About this Journal Submit a Manuscript Table of Contents
International Journal of Microbiology
Volume 2012 (2012), Article ID 151393, 8 pages
http://dx.doi.org/10.1155/2012/151393
Review Article

Gut Microbial Translocation in Critically Ill Children and Effects of Supplementation with Pre- and Pro Biotics

1Pediatric Emergency and Intensive Care Division, Department of Pediatrics, Sapienza University of Rome, Viale Regina Elena 324, 00161 Rome, Italy
2Department of Public Health and Infectious Diseases, Sapienza University of Rome, 100161 Rome, Italy

Received 22 April 2012; Accepted 12 July 2012

Academic Editor: Vincenzo Vullo

Copyright © 2012 Paola Papoff et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. L. Bateman and P. C. Seed, “Procession to pediatric bacteremia and sepsis: covert operations and failures in diplomacy,” Pediatrics, vol. 126, no. 1, pp. 137–150, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. J. C. Marshall, N. V. Christou, and J. L. Meakins, “The gastrointestinal tract: the “undrained abscess” of multiple organ failure,” Annals of Surgery, vol. 218, no. 2, pp. 111–119, 1993. View at Scopus
  3. R. E. Sarginson, N. Taylor, N. Reilly, P. B. Baines, and H. K. F. Van Saene, “Infection in prolonged pediatric critical illness: a prospective four-year study based on knowledge of the carrier state,” Critical Care Medicine, vol. 32, no. 3, pp. 839–847, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. G. Iapichino, M. L. Callegari, S. Marzorati et al., “Impact of antibiotics on the gut microbiota of critically ill patients,” Journal of Medical Microbiology, vol. 57, no. 8, pp. 1007–1014, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. C. J. Doig, L. R. Sutherland, J. D. Sandham, G. H. Fick, M. Verhoef, and J. B. Meddings, “Increased intestinal permeability is associated with the development of multiple organ dysfunction syndrome in critically ill ICU patients,” American Journal of Respiratory and Critical Care Medicine, vol. 158, no. 2, pp. 444–451, 1998. View at Scopus
  6. M. A. de La Cal, E. Cerdá, P. García-Hierro et al., “Survival benefit in critically ill burned patients receiving selective decontamination of the digestive tract: a randomized, placebo-controlled, double-blind trial,” Annals of Surgery, vol. 241, no. 3, pp. 424–430, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. V. Artinian, H. Krayem, and B. DiGiovine, “Effects of early enteral feeding on the outcome of critically ill mechanically ventilated medical patients,” Chest, vol. 129, no. 4, pp. 960–967, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. S. M. Steinberg, “Bacterial translocation: what it is and what it is not,” American Journal of Surgery, vol. 186, no. 3, pp. 301–305, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Guarner and J. R. Malagelada, “Gut flora in health and disease,” The Lancet, vol. 361, no. 9356, pp. 512–519, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. M. B. Roberfroid, F. Bornet, C. Bouley, and J. H. Cummings, “Colonic microflora: nutrition and health—summary and conclusions of an International Life Sciences Institute (ILSI) [Europe] Workshop held in Barcelona, Spain,” Nutrition Reviews, vol. 53, no. 5, pp. 127–130, 1995. View at Scopus
  11. S. C. Singhi and A. Baranwal, “Probiotic use in the critically ILL,” Indian Journal of Pediatrics, vol. 75, no. 6, pp. 621–627, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. M. J. G. Farthing, “Bugs and the gut: an unstable marriage,” Best Practice and Research, vol. 18, no. 2, pp. 233–239, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. J. C. Marshall, “Gastrointestinal flora and its alterations in critical illness1999,” Current Opinion in Clinical Nutrition & Metabolic Care, vol. 2, no. 5, pp. 405–411.
