Prebiotics, Probiotics, and Synbiotics:

Functional Foods
"Y*ACQUELINE*7ESSEL-%D2$#.3$#30#,%,$

I
n the 1950s, my mother read books exist in the healthy gut.3 The colon AAD. Antibiotics affect the anaero-
about nutrition, by authors such as is a reservoir of large quantities; an bic component of fecal flora, which
Adele Davis, that espoused the con- adults large intestine has been esti- are considered to be responsible for
cept of functional foods. Functional mated to contain about 500 different protection against pathogenic prolif-
foods are those that have health benefits bacterial species,3 some beneficial eration. Beta-lactam antibiotics have
beyond that of their nutritional content. and others detrimental to health (see been found most often associated
My mother in her stylish, cinched-waist Table 1). with diarrhea.30
cotton dresses (and high heels) made To be classified as a probiotic, a bac- What about the possible role of
yogurt, which we all dutifully consumed terial strain must be of human origin, probiotics and necrotizing entero-
for our health. be safe for human use, have its ben- colitis (NEC)? Preterm infants have
The concept of functional foods is efits proven scientifically, be stable in delayed establishment of gut flora.31
now back. Prebiotics and probiotics contact with acid and bile, and adhere Probiotics have been shown to mod-
are functional foods, and synbiotics to intestinal mucosa.3,4 Probiotics have ify colonic flora in infants, including
are combinations of prebiotics and been shown in infants and children to VLBW infants.32 In the preterm rat
probiotics. The lining of the GI tract decrease the duration of acute infec- model, probiotics have been shown
is important in host defense the in- tious diarrhea,5-14 provide reasonable to reduce the rate of NEC.33 The
testinal mucosa is on the front line be- protection against antibiotic-associat- premature infant has an immature
tween the host and the outside world. ed diarrhea,15-23 and perhaps play a role immune system, lower gastric acid
Keeping the mucosa intact and healthy in prevention of food allergy in children production (the acid that could have
is therefore important. at high risk of developing atopy.24,25 In killed bacteria), lower concentrations
adults, certain strains of probiotics are of protective mucus, lower proteolyt-
Probiotics effective in decreasing the symptoms ic enzyme activity, and decreased gut
Probiotics may be the more familiar of lactose intolerance.4,26-28 motility; the premature infant is quite
term to most people. The active cul- Probiotics have been studied in vulnerable to infection and inflamma-
ture component of yogurt is a pro- infants (6 to 36 months of age) as a tion.34 One hypothesis about causa-
biotic. Fermented dairy foods such strategy to lessen antibiotic-associ- tion is that inappropriate colonization
as yogurt and acidophilus milk are ated diarrhea (AAD), which may be of bacteria can lead to NEC.35 A
probably the most common probi- mild to severe, and may start imme-
otic-containing foods found in gro- diately or up to 6 weeks after anti-
cery stores. Although they have been biotics have been discontinued.29 Some Probiotic Species
used for many years, the term pro- The disruption of normal fecal flora
biotic was just introduced in 1965.1 is thought to be the reason, with sBifidobacterium bifidum
The term is from the Greek for life.2 broad-spectrum antibiotics the most s Bifidobacterium infantis
Probiotics are beneficial bacteria that frequently implicated as causing s Bifidobacterium breve
s Lactobacillus acidophilus
Table 1: Beneficial and Detrimental Bacteria3 s Lactobacillus reuteri
Species Beneficial Detrimental s Lactobacillus rhamnosus
s Lactobacillus helveticus
Bifidobacterium +
s Streptococcus thermophilus
Eubacterium +
s63,WHICHCONSISTSOFBACTERIAL
Lactobacillus +
STRAINS Bifidobacterium" longum, B
Clostridium + infantis, B breve, Lactobacillus , aci-
Shigella + dophilus, L casei, L bulgaricus, L plan-
Veillonella +
etarium, Streptococcus thermophilus

