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Gastroentérologie Clinique et Biologique (2010) 34, Suppl.

1, S37—S43

Gastroentérologie Clinique et Biologique

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

ISSN 0181-9801

The intestinal microbiotia:

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

● Syndrome d’activation macrophagique
Guest editors: G.
● Corthier & P. Marteau

● Rectite radique
● Cancers du côlon et du rectum

Vol. 34
Supplement 1 – Vol. 34


Intestinal microbiota in short bowel syndrome ✰

Microbiote intestinal dans le syndrome du grêle 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
© 2010 Elsevier Masson SAS. All rights reserved.

Résumé Le syndrome du grêle court (SGC) est la principale cause d’insuffisance intes-
tinale, particulièrement chez l’enfant. Le côlon joue un rôle crucial pour l’adaptation et
le fonctionnement de l’intestin grêle chez les patients qui ont eu une résection étendue
de l’intestin grêle. Cependant, le SGC prédispose à une pullulation bactérienne dans
l’intestin grêle (PBiG), expliquant son importante prévalence chez ces patients. La PBiG
peut altérer significativement les fonctions de digestion et d’absorption intestinales peut
retarder ou empêcher l’arrêt de la nutrition parentérale totale. de plus, la PBiG peut
être l’une des causes de complications hépatiques associées à l’insuffisance intestinale,
pouvant nécessiter le recours à une transplantation hépatique dans certains cas. Les tests
cliniques habituellement utilisés pour évaluer la PBIG sont généralement peu fiables chez
les patients avec SGC. Le traitement de la PBiG par une antibiothérapie de première
intention reste très débattue, alors que d’autres approches, incluant les probiotiques,

*Corresponding author.
E-mail address: (o. Goulet)
✰ A reprint of the french translation of this article is available on request.

© 2010 Elsevier Masson SAS. All rights reserved.