  14. M. Duman, H. Abacioglu, M. Karaman, N. Duman, and H. Özkan, “β-lactam antibiotic resistance in aerobic commensal fecal flora of newborns,” Pediatrics International, vol. 47, no. 3, pp. 267–273, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. A. F. Holton, M. A. Hall, and J. A. Lowes, “Antibiotic exposure delays intestinal colonization by Clostridium difficile in the newborn,” Journal of Antimicrobial Chemotherapy, vol. 24, no. 5, pp. 811–817, 1989. View at Scopus
  16. L. Ferraris, M. J. Butel, F. Campeotto, M. Vodovar, J. C. Roze, and J. Aires, “Clostridia in premature neonates' gut: incidence, antibiotic susceptibility, and perinatal determinants influencing colonization,” PLoS ONE, vol. 7, no. 1, Article ID e30594, 2012.
  17. C. Rousseau, F. Levenez, C. Fouqueray, J. Doré, A. Collignon, and P. Lepage, “Clostridium difficile colonization in early infancy is accompanied by changes in intestinal microbiota composition,” Journal of Clinical Microbiology, vol. 49, no. 3, pp. 858–865, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Kim, J. F. Shaklee, S. Smathers, et al., “Risk factors and outcomes associated with severe clostridium difficile infection in children,” The Pediatric Infectious Disease Journal, vol. 31, no. 2, pp. 134–138, 2012.
  19. J. E. Kohler, O. Zaborina, L. Wu et al., “Components of intestinal epithelial hypoxia activate the virulence circuitry of Pseudomonas,” American Journal of Physiology, vol. 288, no. 5, pp. G1048–G1054, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Alverdy, O. Zaborina, and L. Wu, “The impact of stress and nutrition on bacterial-host interactions at the intestinal epithelial surface,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 8, no. 2, pp. 205–209, 2005. View at Scopus
  21. V. B. Nieuwenhuijs, A. Verheem, H. van Duijvenbode-Beumer et al., “The role of interdigestive small bowel motility in the regulation of gut microflora, bacterial overgrowth, and bacterial translocation in rats,” Annals of Surgery, vol. 228, no. 2, pp. 188–193, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Alverdy, O. Zaborina, and L. Wu, “The impact of stress and nutrition on bacterial-host interactions at the intestinal epithelial surface,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 8, no. 2, pp. 205–209, 2005. View at Scopus
  23. J. W. Alexander, S. T. Boyce, G. F. Babcock et al., “The process of microbial translocation,” Annals of Surgery, vol. 212, no. 4, pp. 496–512, 1990. View at Scopus
  24. P. C. Sedman, J. Macfie, P. Sagar et al., “The prevalence of gut translocation in humans,” Gastroenterology, vol. 107, no. 3, pp. 643–649, 1994. View at Scopus
  25. C. L. Wells, M. A. Maddaus, and R. L. Simmons, “Proposed mechanisms for the translocation of intestinal bacteria,” Reviews of Infectious Diseases, vol. 10, no. 5, pp. 958–979, 1988. View at Scopus
  26. A. S. Gork, N. Usui, E. Ceriati et al., “The effect of mucin on bacterial translocation in I-407 fetal and Caco-2 adult enterocyte cultured cell lines,” Pediatric Surgery International, vol. 15, no. 3-4, pp. 155–159, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. H. H. Wenzl, G. Schimpl, G. Feierl, and G. Steinwender, “Time course of spontaneous bacterial translocation from gastrointestinal tract and its relationship to intestinal microflora in conventionally reared infant rats,” Digestive Diseases and Sciences, vol. 46, no. 5, pp. 1120–1126, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Cossart and P. J. Sansonetti, “Bacterial invasion: the paradigms of enteroinvasive pathogens,” Science, vol. 304, no. 5668, pp. 242–248, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. A. R. Hauser, “The type III secretion system of Pseudomonas aeruginosa: infection by injection,” Nature Reviews Microbiology, vol. 7, no. 9, pp. 654–665, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. R. J. Anand, C. L. Leaphart, K. P. Mollen, and D. J. Hackam, “The role of the intestinal barrier in the pathogenesis of necrotizing enterocolitis,” Shock, vol. 27, no. 2, pp. 124–133, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. M. D. Neal, C. Leaphart, R. Levy et al., “Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier,” Journal of Immunology, vol. 176, no. 5, pp. 3070–3079, 2006. View at Scopus
