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Recommendations for Probiotic Use2008

Martin H. Floch, MD,* W. Allan Walker, MD,wStefano Guandalini, MD,z

Patricia Hibberd, MD,ySherwood Gorbach, MD,J Christina Surawicz, MD,zMary Ellen Sanders, PhD,# Guadalupe Garcia-Tsao, MD,* Eamonn M. M. Quigley, MD, **

Erika Isolauri, MD, PhD, w wRichard N. Fedorak, MD,zzand Levinus A. Dieleman, MD, PhDzz

Abstract: Recommendations for the clinical use of probiotics

were published after a Yale University Workshop in 2005.

A similar workshop was held in 2007, and the recommendations

were updated and extended into other areas. The recommenda-

tions are graded into an A, B, C or no category based on

the experts opinion and review by the workshop participants.

An A recommendation is made for acute childhood diarrhea,prevention of antibiotic-associated diarrhea, preventing and

maintaining remission in pouchitis, and in an immune response

for the treatment and prevention of atopic eczema associated

with cows milk allergy. The group maintained several B

recommendations in other areas of treating inflammatory bowel

disease and irritable bowel syndrome. Although there are

significant studies in the B group, most B recommendations

did not reach an A level because of some negative studies or

a limited number of studies. Many reports in the C

recommendations were significant but fell short of receiving

stronger ratings because of the size of reported patient studies,

and also the factors that limited categories to the B rating.

Key Words: probiotics, recommendations, diarrhea, antibiotic-associated diarrhea, pouchitis, immune response, atopic eczema,

inflammatory bowel disease, irritable bowel syndrome

(J Clin Gastroenterol2008;42:S104S108)

These recommendations are made on evidence pre-sented at the Advances in Clinical Use of ProbioticsWorkshop that was held at Yale University on November16, 2007. This is the second workshop on this topic.The first workshop resulted in the publication of the 2005Recommendations for Probiotic Use.1 The recommenda-tions presented here are an update of the 2005 recom-

mendations and an extension into other areas of clinicaluse.

All of the authors of this manuscript had anopportunity to review these recommendations, whichare a result of an open discussion that occurred at theworkshop, and the manuscripts that are presented in thissupplement.

These recommendations carry with them certaincaveats:1. Specific recommendations made for clinical use are

referenced to a manuscript that describes the probioticused, the dose of the probiotic strain or strains used,and the vehicle in which it was delivered. We caution

that the recommendations are based on thosereferenced results and cannot be extrapolated to theuse of other products. The references are specific.Clinicians may want to use a similar probiotic butshould do that with the understanding that thereported result is based on the probiotic and the wayit was used as cited in the reference. It is emphasizedthat the probiotic upon which a recommendation isbased are for specific strains of organisms and specificproducts used in the referenced work.

2. The dose and method of administration are important.If a recommendation is to be followed, it is for the dosethat was used in the reference.

3. On the basis of the most recent literature, it is stronglyrecommended that probiotics be used with cautionand appropriate monitoring in immunocompromisedpatients.

USE IN SPECIFIC CONDITIONSTable 1 outlines guidelines for probiotic use. It is

updated in this manuscript from the previous report.1

The recommendations for these guidelines are based onthe discussions at the workshop and the literature.

An A recommendation is based on strong,positive, well-conducted, controlled studies in the primaryliterature, not abstract form.Copyright r 2008 by Lippincott Williams & Wilkins

Received for publication January 31, 2008; accepted January 31, 2008.From the *Section of Digestive Diseases, Yale University School of

Medicine, New Haven, CT; wPediatric Gastroenterology andNutrition Unit, Harvard Medical School, Mass General Hospitalfor Children; yPediatric and Public Health; JDivision of Nutritionand Infection, Tufts University School of Medicine, Boston, MA;zDepartment of Pediatrics, University of Chicago Comer ChildrensHospital, Chicago, IL; zDivision of Gastroenterology, University of

Washington, Seattle, WA; #Dairy and Food Culture Technologies,Centennial, CO; **Alimentary Pharmabiotic Centre, NationalUniversity of Ireland, Cork, Ireland; wwDepartment of Pediatrics,University of Turku, Turku, Finland; and zzDivision of Gastro-enterology, University of Alberta, Alberta, Canada.