AbbottNutritionHealthInstitute.org
10 | July 2008 NURSE CURRENTS1
systematic review by Barclay et al36 in pass through gastric, pancreatic, and What is the difference between a
2007 included studies with 1,191 in- bile secretions to arrive in the colon to probiotic and prebiotic? A probiotic in-
fants (<1,500 gms), (see Table 2) and populate the gut.44 The potential for troduces exogenous bacteria into the
concluded that the data appeared to sepsis45,46 and the concern over viabil- colon milieu; a prebiotic stimulates the
lend support to the use of probiotics ity of probiotics are two reasons that growth of one or a limited number of
for the prevention of NEC; however, there is currently an emphasis instead the beneficial indigenous bacteria. Pre-
the data were insufficient for com- on prebiotic research. biotics change or modulate the com-
ment on short- and long-term safe- position of the natural ecosystem.51
ty.36 Another large study by Hoyos Prebiotics What foods are prebiotics? Prebiotic
was not included in the analysis due Prebiotics are a concept that you activity has been seen in short-chain
to low scoring on methodology rat- may not have heard about, although carbohydrates that are resistant to di-
ing.42 There have been isolated case again used in the 1950s (Lactulose gestion in the upper GI tract but are
reports of probiotic sepsis, although was used 50 years ago as a prebiotic hydrolyzed and fermented in the co-
in the five studies reviewed by Bar- formula supplement to increase the lon. Sometimes they are termed nondi-
clay et al, no adverse reactions from numbers of Lactobacillus in infants gestible oligosaccharides (NDOs).4 See
probiotic sepsis were noted.36 A new intestines).47 The term prebiotic was Table 3 for some of the prebiotics that
Cochrane review is supportive but first used by Gibson and Roberfroid have been studied.
recommends a large randomized tri- in 1995.48-50 A prebiotic is: a non- Since Bifidobacterium is the pre-
al to evaluate the potential benefits digestible food ingredient that ben- dominant bacterium in breast-fed in-
and safety profile of probiotics.43 eficially affects the host by selectively fants, much research has focused on
A concern in the use of probiot- stimulating the growth and activity of possible prebiotics that would stimu-
ics is whether the bacteria are able one or a limited number of bacteria late the growth of this organism. In
to reach the colon unscathed as they in the colon.51 adults, fructo-oligosaccharides (FOS)

Table 2: Five Studies Evaluating Probiotics and Necrotizing Enterocolitis (NEC)36

Study Population Number of Organism and Outcomes Limitations
Subjects Quantity
$ANIETAL )NFANTSWEEKS TREATED Lactobacillus GGX#&5 ,OWERINCIDENCEOF.%# Low background incidence
 OR"7GM PLACEBO in mothers milk, donor milk TREATMENTGROUPVS of NEC
.)#5S)TALY or preterm formula CONTROLDIDNOTACHIEVE
STATISTICALSIGNIlCANCE
Costalos et al. )NFANTS WEEKS TREATED Saccaromyces boulardii ,OWERINCIDENCEOF.%# Not powered to detect
 .)#5'REECE PLACEBO #&5INPRETERMFORMULA TREATMENTGROUP changes in NEC rates.
VSCONTROLGROUP 4RENDTOWARDLESS.%#
OF.%#OFANYSEVERITY in treatment group
but did not achieve NOTSIGNIlCANTSTATISTICALLY
STATISTICALSIGNIlCANCE
Lin et al. )NFANTSGM TREATED Lactobacillus acidophilus ,OWERINCIDENCEOFALL.%# Any NEC primary outcome,
 .)#5#HINA PLACEBO MILLIONUNITS VSP although BELL stage 
and Bifidobacterium reported
infantis in mothers milk
or donor milk
Bin-Nun et al. INFANTSGM TREATED #&5 Lower incidence of all NEC Combined outcome of NEC
 Israel PLACEBO Bifidobacterium(B) bifidus, INTHETREATMENTGROUP or death or sepsis measured
B infantis, Streptococcus VSP
thermophilus in mothers
milk or preterm formula
Manzoni et al. INFANTSGM TREATED Lactobacillus (GGX Lower incidence of NEC in Not powered to detect
 .)#5)TALY PLACEBO #&5 INMOTHERSOR THETREATMENTGROUP changes in NEC rates.
donor milk VSNON SIGNIlCANT 4RENDTOWARDLESS.%#
TRENDP in treatment group
NOTSIGNIlCANTSTATISTICALLY

