Gastroentrologie Clinique et Biologique (2010) 34, Suppl.

1, S37S43

Gastroentrologie Clinique et Biologique

Gastroentrologie Clinique et Biologique Vol. 34/1 (2010) 379-441

ISSN 0181-9801
C LINICS AND R ESEARCH IN H EPATOLOGY AND G ASTROENTEROLOGY

The intestinal microbiotia:

Equilibrium and
Mini-symposium on New disorders
Perspectives in Irritable Bowel
Predicting liver failure after major hepatectomy

63601
Syndrome dactivation macrophagique
Guest editors: G.
Cholcystectomie
Corthier & P. Marteau
ambulatoire

ELSEVIER MASSON
Rectite radique
Cancers du clon et du rectum

5
MAI
september
2010
2010
Vol. 34
Supplement 1 Vol. 34

THE PATHoLoGiCAL MiCroBioTA

Intestinal microbiota in short bowel syndrome

Microbiote intestinal dans le syndrome du grle court

O. Goulet a,c,*, F. Joly b,c

a Department of Pediatric Gastroenterology, Hepatology and Nutrition, Hospital Necker - Enfants Malades,
University of Paris- Descartes, Paris, France
b Department of Gastroenterology and Nutrition, Hospital Beaujon, University of Paris - Pierre et Marie Curie, Paris, France
c National Reference Center for Rare Digestive Disease

Summary Short bowel syndrome (SBS) is the main cause of intestinal failure especially
in children. The colon is a crucial partner for small intestine adaptation and function in
patients who have undergone extensive small bowel resection. However, SBS predisposes
the patient to small intestine bacterial overgrowth (SiBo), explaining its high prevalence
in patients with this disorder. SIBO may significantly compromise digestive and absorp-
tive functions and may delay or prevent weaning from total parenteral nutrition (TPn).
Moreover, SiBo may be one of the causes of intestinal failure-associated liver disease,
requiring liver transplantation in some cases. Traditional tests for assessing SiBo may
be unreliable in SBS patients. Management of SIBO with antibiotic therapy as a first-line
approach remains a matter of debate, while other approaches, including probiotics, offer
potential based on experimental evidence, though only few data from human studies are
available.
2010 Elsevier Masson SAS. All rights reserved.

Rsum Le syndrome du grle court (SGC) est la principale cause dinsuffisance intes-
tinale, particulirement chez lenfant. Le clon joue un rle crucial pour ladaptation et
le fonctionnement de lintestin grle chez les patients qui ont eu une rsection tendue
de lintestin grle. Cependant, le SGC prdispose une pullulation bactrienne dans
lintestin grle (PBiG), expliquant son importante prvalence chez ces patients. La PBiG
peut altrer significativement les fonctions de digestion et dabsorption intestinales peut
retarder ou empcher larrt de la nutrition parentrale totale. de plus, la PBiG peut
tre lune des causes de complications hpatiques associes linsuffisance intestinale,
pouvant ncessiter le recours une transplantation hpatique dans certains cas. Les tests
cliniques habituellement utiliss pour valuer la PBIG sont gnralement peu fiables chez
les patients avec SGC. Le traitement de la PBiG par une antibiothrapie de premire
intention reste trs dbattue, alors que dautres approches, incluant les probiotiques,

*Corresponding author.
E-mail address: olivier.goulet@nck.aphp.fr (o. Goulet)
A reprint of the french translation of this article is available on request.

