. Am J Gastroenterol
2007;102:1808-25.
4. Jarosz M, Rychlik E, Siuba M, et al. Dietary and socio-economic factors
in relation to Helicobacter pylori re-infection. World J Gastroenterol
2009;15:1119-25.
5. Starzynska T, Malfertheiner P. Helicobacter and digestive malignancies.
Helicobacter 2006;11(suppl 1):32-5.
6. Rauws EA, Tytgat GN. Cure of duodenal ulcer associated with eradication of Helicobacter pylori. Lancet 1990;335:1233-5.
7. Gotteland M, Brunser O, Cruchet S. Systematic review: are probiotics
useful in controlling gastric colonization by Helicobacter pylori? Aliment Pharmacol Ther 2006;23:1077-86.
8. Tong JL, Ran ZH, Shen J, Zhang CX, Xiao SD. Meta-analysis: the effect
of supplementation with probiotics on eradication rates and adverse
events during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 2007;25:155-68.
9. Cremonini F, Di Caro S, Nista EC, et al. Meta-analysis: the effect of probiotic administration on antibiotic-associated diarrhoea. Aliment Pharmacol Ther 2002;16:1461-7.
10. Kale-Pradhan PB, Jassal HK, Wilhelm SM. Role of Lactobacillus in the
prevention of antibiotic-associated diarrhea: a meta-analysis. Pharmacotherapy 2010;30:119-26.
11. McFarland LV. Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease.
Am J Gastroenterol 2006;101:812-22.
12. Armuzzi A, Cremonini F, Bartolozzi F, et al. The effect of oral administration of Lactobacillus GG on antibiotic-associated gastrointestinal sideeffects during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 2001;15:163-9.
13. Cremonini F, Di Caro S, Covino M, et al. Effect of different probiotic
preparations on antiHelicobacter pylori therapyrelated side effects: a
parallel group, triple blind, placebo-controlled study. Am J Gastroenterol
2002;97:2744-9.
14. Myllyluoma E, Veijola L, Ahlroos T, et al. Probiotic supplementation improves tolerance to Helicobacter pylori eradication therapya placebocontrolled, double-blind randomized pilot study. Aliment Pharmacol
Ther 2005;21:1263-72.
15. Nista EC, Candelli M, Cremonini F, et al. Bacillus clausii therapy to reduce side-effects of antiHelicobacter pylori treatment: randomized,
double-blind, placebo controlled trial. Aliment Pharmacol Ther 2004;20:
1181-8.
16. Sheu BS, Cheng HC, Kao AW, et al. Pretreatment with Lactobacillusand Bifidobacterium-containing yogurt can improve the efficacy of
quadruple therapy in eradicating residual Helicobacter pylori infection
after failed triple therapy. Am J Clin Nutr 2006;83:864-9.
17. Sheu BS, Wu JJ, Lo CY, et al. Impact of supplement with Lactobacillusand Bifidobacterium-containing yogurt on triple therapy for Helicobacter
pylori eradication. Aliment Pharmacol Ther 2002;16:1669-75.
18. Canducci F, Armuzzi A, Cremonini F, et al. A lyophilized and inactivated culture of Lactobacillus acidophilus increases Helicobacter pylori
eradication rates. Aliment Pharmacol Ther 2000;14:1625-9.
19. Kim MN, Kim N, Lee SH, et al. The effects of probiotics on PPI-triple
therapy for Helicobacter pylori eradication. Helicobacter 2008;13:261-8.
20. Cindoruk M, Erkan G, Karakan T, Dursun A, Unal S. Efficacy and safety
of Saccharomyces boulardii in the 14-day triple antiHelicobacter pylori
therapy: a prospective randomized placebo-controlled double-blind
study. Helicobacter 2007;12:309-16.
21. Szajewska H, Albrecht P, Topczewska-Cabanek A. Randomized, doubleblind, placebo-controlled trial: effect of Lactobacillus GG supplementation on Helicobacter pylori eradication rates and side effects during treatment in children. J Pediatr Gastroenterol Nutr 2009;48:431-6.
22. Hurduc V, Plesca D, Dragomir D, Sajin M, Vandenplas Y. A randomized,
open trial evaluating the effect of Saccharomyces boulardii on the eradi-

theannals.com

23.
24.
25.

26.

cation rate of Helicobacter pylori infection in children. Acta Paediatr


2009;98:127-31.
Enache-Angoulvant A, Hennequin C. Invasive Saccharomyces infection:
a comprehensive review. Clin Infect Dis 2005;41:1559-68.
Boyle RJ, Robins-Browne RM, Tang ML. Probiotic use in clinical practice: what are the risks? Am J Clin Nutr 2006;83:1256-64; quiz 446-7.
Salminen MK, Tynkkynen S, Rautelin H, et al. The efficacy and safety of
probiotic Lactobacillus rhamnosus GG on prolonged, noninfectious diarrhea in HIV patients on antiretroviral therapy: a randomized, placebocontrolled, crossover study. HIV Clin Trials 2004;5:183-91.
Wolf BW, Wheeler KB, Ataya DG, Garleb KA. Safety and tolerance of
Lactobacillus reuteri supplementation to a population infected with the
human immunodeficiency virus. Food Chem Toxicol 1998;36:1085-94.