AbbottNutritionHealthInstitute.org
NURSE CURRENTS July 2008 | 112
 Table 3: Prebiotics
Type Abbreviation Type Abbreviation
Fructo-oligosaccharide &/3 Acacia gum '5-

Inulin None Lactulose ,/3

Galacto-oligosaccharide GOS Lactitol None

Polydextrose 0$8

Table 4: Review of Studies using Prebiotic-Supplemented Formulas

Study Population Prebiotic and Quantity Outcomes
-OROETAL &!'!INFANTS GDLGDL&/3'/3ANDCONTROL $OSEDEPENDENTSTIMULATINGEFFECTONBifidobacteria
and Lactobacilli, and softer stool
No intolerance noted
"OEHMETAL 0RETERMINFANTS GDL'/3&/3ANDFORMULAAND BifidobacteriumSIGNIlCANTLYINCREASEDSIMILARTO
WEEKS breast-fed controls breast-fed infants
3TOOLFREQUENCYSIGNIlCANTLYLOWERINCONTROLGROUP
No effect on tolerance or weight/length gain

"ENETAL66 &!'!INFANTS GDL'/3ORCONTROL Stool content of Lactobacilli and Bifidobacterium

higher, similar to breast-fed infant
No side effects noted

Bakker-Zierikzee et al. &!'!INFANTS GDL&/3AND'/3ORB. animalis or "REAST FEDOR&/3'/3INFANTSHADSIMILARmORA

 ADDITIONALCONTROLS FORMULABREAST FEDCONTROLS 0ROBIOTICANDCONTROLFORMULAGROUPHADSIMILARmORA
%ULERETAL68 &!'!INFANTSINA ORGDL&/3ORHUMANMILK &/3SUPPLEMENTEDATGD,RESULTEDINSOFTERMORE
cross-over design frequent stool
Supplemented formula was safe but had minimal effect
ONFECALmORAANDClostridium difficile toxin

+NOLETAL &!'!INFANTS GDL'/3AND&/3ORCONTROL Addition of prebiotics had stimulating effect on the

BREASTFEDCONTROLS growth of Bifidobacterium and on the growth of intesti-
NALmORAPROlLECLOSERTOBREAST FEDINFANTS

"RUZZESEETAL &!'!INFANTS '/3&/3ORCONTROL Infants on prebiotic formula had fewer episodes of

acute diarrhea, fewer upper respiratory infections
#OSTALOSETAL &!'!INFANTS GDLOF'/3AND&/3ANDCONTROL Prebiotic formula well tolerated, normal growth
4RENDTOWARDHIGHERPERCENTAGEOFBifidobacterium
and lower percentage of E. coli in stool, suppresses
Clostridium in stool

-OROETAL INFANTSATRISKFOR GDLOF'/3AND&/3ANDCONTROL )NCIDENCEOFATOPICDERMATITISSIGNIlCANTLYREDUCEDIN

atopy hydrolysed protein formula the infants fed prebiotic formula
:IEGLERETAL &!'!INFANTS GDL 0$8'/3ORGDL0$8 Looser stools on either prebiotic formula
'/3AND,/3ORCONTROL -OREADVERSEEVENTSDIARRHEAECZEMAANDIRRITABILITY
noted in supplemented groups

3CHOLTENSETAL &!'!INFANTS GMDL&/3AND'/3 !TWEEKSTHECONCENTRATIONOFSECRETORY)G!WASHIGHER

in prebiotic group than control, also Bifidobacterium
percentage higher than control and Clostridium lower
!RSLANOGLUETAL &!'!INFANTS GDL'/3&/3 &ORMULAFEDFORlRSTMONTHSFOLLOW UPCONTINUEDFOR
YEARS0REBIOTICGROUPHADSIGNIlCANTLYLOWERALLERGIC
symptoms atopic dermatitis, wheezing, urticaria,
fewer upper respiratory infections than controls during
THElRSTYEARS

Key: FAGAfull-term appropriate for gestational age; GOSgalacto-oligosaccharides; FOSfructo-oligosaccharides; PDXPolydextrose; LOSLactulose.