2010 Elsevier Masson SAS. All rights reserved.

S38 O. Goulet, F. Joly
apparaissent potentiellement intressantes sur la base de donnes exprimentales mais
reposent encore sur peu de donnes valides par des tudes chez lHomme.
2010 Elsevier Masson SAS. Tous droits rservs
Introduction
Intestinal microbiota (IM) has an influence on a variety of
intestinal functions, including the development and matura-
tion of the mucosal barrier and the mucosal immune system
(see paper by Cerf-Bensussan et al.). Short bowel syndrome
(SBS) is the most well recognized cause of intestinal failure
(IF) [1]. Patients who undergo extensive small bowel resec-
tion and are left with SBS are in a state of severe intestinal
malabsorption requiring parenteral nutrition. Small intestine
adaptation leading to intestinal autonomy is a physiological
process in which the colon is a crucial partner. The colon, by
hosting the greatest quantity of the microbiota, may adapt
after small bowel resection. However, small intestine bacte-
rial overgrowth (SIBO) with subsequent risks of translocation
and gut-derived sepsis (GDS) may lead to intestinal failure-
associated liver disease (IFALD). Strategies aiming to avoid
or limit such liver injury are mandatory. However, due to
their central role in adaptation after small bowel resection,
IM should be preserved as much as possible especially for
optimizing the function of the colon.
This short review aims to underline the central role of
the colon and its microbiota in SBS and the risks related
to pathologic changes in the colon leading to bacterial
overgrowth.
Short bowel syndrome
Short bowel syndrome (SBS) is characterized by a state of
malabsorption following extensive resection of the small
bowel. The length of resection results in insufficient nutri-
tive supply requiring artificial nutrition [2]. The functional
consequences of SBS depend on the length, surface and site
of the resected small intestine [3]. The cause of resection
and age of the patient at the time of surgery also influence
the capabilities of the remnant gut function and potential
for adaptation [3-5]. In clinical trials and in clinical practice,
SBS may be classified into 3 different types (Fig. 1): 1) type
1, with jejunostomy where the jejunum is left too short,
i.e., < 40-50 cm; 2) type 2, corresponding to SBS left with
jejunocolic anastomosis, which misses the terminal ileum
and the ileocecal valve, and often at least the right colon;
and 3) type 3, the most favorable with jejunoileal anas-
tomosis that preserves the terminal ileum, the ileocecal
valve and the entire colon. Within the framework of SBS,
the colon, in relation to its microbial contents, becomes
a central digestive and nutritional organ for preserving
nutrients and producing trophic factors.
Nutritional support should aim to maintain an optimal
nutritional status with normal growth and development,
while for infants or children an emphasis is placed on
acquiring or maintaining oral feeding skills. Parenteral
nutrition (PN) is the cornerstone of management, but the
intestine should provide as much nutrition as possible to
the patient in order to improve the physiological processes
of SB adaptation. Oral feeding using enhancement of GI
secretions, salivary EGF release, or gallbladder motility is
recommended. However the mode of feeding administration
varies among different groups as to the optimal composition
(elemental, semi-elemental or polymeric) and mode of
delivery (gastric tube or oral feeding) [6, 7].
According to recent reports, more than 80% of infants
and children now survive after extensive small bowel resec-
tion in the neonatal period [3-5]. Prognosis is related to
anatomical factors including age-adjusted intestinal length,
ileocecal valve and colon preservation and occurrence of
cholestasis [3-5]. However, to date most data on morbidity
and mortality in neonatal SBS are based on individual case
series, including long patient recruitment time, selection
bias, variable SBS definitions, failure to account for gestatio-
nal age and incomplete follow-up. A cohort study reported
that most of the deaths were caused by liver failure or
sepsis and occurred within 1 year from the date of surgery
[8]. A recent survey included 87 children who undergone
extensive neonatal SB resection, followed-up over a mean
15-year period [5]. The overall survival was 89.7% and varied
according to the date of birth. By multivariate analysis, PN