The authors declare no conflict of interest.No funding for any authors. Quigley is a consultant for Procter &

Gamble; Fedorak is a consultant to Biocodex and Procter & Gamble;Sanders is a consultant for Yakult and The Dannon Company; Flochis a consultant for Procter & Gamble and The Dannon Company;Surawicz is on the speakers bureau for Biocodex.

Reprints: Martin H. Floch, MD, Section of Digestive Diseases,Yale University School of Medicine, 333 Cedar Street, 1080 LMP,PO Box 208019, New Haven, CT 06520-8019 (e-mail: [email protected]).

PRESENTATION

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A B recommendation is based on positive, con-trolled studies but the presence of some negative studies.

A C recommendation is based on some positivestudies but clearly inadequate amount of work to esta-

blish the certainty of A or B.

DIARRHEA

Treatment of Nonantibiotic-associated Diarrheaof Children and Adults

The recommendations at this workshop wereessentially the same as the previous recommendations.Probiotics are helpful in acute childhood diarrhea andgiven an A recommendation.

The organisms that seem to be effective, consideringthe treatments throughout the world, are referenced

Saccharomyces boulardii,2 Lactobacillus GG (LGG),3,5,6Lactobacillus reuteri7 and a variety of mixtures, includingLactobacillus acidophilus.4 The references are for thedoses and the specific strains used at the onset of diarrhea.There is an approximately 24 to 30 hours reduction inthe illness.

Only a B recommendation is given for preventionof sporadic, infectious diarrhea. In fact, although allprobiotics tested were found to be completely safe, theevidence of their efficacy in preventing diarrheal episodesin infants and children attending daycare centers or beinghospitalized for reasons other than diarrhea3 is onlymodest statistically significant for some strains only, and

in any case of questionable clinical importance. However,this is most definitely an area worth further exploration.

Antibiotic-associated DiarrheaAntibiotic-associated Diarrhea (not due toClostridium difficile)

An A recommendation is given for prevention inambulatory and hospitalized adult patients.

LGG10,11 and S. boulardii5658 are effective. Thereare good studies for both inpatients and outpatients. Arecent meta-analysis on 10 randomized-controlled clinicaltrials59 confirms the efficacy of LGG and S. boulardii inthe prevention of antibiotic-associated diarrhea in chil-dren. One recent study did show a combination of L.casei, L. bulgaricus and S. thermophilus was effective in adrink given twice per day.8

C. difficile-associated DiarrheaThere are conflicting opinions on whether probio-

tics have any role in prevention ofC. difficile-associateddiarrhea (CDAD) or treatment of initial or severeepisodes of CDAD.

The specific initial treatment ofC. difficile diarrheais one of the antibiotic treatments of the C. difficile.As many as one-third of the patients will relapse aftertreatment and persistentC. difficile can be demonstrated.In these cases, probiotics become important as anadjuvant in the treatment. For this purpose, eitherS. boulardii9,5961 or LGG10,12 are effective.