7% and varied overgrowth. Soluble non-starch polysaccharides and some starches pass Nutritional support should aim to maintain an optimal undigested into the colon where colonic bacteria ferment nutritional status with normal growth and development. The main SCFAs are acetate. © 2010 Elsevier Masson SAS. and often at least the right colon. At this point some electrolytes like sodium. or gallbladder motility is (see paper by Cerf-Bensussan et al. In clinical trials and in clinical practice. the ileocecal may absorb medium-chain triglycerides (MCTs) [11].). small intestine bacte. magnesium and chloride are left as well as indigestible i. Some patients that Short bowel syndrome (SBS) is characterized by a state of are permanently dependent on PN need other innovative malabsorption following extensive resection of the small rehabilitation therapies. salivary EGF release. growth factors. becomes Short-chain fatty acids a central digestive and nutritional organ for preserving nutrients and producing trophic factors. selection or limit such liver injury are mandatory. by tion in the neonatal period [3-5]. They are absorbed by the colon . patients Short bowel syndrome grow up normally.. corresponding to SBS left with carbohydrates known as dietary fiber. Tous droits réservés Introduction nutrition (PN) is the cornerstone of management. metabolizing dietary fibers. including the development and matura. Oral feeding using enhancement of GI tion of the mucosal barrier and the mucosal immune system secretions. malabsorption requiring parenteral nutrition. failure to account for gestatio- their central role in adaptation after small bowel resection. nutrients and 80-90% of the water have been absorbed in the SBS may be classified into 3 different types (Fig. A recent survey included 87 children who undergone the colon and its microbiota in SBS and the risks related extensive neonatal SB resection. including long patient recruitment time. tive supply requiring artificial nutrition [2]. The chyme is mixed jejunocolic anastomosis. valve and the entire colon. 10]. The colon. 1. The overall survival was 89. acquiring or maintaining oral feeding skills. However. the colon. of SB adaptation. nal age and incomplete follow-up. bowel. and mortality in neonatal SBS are based on individual case associated liver disease (IFALD). The length of resection results in insufficient nutri. However the mode of feeding administration (SBS) is the most well recognized cause of intestinal failure varies among different groups as to the optimal composition (IF) [1]. The bacteria. semi-elemental or polymeric) and mode of tion and are left with SBS are in a state of severe intestinal delivery (gastric tube or oral feeding) [6. them not only to hydrogen and methane (“gas”) but also to while for infants or children an emphasis is placed on short-chain fatty acids (SCFAs). However. due to bias. Goulet. Patients who undergo extensive small bowel resec. of the colon and in sparing calories.S38 O. (elemental. < 40-50 cm. may adapt anatomical factors including age-adjusted intestinal length. sepsis and occurred within 1 year from the date of surgery This short review aims to underline the central role of [8]. play a crucial role for nourishment and 3) type 3. A cohort study reported IM should be preserved as much as possible especially for that most of the deaths were caused by liver failure or optimizing the function of the colon. F. to date most data on morbidity and gut-derived sepsis (GDS) may lead to intestinal failure. After PN weaning. surface and site of the resected small intestine [3]. more than 80% of infants adaptation leading to intestinal autonomy is a physiological and children now survive after extensive small bowel resec- process in which the colon is a crucial partner. The functional consequences of SBS depend on the length. ileocecal valve and colon preservation and occurrence of rial overgrowth (SIBO) with subsequent risks of translocation cholestasis [3-5]. in relation to its microbial contents. Moreover. Short bowel syndrome recommended. Strategies aiming to avoid series. intestinal transplantation [9. after small bowel resection. Within the framework of SBS. bowel lengthening. which misses the terminal ileum with mucus and bacteria and becomes feces. the most favorable with jejunoileal anas. most of the for adaptation [3-5]. Parenteral propionate and butyrate. according to the date of birth. followed-up over a mean to pathologic changes in the colon leading to bacterial 15-year period [5]. Joly apparaissent potentiellement intéressantes sur la base de données expérimentales mais reposent encore sur peu de données validées par des études chez l’Homme. However. with normal puberty and final height as expected from genetic target height.e. 1): 1) type small intestine. by and the ileocecal valve. The cause of resection Role of the colon in the short bowel syndrome and age of the patient at the time of surgery also influence the capabilities of the remnant gut function and potential By the time the chyme has reached the colon. 7]. Prognosis is related to hosting the greatest quantity of the microbiota. but the intestine should provide as much nutrition as possible to Intestinal microbiota (IM) has an influence on a variety of the patient in order to improve the physiological processes intestinal functions. with jejunostomy where the jejunum is left too short. a healthy colon tomosis that preserves the terminal ileum. Small intestine According to recent reports. variable SBS definitions. 2) type 2. By multivariate analysis. PN duration is significantly influenced by the length of residual SB and the absence of ICV.