duration is significantly influenced by the length of residual
SB and the absence of ICV. After PN weaning, patients
grow up normally, with normal puberty and final height as
expected from genetic target height. Some patients that
are permanently dependent on PN need other innovative
rehabilitation therapies, bowel lengthening, growth factors,
intestinal transplantation [9, 10].
Role of the colon in the short bowel syndrome
By the time the chyme has reached the colon, most of the
nutrients and 80-90% of the water have been absorbed in the
small intestine. At this point some electrolytes like sodium,
magnesium and chloride are left as well as indigestible
carbohydrates known as dietary fiber. The chyme is mixed
with mucus and bacteria and becomes feces. The bacteria, by
metabolizing dietary fibers, play a crucial role for nourishment
of the colon and in sparing calories. Moreover, a healthy colon
may absorb medium-chain triglycerides (MCTs) [11].
Short-chain fatty acids
Soluble non-starch polysaccharides and some starches pass
undigested into the colon where colonic bacteria ferment
them not only to hydrogen and methane (gas) but also to
short-chain fatty acids (SCFAs). The main SCFAs are acetate,
propionate and butyrate. They are absorbed by the colon
Intestinal microbiota in short bowel syndrome S39
Enterostomy : type I Jejuno-colic : type II
40 - 80 cm 40 - 80 cm
Figure 1 Anatomy of short bowel syndrome in neonates and children
and metabolized by the colonic epithelial cells as a source
of energy [12-15]. It has been estimated that up to 3 MJ of
energy can be absorbed each day by the adult human colon
in the form of SCFAs [16, 17]. In animal models, supplemen-
tation of an elemental diet with pectin, which is fermented
to SCFAs in the colon, improved adaptation of the small
intestine and colon in SBS [18]. The supplementation of
parenteral nutrition with SCFAs or their intracecal infusion
reduced mucosal atrophy and intestinal immune dysfunction
following massive small bowel resection [19-21].
In addition to their local effects, systemic SCFAs in
animal studies can affect the motility of both the stomach
and the ileum through neuroendocrine mechanisms, pro-
bably through the expression of proglucagon and peptide
YY. Furthermore, both systemic and enteral SCFAs exert a
trophic effect on the jejunum by increasing mucosal mass,
DNA and villus height [12, 19, 22].
Role for energy salvage
Since SCFAs are the preferred energy source for colonocytes,
in patients with SBS the colon becomes an important organ
for energy salvage [23]. Approximately 75 mmol of SCFAs are
produced from 10 g of unabsorbed carbohydrate. Patients
with SBS, but intact colon in continuity were able to decrease
fecal energy loss by 1.3-3.1 MJ/day (310-740 kcal) when they
were fed a diet containing 60% carbohydrates [24]. Colonic
metabolism of unabsorbed carbohydrates was indicated by
decreased fecal carbohydrate losses in patients with colon
in continuity. It is possible for an intact colon to absorb up to
2.2-4.9 MJ (525-1170 kcal) daily from dietary fiber [24-26].
Colonic energy absorption may also increase somewhat during
the post-resection adaptation phase, related to increased
colonic bacterial carbohydrate fermentation [27, 28]. This
may be due to increased colonic bacteria in patients with
SBS as well as an increase in the concentration or activity of
various enzymes, such as galactosidase, over time during the
Jejuno-ilecolic : type III
20 - 80 cm
adaptation period [28]. Because SCFAs stimulate sodium and
water absorption, patients might be expected to experience
decreased fecal fluid and sodium loss, but this is not always
observed clinically [24, 29].
Restoration of intestinal continuity, such as re-anasto-
mosis of the small intestine with the colon, should be done
whenever possible. By improving water and electrolyte
absorption, PN can then often be discontinued. In addition
anastomosis enables colonic fermentation of unabsorbed
carbohydrates from the small intestine to occur, being an
important source of energy assimilation.
Morphological adaptation of the colon
In spite of small intestine malabsorption in patients with
SBS, both hyperphagia and adaptation of the remaining
colon improve patient outcomes. A recent study evaluated
morphology, proliferation status and transporters expres-
sion level in the epithelium of the remaining colon of SBS
adult patients compared to controls [30]. The targeted