TABLE 1. Recommendations for Probiotic Use

Clinical Condition Effectiveness Organism References

DiarrheaInfectious adulttreatment A Saccharomyces boulardii, LGG 24Infectious childhoodtreatment A LGG, Lactobacillus reuteri 47Prevention of infection B S. boulardii,LGG 3

Prevention of AAD A S. boulardii,LGG, L. casei, L. bulgaricus, S. thermophilus 8, 9Treatment of recurrent CDAD B S. boulardii,LGG 8, 9Prevention of CDAD B LGG, S. boulardii 812

IBDPouchitis

Preventing and maintaining remission A VSL#3 1315Induce remission C VSL#3 16

Ulcerative colitisInducing remission C Escherichia coliNissle, VSL#3 1719Maintenance C E. coliNissle, VSL#3 2022

Crohns C E. coliNissle, S. boulardii, LGG 2326IBS B Bifidobacterium infantis 2729

C Bifidobacterium animalis, VSL#3,Lactobacillus plantarum

3034

Immune response A LGG, Lactobacillus acidophilus, L. plantarum,Bifidobacterium lactis, Lactobacillus johnsonii

35, 36

AllergyAtopic eczema associated with cows milkallergy

Treatment A LGG, B. lactis 3743Prevention A LGG, B. lactis 4448

Radiation enteritis C VSL#3, L. acidophilus 4952Vaginosis and vaginitis C L. acidophilus,LGG, L. reuteri 5355

AAD indicates antibiotic-associated diarrhea; IBD, inflammatory bowel disease; IBS, irritable bowel syndrome; CDAD,Clostridium difficile-associated diarrhea; LGG,LactobacillusGG.

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The evidence on using probiotics for prevention orrecurrent CDAD is debated. However, meta-analysisdoes reveal positive data using either LGG orS. boulardii.8,9 Therefore, it is given a B recommenda-tion for prevention and as adjuvant therapy.

It was further noted in the presentations that fecal

transplant bacteria therapy has anecdotally and in smallstudies reported as effective in many centers. Norecommendation is made at this time for fecal transplant,but it must be noted that several centers have reported itas effective in resistant cases.8,6264

INFLAMMATORY BOWEL DISEASE POUCHITIS

Pouchitis

Maintenance of RemissionAn A recommendation continues for the main-

tenance of remission of pouchitis in ileal-pouch-anal-anastomosis, either after induction of remission with

antibiotic therapy or immediately after surgical formationof the pouch. VSL#3 is the probiotic mixture that hasbeen reported as effective in the literature. Use anddosage are as recommended in the specific references.1315

Induction of RemissionThere is a level C recommendation for induction

of remission of pouchitis given a recently published open-label study that demonstrated that high dose VLS#3 wasable to induce remission of active pouchitis.16

Ulcerative Colitis

Maintenance of Remission

The workshop panel felt that there was Cevidence for maintenance of remission using EscherichiacoliNissle, in that the 2 large randomized-controlled trialshave demonstrated that E. coliNissle had similar efficacyto that of mesalamine. Because of the 2 positive trials, thiscan be considered as a B17,18 but many felt there werenot strong enough published data in this controversialarea.

Induction of RemissionFor induction of remission, the workshop panel

agreed that a C recommendation remains because thetrials were limited to open-label studies. However, there isaccumulating evidence suggestive that it maybe helpful.

Both E. coli Nissle and VSL#3 hold promise as beinghelpful in acute ulcerative colitis, but random-controlledtrials in larger number of patients are still needed. E. coliNissle has been used both in induction17,18 and main-tenance of remission,20 whereas VSL#3 seemed effectivein inducing remission,19 as an adjuvant therapy,21 and inmaintaining remission.22

Crohns DiseaseThe recommendation for this remains at a C level

for both induction of remission and maintenance ofremission. Results are variable, studies are small, mostlyopen label, and there are not enough studies or with large

enough number of patients to make a definite recom-mendation.23

E. coliNissle,24 S. boulardii,25 andLGG26 have beenused with variable results.

IRRITABLE BOWEL SYNDROMEBecause of the high incidence of this syndrome,there is a great deal of interest. There are mixed opinionsof whether to leave this at a C level, because there aresome promising results that demonstrate a decrease insymptoms.27 On the basis of expert opinion, we havelisted it as both B and C for different probiotics.