In addition reduced mucosal atrophy and intestinal immune dysfunction anastomosis enables colonic fermentation of unabsorbed following massive small bowel resection [19-21]. being an In addition to their local effects. both hyperphagia and adaptation of the remaining DNA and villus height [12. over time during the with severe malabsorption.2-4.Intestinal microbiota in short bowel syndrome S39 Enterostomy : type I Jejuno-colic : type II Jejuno-ilecolic : type III ≤ 40 . Crypt depth and the number of cells per crypt was Colonic energy absorption may also increase somewhat during 35 percent and 22 percent higher. It seems that in hyperphagic SBS patients various enzymes.80 cm Figure 1 Anatomy of short bowel syndrome in neonates and children and metabolized by the colonic epithelial cells as a source adaptation period [28]. This were unchanged. patients might be expected to experience energy can be absorbed each day by the adult human colon decreased fecal fluid and sodium loss. but intact colon in continuity were able to decrease controls. the post-resection adaptation phase. carbohydrates from the small intestine to occur. related to increased whereas the proliferation and apoptotic levels per crypt colonic bacterial carbohydrate fermentation [27. Patients years after the last surgery and compared to 11 healthy with SBS. both systemic and enteral SCFAs exert a In spite of small intestine malabsorption in patients with trophic effect on the jejunum by increasing mucosal mass. adaptive colonic changes include . PepT1 and NHE2 mRNA were unmodified.3-3. The targeted Since SCFAs are the preferred energy source for colonocytes. In animal models. 19. By improving water and electrolyte parenteral nutrition with SCFAs or their intracecal infusion absorption. systemic SCFAs in important source of energy assimilation. Because SCFAs stimulate sodium and of energy [12-15]. proliferation status and transporters’ expres- Role for energy salvage sion level in the epithelium of the remaining colon of SBS adult patients compared to controls [30].005).9 MJ (525-1170 kcal) daily from dietary fiber [24-26]. The supplementation of whenever possible. The proliferating and apoptotic were fed a diet containing 60% carbohydrates [24]. NHE3 and PepT1 mRNAs were quantified decreased fecal carbohydrate losses in patients with colon by quantitative RT-PCR. It has been estimated that up to 3 MJ of water absorption.80 cm ≤ 20 . Twelve adult patients for energy salvage [23]. Hyperphagia. 17]. 29]. such as re-anasto- to SCFAs in the colon. animal studies can affect the motility of both the stomach and the ileum through neuroendocrine mechanisms. transporters were Na+/H+ exchangers (NHE2 and 3) and in patients with SBS the colon becomes an important organ oligopeptide transporter (PepT1).1 MJ/day (310-740 kcal) when they per crypt were quantified. supplemen. controls. SBS. but this is not always in the form of SCFAs [16. The depth of crypts and number of epithelial cells fecal energy loss by 1. Colonic cell contents were evaluated by revealing Ki67. colon improve patient outcomes. as well as severe in continuity. PCNA and metabolism of unabsorbed carbohydrates was indicated by caspase 3. respectively (p<0.80 cm ≤ 40 . Morphological adaptation of the colon bably through the expression of proglucagon and peptide YY. NHE2. Furthermore. should be done intestine and colon in SBS [18]. Approximately 75 mmol of SCFAs are with a jejunocolonic anastomosis were studied at least two produced from 10 g of unabsorbed carbohydrate. which is fermented Restoration of intestinal continuity. It is possible for an intact colon to absorb up to malabsorption. tation of an elemental diet with pectin. improved adaptation of the small mosis of the small intestine with the colon. 28]. such as galactosidase. pro. may be due to increased colonic bacteria in patients with NHE3 mRNA was down-regulated near the anastomosis and SBS as well as an increase in the concentration or activity of unmodified distally. observed clinically [24. was observed in SBS patients compared to 2. PN can then often be discontinued. A recent study evaluated morphology. 22].