transporters were Na+/H+ exchangers (NHE2 and 3) and
oligopeptide transporter (PepT1). Twelve adult patients
with a jejunocolonic anastomosis were studied at least two
years after the last surgery and compared to 11 healthy
controls. The depth of crypts and number of epithelial cells
per crypt were quantified. The proliferating and apoptotic
cell contents were evaluated by revealing Ki67, PCNA and
caspase 3. NHE2, NHE3 and PepT1 mRNAs were quantified
by quantitative RT-PCR. Hyperphagia, as well as severe
malabsorption, was observed in SBS patients compared to
controls. Crypt depth and the number of cells per crypt was
35 percent and 22 percent higher, respectively (p<0.005),
whereas the proliferation and apoptotic levels per crypt
were unchanged. PepT1 and NHE2 mRNA were unmodified;
NHE3 mRNA was down-regulated near the anastomosis and
unmodified distally. It seems that in hyperphagic SBS patients
with severe malabsorption, adaptive colonic changes include
S40 O. Goulet, F. Joly
an increased absorptive surface with an unchanged prolife-
rative/apoptotic ratio and well-preserved absorption NHE2,
NHE3 and PepT1 transporters mRNA levels [30].
The Intestinal microbiota in the short bowel
syndrome
Changes in microbiota
The remnant colon and its associated microbiota play a
major role in the outcome of patients with SBS. As mentioned
before, preservation of the colon in SBS patients is essential
for recovering energy and is consequently a determinant in
reducing the need for PN. The essential role of the colon in
SBS patients is linked to its own absorptive capability, its
adaptive increased absorptive surface and the metabolic
capability of the microbiota. Bacteriological analysis based on
culture-dependent methods has found that the microbiota of
SBS patients is mainly composed of Lactobacilli [31, 32], but
neither qualitative nor quantitative information is available
concerning the other main bacterial groups. By using TTGE
analysis and quantitative PCR, a recent study in adult SBS
patients showed that the dominant fecal and mucosal groups
were mainly composed of Lactobacilli and, to a lesser
extent, Bifidobacteria [33]. Bacteria that usually account for
up to 90% of the normal microbial community were absent,
e.g., Clostridium leptum or Clostridium coccoides, or were
underrepresented, such as Bacteroidetes. Interestingly,
Lactobacillus mucosa, a bacteria never detected in healthy
humans, was present within the fecal and mucosa-associa-
ted microbiota of the SBS patients. L. mucosa is likely to
be specific to SBS since it has never been described as part
of the gut microbiota in healthy humans. New probiotics
should ideally promote the presence of deficient phyla and
restore a classical profile of microbiota. To fully explore the
effect of these conceptually new probiotics, it is important
to consider the overall composition of microbiota in SBS
pathology. The changes in microbiota involving SBS patients
should be extensively investigated and considered carefully
since microbiota plays a central role in energy recovery by the
colon. Experimental models of SBS have shown that butyrate
is the SCFA that augments intestinal adaptation by increasing
proliferation and decreasing apoptosis, while GLP-2 may be
the mediator of the changes [34].
On the other hand, microbiota, which is as key factor in
bowel function and adaptation, should always be carefully
preserved by avoiding oral antibiotics as much as possible
for bowel decontamination. SBS including ileocecal valve
resection often leads to small intestinal bacterial over-
growth with the risk of liver disease. Management should
promote surgical procedures such as bowel tapering and
lengthening instead of aggressive enteral feeding and/or
oral large spectrum antibiotic cocktails [8, 9].
Vitamin K synthesis
About 60% of vitamin K is synthesized by colonic bacteria
[35]. Deficiency is therefore uncommon in patients with an
intact colon. However, vitamin K deficiency may occur in
patients left without colon, patients with protracted small
intestine enterostomy or in those who received broad-spec-
trum antibiotics. The daily requirement in pediatric patients
is 0.1mg/kg. Pediatric multivitamin parenteral formulations
generally contain vitamin K.
D-lactic acidosis
D-lactic acidosis, also referred to as D-lactate encephalopa-
thy, is a rare neurologic syndrome that occurs in individuals