AbbottNutritionHealthInstitute.org
12 | July 2008 NURSE CURRENTS3
have been shown to result in numeri- influenced by extrinsic factors; spe- of choice in the first year of life.63,64 How-
cal predominance of Bifidobacteria in cifically, the type of feeding the baby ever, use of prebiotic-supplemented
the stool.48,52,53 In studies of rats colo- receives is one factor that determines infant formulas may have benefits for
nized with human fecal flora, the use the composition of the GI flora.58,59 the infant who does not receive moth-
of galacto-oligosaccharide (GOS) has The intestinal flora of infants receiv- ers milk, for whatever reason. As seen
been shown to have similar effects.54 ing breast milk is different from the in the study outcomes in Table 4, the
Formulas have been made with flora of formula-fed infants. The flora of benefits from prebiotic-supplemented
FOS and GOS for preterm, term, and breast-fed infants is predominantly Bifi- formulas included:
weaning infants.55,56 Table 4 reviews dobacteria and Lactobacilli.58 (This was 1. Higher counts of Bifidobacteria by
studies of prebiotic-supplemented noted in a work by Tissier in 1905.)60 4 weeks of age.
formulas. Only the study by Ziegler This microbial pattern is thought to 2. An increased number of Bifidobac-
had documented GI side effects.56 have beneficial effects on the develop- teria is associated with lower num-
GOS/FOS in formula appears to be ment of the immune system and exert bers of intestinal pathogens.
well tolerated: the mixture appears a beneficial effect on intestinal func- 3. The pattern of bifidobacterial sub-
to: (a) decrease diarrhea, (b) result tion. Formula-fed babies have been species is similar to the pattern of
in a softer stool, (c) be associated noted to have more diverse flora, with the breast-fed infant.
with fewer respiratory infections and larger numbers of Enterobacteriaceae 4. Prebiotic formulas result in stool pH
atopic dermatitis symptoms, and (d) and gram-negative organisms.4,58 and short-chain fatty acid patterns
change the intestinal flora to that Why do breast-fed babies have dif- similar to the breast-fed infant.
similar to the breast-fed infant. In- ferent colonies of bacteria? Human 5. Stool frequency and consistency is
vestigators have also found other milk possesses oligosaccharides that more like the breast-fed infant.
benefits: that certain prebiotics may have been identified as a bifido- 6. Reduced allergic reaction (atopic
decrease the growth of certain patho- genic factor prebiotics! These dermatitis) and reduced URI in the
genic bacteria, again trying to make carbohydrates have been found to first year of life.
the colonic bacterial mix optimal for be resistant to enzymatic degradation 7. Fewer episodes of acute diarrhea.
health. For example, cellobiose has in the upper gastrointestinal tract. 8. Prebiotic-supplemented formula is
the ability to attenuate the virulence Why do breast-fed infants have fewer easily tolerated, with no difference in
of Listeria.57 colonies of gram-negative bacteria? growth patterns.
Prebiotics are substrates for fermen- Bifidobacteria and Lactobacilli pro-
tation and are thought to aid in the reg- duce short-chain fatty acids, includ- There are some things to consider
ulation of colonic function by increasing ing lactic and other organic acids as you see reports in the literature
fecal bulk and water retention through that lower colonic pH and inhibit the and read studies on these functional
the increased bacterial mass. growth of some pathogenic bacteria. foods. You cannot safely extrapolate
Synbiotics are substances that incor- A commonly held belief is that Bifi- the effect on adults to infants, espe-
porate both pre- and probiotics. dobacteria produce a balanced and cially to preterm infants. Further, the
appropriate stimulation of the infant action of one probiotic or prebiotic
immune system.4 cannot be compared to that of anoth-
Synbiotics
er. The amount of pro- and prebiotics
sBifidobacteriaAND&/3 Uses for Prebiotics and Probiotics used in a study should also be similar
sLactobacilli and lactitol What is the future of the use of prebi- for a valid comparison. This is a fasci-
otics and probiotics? The use of such nating area of research, and one that
sBifidobacteriaAND'/3
functional foods appears very promis- may prove beneficial to our patients
ing. In the United States we are slower and their care givers.
Neonatal Gastrointestinal Flora: to come to the concept of functional
Breast-fed versus Formula-fed foods for infants; for more than 10 About the Author
Where does it start? A baby before years, the majority of infant formulas in Jacqueline J Wessel, MEd, RD, CNSD,
birth has a sterile GI tract. In a vagi- Japan have contained prebiotics;55,61,62 CSP, CLE, LD is a neonatal nutritionist
nal delivery, the baby is colonized, ini- and they have been used in Europe for at Cincinnati Childrens Hospital in the
tially, with flora from the mother. The the past seven years.62 NICU and in their High Risk Outpatient
baby born by C-section is colonized Clearly, breast milk is the gold stan- Clinic. She has been active in the pe-
with bacteria from the hospital envi- dard for neonatal and infant nutrition diatric section of ASPEN and has writ-
ronment instead of from the moth- and is recommended by the American ten several articles and book chapters
er.58,59 After birth, the intestinal flora is Academy of Pediatrics as the nutrition about neonatal nutrition.