intestine enterostomy or in those who received broad-spec- trum antibiotics. SIBO causes growth with the risk of liver disease. one should consider the of the gut microbiota in healthy humans. They e. syndrome D-lactic acidosis Changes in microbiota D-lactic acidosis. is a rare neurologic syndrome that occurs in individuals The remnant colon and its associated microbiota play a with SBS or following jejunoileal bypass surgery. Interestingly. including Clostridium concerning the other main bacterial groups. 40]. 9].1mg/kg. F. for recovering energy and is consequently a determinant in Neurologic symptoms include altered mental status. which may further lengthening instead of aggressive enteral feeding and/or exacerbate nutrient malabsorption. However. with patients often appearing drunk. The daily requirement in pediatric patients The Intestinal microbiota in the short bowel is 0. To fully explore the be destroyed by unnecessary and/or inappropriate use of effect of these conceptually new probiotics. Goulet. mucosal inflammation. is the cause or whether other factors are responsible [38]. Thiamine SBS patients is mainly composed of Lactobacilli [31. promote surgical procedures such as bowel tapering and allergic reactions and villous atrophy. is normal. components in the course of SBS patients. oral metronidazole. Pediatric multivitamin parenteral formulations generally contain vitamin K. cramps. SBS patients is linked to its own absorptive capability. microbiota. As mentioned this complication is very rare. Management should increased intestinal permeability. It is usually associated About 60% of vitamin K is synthesized by colonic bacteria with anorexia. These organisms may prolife- were mainly composed of Lactobacilli and. to consider the overall composition of microbiota in SBS pathology. which cannot be metabolized patients showed that the dominant fecal and mucosal groups by D-lactate dehydrogenase. Bacteriological analysis based on L-lactate concentration. (with spontaneous resolution). neither qualitative nor quantitative information is available Lactobacilli and other bacteria.. 32]. mucosa is likely to cin. vomiting. The up to 90% of the normal microbial community were absent. vitamin K deficiency may occur in rative/apoptotic ratio and well-preserved absorption NHE2. its Onset of neurologic symptoms is accompanied by metabolic adaptive increased absorptive surface and the metabolic acidosis and elevation of D-lactate plasma concentration. was present within the fecal and mucosa-associa. Fortunately. mechanism for the neurological symptoms is unknown. a bacteria never detected in healthy Treatments described in case reports have included nothing humans. but it is unclear if this underrepresented. a recent study in adult SBS carbohydrate to D-lactic acid. abdominal [35]. By using TTGE perfringens and Streptococcus bovis. major role in the outcome of patients with SBS. Symptoms typically pre- before. patients with protracted small NHE3 and PepT1 transporters mRNA levels [30]. 37].g. or were have been attributed to D-lactate. Bacteria that usually account for the metabolism of unabsorbed carbohydrates to SCFAs. diarrhea. Experimental models of SBS have shown that butyrate is the SCFA that augments intestinal adaptation by increasing proliferation and decreasing apoptosis. slurred reducing the need for PN. which is usually measured when culture-dependent methods has found that the microbiota of serum lactate concentration is ordered. Clostridium leptum or Clostridium coccoides. The essential role of the colon in speech and ataxia. . and deplete the bile salt pool with subsequent impaired micellar solubilization resulting in steatorrhea and fat solu- Vitamin K synthesis ble vitamin malabsorption [41-45]. The changes in microbiota involving SBS patients should be extensively investigated and considered carefully Small intestinal bacterial overgrowth as a since microbiota plays a central role in energy recovery by the limiting factor in the short bowel syndrome colon. also referred to as D-lactate encephalopa- thy. Deficiency is therefore uncommon in patients with an distension and failure to thrive. Lactobacillus mucosa. intact colon. while GLP-2 may be Consequences of small intestinal bacterial the mediator of the changes [34]. Bifidobacteria [33]. vancomycin. capability of the microbiota. Joly an increased absorptive surface with an unchanged prolife. (for 10-14 days) and avoidance of “refined” be specific to SBS since it has never been described as part carbohydrates [39. ferment unabsorbed analysis and quantitative PCR. to a lesser rate in an acidic environment that may be promoted by extent. SBS including ileocecal valve intestinal bacterial overgrowth (SIBO) emerge as essential resection often leads to small intestinal bacterial over. SIBO increases the risk of intestinal bacterial translocation. should always be carefully Functional factors such as absorption capability and preserved by avoiding oral antibiotics as much as possible intestinal motility of the remnant small intestine or small for bowel decontamination. but deficiency should be excluded [36. New probiotics intestinal microbiota as a major factor for achieving intes- should ideally promote the presence of deficient phyla and tinal adaptation and should be always “respected” and not restore a classical profile of microbiota. deconjugate bile salts oral large spectrum antibiotic cocktails [8. L.S40 O. However. patients left without colon. overgrowth (SIBO) On the other hand. it is important oral antibiotics. which is as key factor in bowel function and adaptation. preservation of the colon in SBS patients is essential sent after the ingestion of high-carbohydrate feedings. such as Bacteroidetes. neomy- ted microbiota of the SBS patients.