with SBS or following jejunoileal bypass surgery. Fortunately,
this complication is very rare. Symptoms typically pre-
sent after the ingestion of high-carbohydrate feedings.
Neurologic symptoms include altered mental status, slurred
speech and ataxia, with patients often appearing drunk.
Onset of neurologic symptoms is accompanied by metabolic
acidosis and elevation of D-lactate plasma concentration.
L-lactate concentration, which is usually measured when
serum lactate concentration is ordered, is normal. Thiamine
deficiency should be excluded [36, 37].
Lactobacilli and other bacteria, including Clostridium
perfringens and Streptococcus bovis, ferment unabsorbed
carbohydrate to D-lactic acid, which cannot be metabolized
by D-lactate dehydrogenase. These organisms may prolife-
rate in an acidic environment that may be promoted by
the metabolism of unabsorbed carbohydrates to SCFAs. The
mechanism for the neurological symptoms is unknown. They
have been attributed to D-lactate, but it is unclear if this
is the cause or whether other factors are responsible [38].
Treatments described in case reports have included nothing
(with spontaneous resolution), oral metronidazole, neomy-
cin, vancomycin, (for 10-14 days) and avoidance of refined
carbohydrates [39, 40]. However, one should consider the
intestinal microbiota as a major factor for achieving intes-
tinal adaptation and should be always respected and not
be destroyed by unnecessary and/or inappropriate use of
oral antibiotics.
Small intestinal bacterial overgrowth as a
limiting factor in the short bowel syndrome
Consequences of small intestinal bacterial
overgrowth (SIBO)
Functional factors such as absorption capability and
intestinal motility of the remnant small intestine or small
intestinal bacterial overgrowth (SIBO) emerge as essential
components in the course of SBS patients. SIBO causes
increased intestinal permeability, mucosal inflammation,
allergic reactions and villous atrophy, which may further
exacerbate nutrient malabsorption, deconjugate bile salts
and deplete the bile salt pool with subsequent impaired
micellar solubilization resulting in steatorrhea and fat solu-
ble vitamin malabsorption [41-45]. SIBO increases the risk
of intestinal bacterial translocation. It is usually associated
with anorexia, vomiting, diarrhea, cramps, abdominal
distension and failure to thrive.
Intestinal microbiota in short bowel syndrome S41
Management of SIBO
Early detection and appropriate treatment of SIBO is necessary
to avoid morbidity and mortality following these severe SBS
complications [41]. SIBO exacerbates hepatotoxicity related
to PN and is likely to occur in the case of ICV resection,
poor motility of a dilated small bowel segment [9, 41, 42].
When possible, the performance of an intestinal tapering and
lengthening procedure or resection of a tight anastomosis
may be essential to obtaining SIBO resolution [8, 9].
Indeed, medical therapy is difficult since the use of proki-
netic drugs for enhancing gut motor activity is contraindicated
in these conditions. Antimotility agents such as loperamide
may exacerbate SIBO and is also contraindicated. Antibiotics
should be used very cautiously due to their effects on the
colonic bacterial flora which should be preserved for produc-
tion of SCFAs and trophic factors. Intermittent antimicrobial
therapy based on oral metronidazole, either alone or in
combination with trimethoprim-sulfamethoxazole, has been
thought to be an effective approach. The use of broad-spec-
trum antimicrobial therapy must be very limited due to the
high risk of emergent multiresistant strains of bacteria and
the anti-physiologic effects on colonic bacterial flora [9].
Role of probiotics in SBS
The use of probiotics might be helpful in SBS pediatric
patients [46]. However they should be used very cautiously
because of the addition of exogenous flora to an already
overgrown small bowel bacterial flora. Moreover, cases of
Lactobacillus bacteremia during probiotic treatment of SBS
pediatric patients have been reported [47-49]. Cases of S.
boulardii fungemia have been reported in SBS patients with
a central venous catheter (CVC) [50]; S. boulardii treatment
is contra-indicated in patients with a CVC. However, the
successful use of probiotics for the prevention of necrotizing
enterocolitis in premature babies has been well documented
[51, 52].
The effects of probiotics on bacterial translocation