Bifidobacterium infantis,28,29 Bifidobacterium ani-malis,30 and VSL#331,32 have shown to relieve symptomsin most recent studies. Older studies used Lactobacillusplantarum33,34 with some success but have not beenrepeated. Only B. infantis has been raised to a B levelbased on 2 large, random, controlled trials.2729

IMMUNE RESPONSE AND ALLERGY

Immune ResponseThe panel now feels that they can give this an A

recommendation. The evidence has accumulated andsubstantiated that the immune response is definitelyaffected by the administration of probiotics.35,36

Furthermore, it is now accepted in many areas ofthe world that probiotics are helpful in the treatmentof childhood allergy and eczema. The workshop paneldiscussed allergy for the first time. The all encompassingdata were presented.37 We now feel we can make an A

recommendation for the use of specific probiotics,particularly the strains of LGG and Bifidobacteriumlactis,in infants and children for the treatment of allergicdisorders with intestinal involvement, such as atopiceczema associated with cows milk allergy3843 and theirprevention.4448

OTHER DISEASES

Necrotizing EnterocolitisThis was reviewed in detail.49 There is not enough

information to make a recommendation. Studies havebeen small and used different probiotics in different

populations. However, the use of probiotics to prevententerocolitis is promising, and more information shouldbe forthcoming and should enable a recommendation infuture years.

Radiation EnteritisA C recommendation is made because there

are limited studies. However, the data in these studies areimpressive, but the number of subjects studied is small.More data are needed before the recommendation can beupgraded.

VSL#3 has been used effectively,50 and also thestrains ofL. acidophilus51,52 in those studies.

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Vaginitis and VaginosisThis was not specifically addressed at the con-

ference, but probiotics seem promising in the treatment ofvaginitis and vaginosis. The previously assigned categoryC recommendation stands, although the 2 recentcontrolled trials from Africa are impressive.

The organisms used have been LGG,53 L. reuteri,53,54andL. acidophilus.55

PREVENTION OF DISEASE IN HEALTHMAINTENANCE

In many societies of the world, probiotics andyogurts as foods are used to maintain health.65

The feeling is that this is such a broad area of studythat additional studies for the different end points(eg, duration of colds or absences from work) are neededso that specific recommendations can be made.

A variety of studies have been conducted with

probiotics which suggest that consuming them may helpkeep people healthy.66 L. reuteriATCC 55730 was shownto reduce absences from work or daycare, crying timein colicky babies, and episodes of fever and diarrhea ininfants with childcare.Lactobacillus caseiDN114-001 andLGG also improved resistance to illness in children indaycare settings. A combination probiotic (Bifidobac-terium longum, Bifidobacterium bifidum, Lactobacillusgasseri) tested in healthy adults showed a reduction induration, but not incidence, of colds. The likely mechan-isms for this effect include enhancement of immunefunction and direct inhibition of pathogens. Such findingssuggest that probiotics might be of value for incorpora-

tion into the daily diet of healthy people for the purposeof staying healthy. However, such a recommendation ismore of a dietary recommendation than a clinical one.This subject is complex and has many ramifications thatthe group felt prevented making a specific clinicalrecommendation at this time.65,66

SUMMARYUses of probiotic organisms are promising in main-

taining health and treating disease in humans. Table 1outlines our recommendations for their use. Each indicationis referenced. The reference should be consulted when a

probiotic is prescribed. The evidence reveals they areindicated in treatment of acute childhood diarrhea, preven-tion of antibiotic-associated diarrhea, pouchitis, to obtainan immune response, and in atopic dermatitis. Evidence israpidly accumulating that they maybe helpful in otherdisorders such as treatment ofC. difficile-associated colitis,radiation enteritis, ulcerative colitis, and irritable bowelsyndrome. Using probiotics for other indications includingmaintenance in health need to be reevaluated in the nextfew years. There is an urgent need for improvements in thequality of clinical trials to evaluate the safety and efficacyof specific probiotics before recommendations can beupgraded.

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