AbbottNutritionHealthInstitute.org
NURSE CURRENTS July 2008 | 134
Prebiotics, Probiotics, and Synbiotics:
Functional Foods
By Jacqueline J Wessel, MEd, RD, CNSD, CSP, CLE, LD

References 16. Hoganauer C, Hammer HF, Krejs GJ, et al: Mechanisms and 31. Butel MJ, Suau A, Campeotto F, et al: Impaired bifidobacterial
1. Lilly DM, Stillwell RH: Probiotics: growth promoting factors pro- management of antibiotic associated diarrhea, Clin Infect Dis colonization in preterm infants born before 31 weeks gesta-
duced by microorganisms, Science 1965:147: 747. 1998; 27: 702. tion, J Pediatr Gastroenterol Nutr 2006; 42: e35.
2. Reid G. Jass J, Sebulsky MT, et al: Potential uses of probiotic in 17. McFarland LV, Brandmarker SA, Guandalini S: Pediatric 32. Caplan MS, Miller-Catchpole R, Kaup S, et al: Bifidobacterial
clinical practice, Clin Microbiol Rev 2003; 16: 658. Clostridium difficile: A phantom menace or a clinical reality? supplementation increases the incidence of necrotizing en-
J Pediatr Gastroenterol Nutr 2000; 31: 220. terocolitis in a neonatal rat model, Gastroenterology 1999;
3. Salminen S, Bouley C, Boutron-Rualt MC, et al: Functional food 117: 577.
science and gastrointestinal physiology and function, Br J Nutr 18. Tankanov RM, Ross MB, Ertel IJ, et al: Double-blind, placebo-
1998:80 (suppl): S147. controlled study of the efficacy of lactinex in the prophylaxis 33. Kitajima H, Sumida Y, Tanaka R et al: Early administration of
of amoxicillin-induced diarrhea, Ann Pharmacotherap 1990; Bifidobacterium breva to preterm infants: Randomized con-
4. Collins MD, Gibson GR: Probiotics, prebiotics and synbiotics: 24: 382. trolled trial., Arch Dis Child Fetal Neonatal Ed 1997; 76: F101.
Approaches for modulating the microbial ecology of the gut,
Am J Clin Nutr 1999; 69(suppl): 1052S. 19. Jirapinyo P, Thamonsiri N, Densupsoontorn N, et al: Preven- 34. Isolauri E: Probiotics in premature infants: A controversial is-
tion of antibiotic associated diarrhea in infants by probiotics, J sue, J Pediatr Gastroenterol Nutr 2007; 45: S188.
5. Szajewska H, Mrukowicz J: Probiotics in the treatment and Med Assoc Thai 2002; 85: S739.
prevention of acute infectious diarrhea in infants and children: 35. Claud EC, Walker WA: Hypothesis: Inappropriate colonization
A systematic review of published randomized, double blind, 20. Vanderhoof JA, Whitney DB, Aronson DL, et al: Lactobacillus of the premature intestine can cause neonatal necrotizing en-
placebo controlled trials, J Pediatr Gastroenterol Nutr 2001; GG in the prevention of antibiotic associated diarrhea in chil- terocolitis, FASEB J 2001; 15: 1398.
33: S17. dren, Pediatrics 1999: 135: 564. 36. Barclay AR, Stenson B, Simpson JH, et al: Probiotics for necro-