(BT) and mucosal intestinal trophicity after massive small
bowel resection were studied in rat models. The effects of
Saccharomyces boulardii versus placebo was studied in rats
after 50% small bowel resections. S. boulardii significantly
enhances the functional adaptation of the remaining intestinal
segments as shown by jejunal mucosal protein content and
brush-border enzymes [53]. In another experiment, probiotics
decreased BT through mechanisms which may be dependent
on intestinal mucosal integrity. In addition, SBS rats had a
greater proliferation index and apoptotic index in both the
jejunum and ileum compared with sham animals [54].
Intestinal permeability (IP) was assessed in SBS patients in
a double-blind, placebo-controlled crossover clinical trial by
using lactulose-to-mannitol ratio [55]. Twenty-one children
(9 months to 17.5 years old) with SBS participated in the
study. Nine children received a daily dose of 10 billion CFU of
Lactobacillus rhamnosus (also known as LGG) or placebo for
4 weeks, followed by a 3-week washout before therapy was
crossed-over for another 4 weeks. In this sample of children,
the IP was within normal limits and did not correlate with
age. LGG therapy had no consistent effects on IP.
Two open trials involving Saccharomyces boulardii (SB)
administration were performed in SBS pediatric patients [56,
57]. Clinical symptoms including vomiting, abdominal pain
and distension, bloating and flatulence, as well as abnormal
hydrogen breath test, were assessed before and after the
administration of high doses of SB (250 mg x 3 per day) for
one month (Fig. 2). Both trials led to a significant decrease
in the frequency and intensity of symptoms in patients with
SBS. In the Necker study, the disappearance of bacterial
strains such as Klebsiella pneumoniae or Serratia marcen-
sens as assessed by conventional stool cultures suggests that
a one-month administration of SB may positively influence
SIBO in patients with SBS.
Finally, understanding the colonic physiology and
microbiota helps measure the importance played by both
in the management of patients with SBS. The colon and
its microbiota should be considered as partners rather
than potential deleterious factors, even if SIBO related
complications are limiting factors in the long-term survival
of patients with SBS. Future developments in the field of
probiotics might provide safe and targeted approaches in
modulating microbiota.
Saccharomyces boulardii in SBS
Administration of 250 mg x 3 /day in children
Clinical score Breath Hydrogen
40
30 P < 0.05
20
10
0
Day 0 Day 28 Day 0 Day 28
Figure 2 Improvement of clinical symptoms and breath test af-
ter administration of S. boulardii
SBS: short bowel syndrome
Conflicts of interests
O. Goulet: None
F. Joly: None
References
[1] Goulet O, Ruemmele F, Lacaille F, Colomb V. Irreversible
intestinal failure in children: a diagnostic and therapeutic
challenge. J Pediatr Gastroenterol Nutr 2004;38:250-69.
S42 O. Goulet, F. Joly
[2] Sondheimer JM, Cadnapaphornchai M, Sontag M, Zerbe GO.
Predicting the duration of dependence on parenteral nutrition
after neonatal intestinal resection. J Pediatr 1998;132:80-4.
[3] Quiros-Tejeira RE, Ament ME, Reyen L, Herzog F, Merjanian
M, Olivares-Serrano N, et al. Long-term parenteral nutritional
support and intestinal adaptation in children with short bowel
syndrome: a 25-year experience. J Pediatr 2004;145:157-63.
[4] Spencer AU, Neaga A, West B, Safran J, Brown P, Btaiche I, et
al. Pediatric short bowel syndrome: redefining predictors of
success. Ann Surg 2005;242:403-9.
[5] Goulet O, Baglin-Gobet S, Talbotec C, Fourcade L, Colomb V,
Sauvat F, et al. Outcome and long-term growth after extensive
small bowel resection in the neonatal period: a survey of 87
children. Eur J Pediatr Surg 2005;15:95-101.
[6] Vanderhoof JA, Young RJ. Enteral and parenteral nutrition in
the care of patients with short-bowel syndrome. Best Pract
Res Clin Gastroenterol 2003;17:997-1015.
[7] DiBaise JK, Young RJ, Vanderhoof JA. Intestinal rehabilitation
and the short bowel syndrome: part 1. Am J Gastroenterol
2004;99:1386-95.
[8] Wales PW, de Silva N, Kim JH, Lecce L, Sandhu A, Moore AM.
Neonatal short bowel syndrome: a cohort study. J Pediatr Surg
2005;40:755-62.
[9] Goulet O, Sauvat F. Short bowel syndrome and intestinal
transplantation in children. Curr Opin Clin Nutr Metab Care
2006;9:304-13.
[10] Wales PW. Surgical therapy for short bowel syndrome. Pediatr