El rol de los Probiticos Como Terapia Adyuvante Para


Helicobacter pylori
SM Wilhelm, JL Johnson, y PB Kale-Pradhan
Ann Pharmacother 2011;45:960-6.
EXTRACTO

Revisar la literatura concerniente al rol de los agentes


probiticos en el tratamiento de infecciones con Helicobacter pylori
(HP).
FUENTE DE DATOS: Se realiz una bsqueda de la literatura en la base de
datos MEDLINE (1966marzo 2011) utilizando los trminos
Helicobacter pylori, probitico, Lactobacillus, Bifidobacterium,
Saccharomyces, Bacillus clausii, y Propionibacterium. Se revisaron las
referencias para identificar artculos y extractos relevantes adicionales.
SELECCIN DE ESTUDIOS Y EXTRACCIN DE DATOS: Se evaluaron todos los
artculos publicados en el idioma ingls. En la revisin se incluy
estudios aleatorios, doble ciegos, controlados con placebo que evaluaron
el uso de probiticos combinados con tratamientos estandarizados para
erradicacin de HP.
SNTESIS DE DATOS: Este artculo repasa la evidencia relacionada con el
uso de probiticos como terapia adyuvante para HP. Varios probiticos,
incluyendo Lactobacillus spp, Saccharomyces spp., Bifidobacterium
spp., y Bacillus clausii reducen efectos adversos tales como nusea,
alteracin del sentido del gusto, diarrea y dolor epigstrico y aumenta la
tolerancia a los tratamientos para erradicar HP. Segn los estudios
revisados, los probiticos no alteran la tasa de erradicacin de HP.
CONCLUSIONES: Los probiticos pueden ser de beneficio en el tratamiento
para erradicar HP al reducir los efectos adversos y aumentar la tolerancia
al tratamiento. Los probiticos pueden ser considerados para pacientes
que estn recibiendo tratamiento para erradicar HP y para pacientes con
HP recurrente e historial de efectos adversos relacionados al tratamiento
con antibiticos. Los farmacuticos pueden jugar un papel importante en
la educacin de pacientes en el uso de probiticos durante la terapia de
erradicacin de HP.
OBJETIVO:

Traducido por Astrid J Garca-Ortiz

Traiter les Bactries par des Bactries: Le Rle des Probiotiques


Comme Traitement Adjuvant de lHlicobacter pylori
SM Wilhelm, JL Johnson, y PB Kale-Pradhan
Ann Pharmacother 2011;45:960-6.
RSUM

Revoir la documentation scientifique sur le rle des


probiotiques pour le traitement des infections Hlicobacter pylori
(HP).
SOURCES DE DONNES: La recherche de la documentation scientifique a
t effectue par le biais de MEDLINE (1966-Mars 2011) avec les
OBJECTIF:

The Annals of Pharmacotherapy

2011 July/August, Volume 45

Copyrighted material. Reproduo proibida.

965

SM Wilhelm et al.

termes Hlicobacter pylori, probiotique, Lactobacillus, Bifidobacterium,


Saccharomyces, Bacillus clausii, et Propionibacterium. Les articles de
rfrences ont t revus afin de dceler dautres articles et rsums
pertinents.
SLECTION DES TUDES ET EXTRACTION DES DONNES: Tous les articles
publis de langue anglaise ont t valus. Les tudes randomises,
double insu avec un contrle placebo valuant lutilisation de
probiotiques combins un traitement standard pour lradication de
linfection HP chez les adultes ont t inclues dans la revue.
SYNTHSE DES DONNES: Cette article revoit les donnes concernant
lutilisation des probiotiques pour le traitement adjuvant du HP. Une
varit de probiotiques incluant Lactobacillus spp., Saccharomyces ssp., et
Bacillus clausii reduisent les effets indsirables tels que les nauses,
laltration du got, les diarrhes et la douleur gastrique et amliore la

tolrance au traitement pour lradication du HP. Selon les tudes rvises,


les probiotiques ne compromettent pas les taux dradication du HP.
CONCLUSIONS: Lutilisation des probiotiques pourrait tre bnfique pour
rduire les effets indsirables et augmenter la tolrance au traitement lors
de lutilisation de traitements pour radiquer le HP. Les probiotiques
pourraient tre considrs pour lemploi lorsque les patients utilisent un
traitement pour radiquer le HP. Les probiotiques pourraient tre utiles
spcialement chez les patients qui ont une histoire de rcurrence
dinfection HP et des effets indsirables documents avec les
antibiotiques. Les pharmaciens pourraient jouer un rle important dans
lducation de ces patients concernant lutilisation de probiotiques
durant leur traitement pour liminer le HP.
Traduit par Chantal Guvremont

Articles published in The Annals


Are posted in The Annals Online and indexed in PubMed weeks before appearing in print.
Appear on the prestigious HighWire Press platform at Stanford University, host to the most
frequently cited journals.
Permit readers to access citations to other HighWire journals through free full-text access links.
Receive extensive peer review and contribute to The Annals high journal impact factor.

Authors publishing in The Annals realize these additional benefits


Quick and easy online manuscript submission for faster turnaround.
No submission fees or page charges.
And more: visit www.theannals.com and select Author Information.

966

The Annals of Pharmacotherapy

2011 July/August, Volume 45

Copyrighted material. Reproduo proibida.

theannals.com

You might also like