6. Van Niel C, Freudiner C, Garrison NM, et al: Lactobacillus ther- 21. Arvolo T, Laiho K, Torkkeli S, et al: Prophylactic Lactobacillus tizing enterocolitis: A systematic review, J Pediatr Gastroen-
apy for acute infectious diarrhea in children: A meta analysis, GG reduces antibiotic associated diarrhea in children with terol Nutr 2007; 45: 569.
Pediatrics 2002; 109: 768. respiratory infections: A randomized study, Pediatrics 1999; 37. Dani C, Viadioli R, Bertini G, et al: Probiotics feeding in preven-
104: e64. tion of urinary tract infections, bacterial sepsis, and necrotiz-
7. Huang JS, Bouvaros A, Lee JW, et al: Efficacy of probiotic use in
acute diarrhea in children: A meta analysis, Dig Dis Sci 2002; 22. Kotowska M, Albreacht P, Szajewska H: Saccharomyces bou- ing enterocolitis in preterm infants: A prospective double-blind
47: 2625. lardii in the prevention of antibiotic associated diarrhea in study, Biol Neonate 2002; 82:104.
children: A randomized, double-blind, placebo-controlled trial, 38. Costalos C, Kapiki A, Apostolou M, Papathoma E: The effect of
8. Allen SJ, Okoko B, Marion E, et al: Probiotics for treating infec- Aliment Pharmacol Ther 2005; 21: 583.
tious diarrhea, The Cochrane Database of Systematic Reviews prebiotic supplement formula on growth and stool microbiol-
2003, issue 4. 23. Correa NBO, Peret Filho LA, Penna FJ, et al: A randomized ogy of term infants, Early Hum Dev 2008; 84: 45.
formula controlled trial of Bifidobacterium lactis and Strep- 39. Lin HC, Su BH, Chen AC, et al: Oral probiotics reduce the in-
9. Costa- Ribeiro H, Ribeiro TC, Mattos AP, et al: Limitations of pro- tococcus thermophilus for prevention of antibiotic associated
biotic therapy on acute, severe dehydrating diarrhea, J Pediatr cidence and severity of necrotizing enterocolitis in very low
diarrhea in infants, J Clin Gastroenterol 2995; 39: 385. birth weight infants, Pediatrics 2005; 115: 1.
Gastroenterol Nutr 2003; 36:112.
24. Soh SE, Aw M, Gerez I, et al: Influence of probiotic supple- 40. Bin-Nun A, Bromiker R, Wilschanski M, et al: Oral probiotics
10. Salazar-Lindo E, Mirans-Langschwager P, Campos-Sanchez mentation on the primary prevention of eczema and allergen
M, et al: Lactobacillus casei strain GG in the treatment of in- prevent necrotizing enterocolitis in very low birthweight in-
sensitization in at risk Asian infants: A randomized double- fants, J Pediatrics 2005; 147: 192.
fants with acute, watery diarrhea: A randomized, double-blind blind placebo-controlled trial, J Allergy Clin Immunol 2008;
placebo controlled clinical trial, BMC Pediatr 2004; 4:18. 121: S33. 41. Manzoni P: Use of Lactobacillus casei subspecies Rhamno-