Surg Int 2004;20:647-57.
[11] Jeppesen PB, Mortensen PB. The influence of a preserved
colon on the absorption of medium chain fat in patients with
small bowel resection. Gut 1998;43:478-83.
[12] Koruda MJ, Rolandelli RH, Settle RG, Zimmaro DM, Rombeau JL.
Effect of parenteral nutrition supplemented with short-chain
fatty acids on adaptation to massive small bowel resection.
Gastroenterology 1988;95:715-20.
[13] Jeppesen PB, Mortensen PB. Colonic digestion and absorp-
tion of energy from carbohydrates and medium-chain fat in
small bowel failure. JPEN J Parenter Enteral Nutr 1999;23(5
Suppl):S101-5.
[14] Royall D, Wolever TM, Jeejeebhoy KN. Evidence for colonic
conservation of malabsorbed carbohydrate in short bowel
syndrome. Am J Gastroenterol 1992;87:751-6.
[15] Nordgaard I, Hansen BS, Mortensen PB. Colon as a digestive
organ in patients with short bowel. Lancet 1994;343:373-6.
[16] Tappenden KA, Thomson AB, Wild GE, McBurney MI. Short-chain
fatty acids increase proglucagon and ornithine decarboxylase
messenger RNAs after intestinal resection in rats. JPEN J
Parenter Enteral Nutr 1996;20:357-62.
[17] Koruda MJ, Rolandelli RH, Settle RG, Saul SH, Rombeau JL.
Harry M. Vars award. The effect of a pectin-supplemented
elemental diet on intestinal adaptation to massive small bowel
resection. JPEN J Parenter Enteral Nutr 1986;10:343-50.
[18] Tappenden KA, Thomson AB, Wild GE, McBurney MI. Short-
chain fatty acid-supplemented total parenteral nutrition
enhances functional adaptation to intestinal resection in rats.
Gastroenterology 1997;112:792-802.
[19] Welters CF, Deutz NE, Dejong CH, Soeters PB, Heineman E.
Supplementation of enteral nutrition with butyrate leads to
increased portal efflux of amino acids in growing pigs with
short bowel syndrome. J Pediatr Surg 1996;31:526-9.
[20] Bartholome AL, Albin DM, Baker DH, Holst JJ, Tappenden KA.
Supplementation of total parenteral nutrition with butyrate
acutely increases structural aspects of intestinal adaptation
after an 80% jejunoileal resection in neonatal piglets. JPEN J
Parenter Enteral Nutr 2004;28:210-22.
[21] Pratt VC, Tappenden KA, McBurney MI, Field CJ. Short-chain
fatty acid-supplemented total parenteral nutrition improves
nonspecific immunity after intestinal resection in rats. JPEN
J Parenter Enteral Nutr 1996;20:264-71.
[22] Bond JH, Currier BE, Buchwald H, Levitt MD. Colonic con-
servation of malabsorbed carbohydrate. Gastroenterology
1980;78:444-7.
[23] Cummings JH, Gibson GR, Macfarlane GT. Quantitative esti-
mates of fermentation in the hind gut of man. Acta Vet Scand
Suppl 1989;86:76-82.
[24] Nordgaard I, Hansen BS, Mortensen PB. Colon as a digestive
organ in patients with short bowel. Lancet 1994;343:373-6.
[25] Nightingale JMD, Lennard-Jones JE, Gertner DJ, Wood SR,
Bartran CI. Colonic preservation reduces need for parenteral
therapy, increases incidence of renal stones, but does not
change high prevalence of gallstones in patients with a short
bowel. Gut 1992;33:1493-7.
[26] Nordgaard I, Hansen BS, Mortensen PB. Importance of colonic
support for energy absorption as small-bowel failure proceeds.
Am J Clin Nutr 1996;64:222-31.
[27] Florent C, Flourie B, Leblond A, Rautureau M, Bernier JJ,
Rambaud JC. Influence of chronic lactulose ingestion on the
colonic metabolism of lactulose in man (an in vivo study). J
Clin Invest 1985;75:608-13.
[28] Briet F, Flouri B, Achour L, Maurel M, Rambaud JC, Messing B.
Bacterial adaptation in patients with short bowel and colon in
continuity. Gastroenterology 1995;109:1446-53.
[29] Ruppin H, Bar-Meir S, Soergel KH, Wood CM, Schmitt MG
Jr. Absorption of short-chain fatty acids by the colon.
Gastroenterology 1980;78:1500-7.
[30] Joly F, Mayeur C, Messing B, Lavergne-Slove A, Cazals-Hatem D,
Noordine ML, et al. Morphological adaptation with preserved
proliferation/transporter content in the colon of patients with
short bowel syndrome. Am J Physiol Gastrointest Liver Physiol
2009;297:G116-23.
[31] Bongaerts GP, Tolboom JJ, Naber AH, Sperl WJ, Severijnen
RS, Bakkeren JA, et al. Role of bacteria in the pathogenesis
of short bowel syndrome-associated D-lactic acidemia. Microb
Pathog 1997;22:285-93.
[32] Kaneko T, Bando Y, Kurihara H, Satomi K, Nonoyama K,
Matsuura N. Fecal microflora in a patient with short-bowel
syndrome and identification of dominant lactobacilli. J Clin
Microbiol 1997;35:3181-5.
[33] Joly F, Mayeur C, Bruneau A, Noordine ML, Meylheuc T, Langella