Antibiotics SIBO in patients with SBS. were assessed before and after the to PN and is likely to occur in the case of ICV resection. probiotics Figure 2 Improvement of clinical symptoms and breath test af- decreased BT through mechanisms which may be dependent ter administration of S. 9]. In the Necker study. 20 The effects of probiotics on bacterial translocation (BT) and mucosal intestinal trophicity after massive small bowel resection were studied in rat models. one month (Fig. Joly: None study. S. either alone or in its microbiota should be considered as partners rather combination with trimethoprim-sulfamethoxazole. The effects of 10 Saccharomyces boulardii versus placebo was studied in rats after 50% small bowel resections. microbiota helps measure the importance played by both tion of SCFAs and trophic factors.5 years old) with SBS participated in the F. In this sample of children. LGG therapy had no consistent effects on IP. 2).05 successful use of probiotics for the prevention of necrotizing enterocolitis in premature babies has been well documented [51. Lacaille F. modulating microbiota. In another experiment. Future developments in the field of high risk of emergent multiresistant strains of bacteria and probiotics might provide safe and targeted approaches in the anti-physiologic effects on colonic bacterial flora [9]. the disappearance of bacterial may be essential to obtaining SIBO resolution [8. Clinical symptoms including vomiting. 40 boulardii fungemia have been reported in SBS patients with a central venous catheter (CVC) [50]. understanding the colonic physiology and colonic bacterial flora which should be preserved for produc. The colon and therapy based on oral metronidazole. S. the performance of an intestinal tapering and in the frequency and intensity of symptoms in patients with lengthening procedure or resection of a tight anastomosis SBS. even if SIBO related thought to be an effective approach. In addition. Moreover. SBS rats had a SBS: short bowel syndrome greater proliferation index and apoptotic index in both the jejunum and ileum compared with sham animals [54]. boulardii significantly 0 enhances the functional adaptation of the remaining intestinal Day 0 Day 28 Day 0 Day 28 segments as shown by jejunal mucosal protein content and brush-border enzymes [53]. Ruemmele F. administration of high doses of SB (250 mg x 3 per day) for poor motility of a dilated small bowel segment [9. Antimotility agents such as loperamide may exacerbate SIBO and is also contraindicated. 42]. boulardii on intestinal mucosal integrity. J Pediatr Gastroenterol Nutr 2004. as well as abnormal complications [41]. Intermittent antimicrobial in the management of patients with SBS. bloating and flatulence. However. [1] Goulet O. medical therapy is difficult since the use of proki- sens as assessed by conventional stool cultures suggests that netic drugs for enhancing gut motor activity is contraindicated a one-month administration of SB may positively influence in these conditions. Nine children received a daily dose of 10 billion CFU of Lactobacillus rhamnosus (also known as LGG) or placebo for References 4 weeks. 52]. Role of probiotics in SBS Saccharomyces boulardii in SBS The use of probiotics might be helpful in SBS pediatric Administration of 250 mg x 3 /day in children patients [46]. Early detection and appropriate treatment of SIBO is necessary 57]. followed by a 3-week washout before therapy was crossed-over for another 4 weeks.Intestinal microbiota in short bowel syndrome S41 Management of SIBO Two open trials involving Saccharomyces boulardii (SB) administration were performed in SBS pediatric patients [56. Intestinal permeability (IP) was assessed in SBS patients in Conflicts of interests a double-blind. 41. Irreversible the IP was within normal limits and did not correlate with intestinal failure in children: a diagnostic and therapeutic age. SIBO exacerbates hepatotoxicity related hydrogen breath test. Both trials led to a significant decrease When possible. placebo-controlled crossover clinical trial by using lactulose-to-mannitol ratio [55]. challenge. has been than potential deleterious factors.38:250-69. Twenty-one children O. Goulet: None (9 months to 17. strains such as Klebsiella pneumoniae or Serratia marcen- Indeed. Cases of S. should be used very cautiously due to their effects on the Finally. complications are limiting factors in the long-term survival trum antimicrobial therapy must be very limited due to the of patients with SBS. The use of broad-spec. However they should be used very cautiously because of the addition of exogenous flora to an already Clinical score Breath Hydrogen overgrown small bowel bacterial flora. . Colomb V. cases of Lactobacillus bacteremia during probiotic treatment of SBS pediatric patients have been reported [47-49]. the 30 P < 0. abdominal pain to avoid morbidity and mortality following these severe SBS and distension. boulardii treatment is contra-indicated in patients with a CVC.

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