11. Sarker SA, Sultana S, Fuchs GJ, et al: Lactobacillus paraca- sus GG and gastrointestinal colonization by Candida species
25. Kalliomaki M, Kirjavaneinen P, Eorola E, et al: Distinct patterns in preterm neonates, J Pediatr Gastroenterol Nutr 2007; 45:
sei strain ST11 has no effect on rotavirus but ameliorates the of neonatal gut microflora in infants in whom atopy was and
outcome of non-rotavirus diarrhea in children from Bangla- S190.
was not developing, J Allergy Clin Immunol 2001; 107:129.
desh, Pediatrics 2005; 116: e221. 42. Alfaleh K, Bassler D: Probiotics for prevention of necrotizing
26. Kim HS, Gilliland SE: Lactobacillus acidophilus as a dietary enterocolitis in preterm infants, Cochrane Database Syst Rev
12. Kowalska-Duplaga K, Fyderek K, Szajewska H, et al: Efficacy adjunct for milk to aid lactose indigestion in humans, J Dairy
of Trilac in the treatment of acute diarrhea in infants and 2008; 23: CD005496.
Sci 1983; 66: 959.
young children: A muticentre, randomized, double-blind pla- 43. Roberfrois MB: Prebiotics: Preferential substrates for specific
cebo controlled study, Pediatr Wspoczesna Gastroenterologia 27. Gilliland SE, Kim HA: Effect of viable starter culture bacteria germs? Am J Clin Nutr 2001; 73 (suppl): 406S.
Iywienie Dziecka 2004; 3: 295. in yoghurt on lactose utilization in humans, J Dairy Sci 1984;
67: 1. 44. Cummings JH, Macfarlane GT, Englyst HN: Prebiotic digestion
13. Kurugol Z, Koturogolu G: Effects of Saccharomyces boulardii and fermentation, Am J Clin Nutr 2001; 73 (suppl): 415S.
in children with acute diarrhea, Acta Paediatr 2005; 94: 44. 28. Pettoelo MM, Guandalini S, Ecuba P, et al: Lactose malabsorp-
tion in children with symptomatic Giardia lamblia infection: 45. OConnor JA: Probiotics and disease: User friendly bacteria, J
14. Szajewska H, Setty M, Mrukowica J, et al: Probiotics in gas- Feasibility of yoghurt supplementation, J Pediatr Gastroenetrol Clin Gastroenterol 2005; 39: 351.
trointestinal diseases in children: Hard and not-so-hard evi- Nutr 1989; 9: 295. 46. Thomson C, McCarter YS, Krause PJ, et al: Lactobacillus aci-
dence of efficacy, J Pediatr Gastroenterol Nutr 2006; 42: 454. dophilus sepsis in a neonate, J Perinatol 2001; 21: 258.
29. Bartlett JG: Antibiotic associated diarrhea, Clin Infect Dis
15. Bartlett JG, Chang TW, Gurwith M, et al: Antibiotics associated 1992; 15: 573. 47. Macgillivray PC, Finlay HVL, Binns TB: Use of lactulose to cre-
pseudomembranous colitis due to toxin producing Clostridia, ate a preponderance of Lactobacilli in the intestine of bottle
N Engl J Med 1978; 298: 531. 30. McFarland IV, Surawicz CM, Greenberg RN, et al: Prevention of
beta-lactam diarrhoea by Saccharomyces boulardii compared fed infants, Scott Med J 1959; 4: 182.
to placebo, J Gastroenterol 1995; 90: 439.