P, et al. Drastic changes in fecal and mucosa-associated micro-
biota in adult patients with short bowel syndrome. Biochimie
2010, in press.
[34] Bartholome AL, Albin DM, Baker DH, Holst JJ, Tappenden KA.
Supplementation of total parenteral nutrition with butyrate
acutely increases structural aspects of intestinal adaptation
after an 80% jejunoileal resection in neonatal piglets. JPEN J
Parenter Enteral Nutr 2004;28:210-22.
[35] Conly JM, Stein K, Worobetz L, Rutledge-Harding S. The
contribution of vitamin K2 (menaquinones) produced by the
intestinal microflora to human nutritional requirements for
vitamin K. Am J Gastroenterol 1994;89:915-23.
[36] From the Centers for Disease Control and Prevention. Lactic
acidosis traced to thiamine deficiency related to nationwide
shortage of multivitamins for total parenteral nutrition--Uni-
ted States, 1997. JAMA 1997;278:109-11.
[37] Kitamura K, Yamaguchi T, Tanaka H, Hashimoto S, Yang M,
Takahashi T. TPN-induced fulminant beriberi: a report on
our experience and a review of the literature. Surg Today
1996;26:769-76.
[38] Petersen C. D-lactic acidosis.Nutr Clin Pract 2005;20:634-45.
[39] Hudson M, Pocknee R, Mowat NA. D-lactic acidosis in short
bowel syndromean examination of possible mechanisms. Q
J Med 1990;74:157-63.
[40] Kadakia SC. D-lactic acidosis in a patient with jejunoileal
bypass. J Clin Gastroenterol 1995;20:154-6.
[41] Kaufman SS, Loseke CA, Lupo JV, Young RJ, Murray ND, Pinch
Intestinal microbiota in short bowel syndrome S43
LW, et al. Influence of bacterial overgrowth and intestinal
inflammation on duration of PN in children with short bowel
syndrome. J Pediatr 1997:131:356-61.
[42] Sondheimer JM, Asturias E, Cadnapaphornchai M. Infection and
cholestasis in neonates with intestinal resection and long-term
PN. J Pediatr Gastroenterol Nutr 1998:27:131-7.
[43] Forchielli ML, Walker WA. Nutritional factors contributing
to the development of cholestasis during total parenteral
nutrition. Dev Pediatr 2003;50:245-67.
[44] Cole CR, Ziegler TR. Small bowel bacterial overgrowth:
a negative factor in gut adaptation in pediatric SBS. Curr
Gastroenterol Rep 2007;9:456-62.
[45] Goulet O, Joly F, Corriol O, Colomb-Jung V. Some new insights
in intestinal failure-associated liver disease. Curr Opin Organ
Transplant 2009;14:256-61.
[46] Quigley EM. Bacteria: a new player in gastrointestinal motility
disorders--infections, bacterial overgrowth, and probiotics.
Gastroenterol Clin North Am 2007;36:735-48.
[47] Floch MH, Walker WA, Guandalini S, et al. Recommendations
for probiotic use--2008. J Clin Gastroenterol 2008;42(Suppl
2):S104-8.
[48] Wallace B. Clinical use of probiotics in the pediatric popula-
tion. Nutr Clin Pract 2009;24:50-9.
[49] Kunz AN, Noel JM, Fairchok MP. Two cases of Lactobacillus
bacteremia during probiotic treatment of short gut syndrome.
J Pediatr Gastroenterol Nutr 2004;38:457-8.
[50] Hennequin C, Kauffmann-Lacroix C, Jobert A, Viard JP,
Ricour C, Jacquemin JL, et al. Possible role of catheters in
Saccharomyces boulardii fungemia. Eur J Clin Microbiol Infect
Dis 2000;19:16-20.
[51] Alfaleh K, Bassler D. Probiotics for prevention of necrotizing
enterocolitis in preterm infants. Cochrane Database Syst Rev
2008;1:CD005496.
[52] Alfaleh K, Anabrees J, Bassler D. Probiotics reduce the risk of
necrotizing enterocolitis in preterm infants: a meta-analysis.
Neonatology 2010;97:93-9.
[53] Zaouche A, Loukil C, De Lagausie P, Peuchmaur M, Macry J,
Fitoussi F, et al. Effects of oral Saccharomyces boulardii on
bacterial overgrowth, translocation, and intestinal adaptation
after small-bowel resection in rats. Scand J Gastroenterol
2000;35:160-5.
[54] Mogilner JG, Srugo I, Lurie M, Shaoul R, Coran AG, Shiloni E,
et al. Effect of probiotics on intestinal regrowth and bacterial
translocation after massive small bowel resection in a rat. J
Pediatr Surg 2007;42:1365-71.
[55] Sentongo TA, Cohran V, Korff S, Sullivan C, Iyer K, Zheng X.
Intestinal permeability and effects of Lactobacillus rhamnosus
therapy in children with short bowel syndrome. J Pediatr
Gastroenterol Nutr 2008;46:41-7.
[56] Sadoun-Journo E, Gaillard JL, Blehaut H, Goulet O, Bernasconi
P, Ricour C. Grle court dysfonctionnel compliqu de pullu-
lation bactrienne chez lenfant : effet de Saccharomyces
boulardii. Gastroenterol Clin Biol 1994;18:A101.
[57] yszkowska M, Popiska K, Idzik M, Ksiyk J. Probiotics in
children with gut failure (abstract). J Pediatr Gastroenterol
Nutr 2008; 46:543.