AbbottNutritionHealthInstitute.org
2 | July 2008 NURSE CURRENTS5
48. Gibson GR, Roberfroid MB: Dietary modulation of the human 67. Bakker-Zierikzee AM, Alles MS, et al: Effects of infant formula
colonic microbiota: Introducing the concept of prebiotics, J containing a mixture of galacto- and fructo-oligosaccharides
Nutr 1995; 125: 1401. or viable Bifidobacteria animalis on the intestinal nicroflora
49. Gibson GR, Beatty EB, Wang X, et al: Selective stimulation of during the first 4 months of life, Br J Nutr 2005; 94: 83.
Bifidobacteria in the human colon by oligofructose and inulin, 68. Euler AR, Mitchell DK, Kline R, et al: Prebiotic effect of fructo-
Gastroenterol 1995; 108: 975. oligosaccharide supplemented term infant formula at two
50. Roberfroid MB: Prebiotics: Preferential substrates for specific concentrations compared with unsupplemented formula and
germs? Am J Clin Nutr 2001; 73 (suppl): 406S. human milk, J Pediatr Gastroenterol Nutr 2005; 40: 157.
51. Duggan C, Gannon J, Walker WA: Protective nutrients and 69. Knol J, Scholtens P, Kafka C, et al: Colon microflora in infants
functional foods for the gastrointestinal tract, Am J Clin Nutr fed formula with galacto- and fructo-oligosaccharides: More
2002; 75:789. like breast fed infants, J Pediatr Gastroenterol Nutr 2005; 40:
36.
52. Neu C, Romond C, Beerens H: A contribution to the study of
the distribution of Bifidobacterium in the fecal flora of breast- 70. Bruzzese E, et al: Effect of early administration of GOS/FOS on
fed and bottle fed infants, Reprod Nutr Dev 1980; 20: 1674. the prevention of intestinal and extra intestinal infections in
healthy infants, J Paediatr Gastroenterol Nutr 2006; 42: e95.
53. Buddington RF, Williams CH, Chen SC, et al: Dietary supple-
mentation of neosugar alters the fecal flora and decreases 71. Moro G, Arslanoglu S, Stahl B, et al: A mixture of prebiotic oli-
activity of some reductive enzymes in human subjects, Am J gosaccharides reduces the incidence of atopic dermatitis dur-
Clin Nutr 1996; 63: 709. ing the first six months of age, Arch Dis Child 2006; 9: 814.
54. Rowland IR, Tanaka R: The effects of transgalactosylated oli- 72. Scholtens PAM, Alliet P, Raes M, et al: Fecal secretory im-
gosaccharides on gut flora metabolism in rats associated with munoglobulin A is increased in healthy infants who receive a
human fecal flora, J Appl Bacteroiol 1993; 74: 667. formula with short-chain galacto-oligosaccharides and long-
chain fructo-oligosaccharides, J Nutr 2008;138: 1141.
55. Ziegler E, Vanderhoof JA, Petshow B, et al: Term infants fed
formula supplemented with selected blends of prebiotics 73. Arslanoglu S, Moro GE, Boehm G: Early supplementation of
grow normally and have soft stools similar to those reported prebiotic oligosaccharides protects formula-fed infants against
for breast fed infants, J Pediatr Gastroenterol Nutr 2007; 44: infections during the first 6 moths of life, J Nutr 2007;
359.
56. Moro G, Minoli I, Mosca M, et al: Dosage-related bifidogenic
effects of galacto- and fructo-oligosaccharides in formula fed
infants, J Pediatr Gastroenterol Nutr 2002; 34: 291.
57. Park SF, Kroll RG: Expression of listeriolysin and phosphati-
dylinositol specific phospholipase C is repressed by the plant
derived molecule cellobiose in Listeria monocytogenes, Mol
Micro 1993; 8: 653.
58. Kligler B, Hanaway P, Cohressen A: Probiotics in children, Pe-
diatr Clin N Am 2007; 54: 949.
59. Hall MA, Cole CB, Smith SL, et al: Factors influencing the
presence of faecal Lactobacilli in early infancy, Arch Dis Child
1990; 65:185.
60. Tissier H: Repartition des microbes dans lintestine du nouris-
son. (Distribution of microorganisms in the newborn intestinal
tract), Ann Inst Pasteur 1905; 19: 109.
61. Matsumoto K, Kobayashi Y, Ueyama S, et al: Galactooligosac-
charides, Geneva: Gordon & Breach Science, 1994.
62. Ghisoldi J: Dietary fibre and prebiotics in infant formula, Proc
Nutr Soc 2003; 62: 183.
63. American Academy of Pediatrics: Committee on Nutrition: Iron
fortification of infant formulas, Pediatrics 1999; 104:119.
64. American Academy of Pediatrics, Section on Breastfeeding:
Breast feeding and the use of human milk, Pediatrics 115;
496: 2005.
65. Boehm G, Lidestri M, Casetta P, et al: Supplementation of a
bovine milk formula with an oligosaccharide mixture increas-
es counts of faecal bifidobacterium in preterm infants, Arch
Dis Child Fetal Neonatal Ed 2002; 86: F178
66. Ben XM, Zhiu XY, Zhau WN, et al: Supplementation of milk
formula with galacto-oligosaccharides improves intestinal
micro-flora and fermentation of term infants, Chin Med J
2004; 117: 927.

AbbottNutritionHealthInstitute.org
NURSE CURRENTS July 2008 | 36