  32. B. Weber, L. Saurer, and C. Mueller, “Intestinal macrophages: differentiation and involvement in intestinal immunopathologies,” Seminars in Immunopathology, vol. 31, no. 2, pp. 171–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. L. C. Duffy, “Interactions mediating bacterial translocation in the immature intestine,” Journal of Nutrition, vol. 130, no. 2, supplement, pp. 432S–436S, 2000. View at Scopus
  34. A. Yachie, N. Takano, K. Ohta et al., “Defective production of interleukin-6 in very small premature infants in response to bacterial pathogens,” Infection and Immunity, vol. 60, no. 3, pp. 749–753, 1992. View at Scopus
  35. E. A. Deitch, W. M. Bridges, J. W. Ma, R. D. Berg, and R. D. Specian, “Obstructed intestine as a reservoir for systemic infection,” American Journal of Surgery, vol. 159, no. 4, pp. 394–401, 1990. View at Scopus
  36. E. A. Deitch, “Simple intestinal obstruction causes bacterial translocation in man,” Archives of Surgery, vol. 124, no. 6, pp. 699–701, 1989. View at Scopus
  37. J. W. Ding, R. Andersson, V. Soltesz, R. Willén, and S. Bengmark, “Obstructive jaundice impairs reticuloendothelial function and promotes bacterial translocation in the rat,” Journal of Surgical Research, vol. 57, no. 2, pp. 238–245, 1994. View at Publisher · View at Google Scholar · View at Scopus
  38. J. V. Reynolds, P. Murchan, H. P. Redmond et al., “Failure of macrophage activation in experimental obstructive jaundice: association with bacterial translocation,” British Journal of Surgery, vol. 82, no. 4, pp. 534–538, 1995. View at Publisher · View at Google Scholar · View at Scopus
  39. S. M. Sheen-Chen, P. Chau, and H. W. Harris, “Obstructive jaundice alters kupffer cell function independent of bacterial translocation,” Journal of Surgical Research, vol. 80, no. 2, pp. 205–209, 1998. View at Publisher · View at Google Scholar · View at Scopus
  40. R. W. Parks, C. H. Stuart Cameron, C. D. Gannon, C. Pope, T. Diamond, and B. J. Rowlands, “Changes in gastrointestinal morphology associated with obstructive jaundice,” The Journal of Pathology, vol. 192, no. 4, pp. 526–532, 2000.
  41. C. L. Wells, R. P. Jechorek, and S. L. Erlandsen, “Inhibitory effect of bile on bacterial invasion of enterocytes: possible mechanism for increased translocation associated with obstructive jaundice,” Critical Care Medicine, vol. 23, no. 2, pp. 301–307, 1995. View at Publisher · View at Google Scholar · View at Scopus
  42. H. J. Sugerman, G. L. Bloomfield, and B. W. Saggi, “Multisystem organ failure secondary to increased intraabdominal pressure,” Infection, vol. 27, no. 1, pp. 61–66, 1999. View at Scopus
  43. F. A. Moore, “The role of the gastrointestinal tract in postinjury multiple organ failure,” American Journal of Surgery, vol. 178, no. 6, pp. 449–453, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Moy, D. J. Lee, C. M. Harmon, R. A. Drongowski, and A. G. Coran, “Confirmation of translocated gastrointestinal bacteria in a neonatal model,” Journal of Surgical Research, vol. 87, no. 1, pp. 85–89, 1999. View at Publisher · View at Google Scholar · View at Scopus
  45. N. Pathan, M. Burmester, T. Adamovic, et al., “Intestinal injury and endotoxemia in children undergoing surgery for congenital heart disease,” American Journal of Respiratory and Critical Care Medicine, vol. 184, no. 11, pp. 1261–1269, 2011.
  46. L. Cicalese, P. Sileri, M. Green, K. Abu-Elmagd, S. Kocoshis, and J. Reyes, “Bacterial translocation in clinical intestinal transplantation,” Transplantation, vol. 71, no. 10, pp. 1414–1417, 2001. View at Scopus
  47. A. Pierro, H. K. F. van Saene, S. C. Donnell et al., “Microbial translocation in neonates and infants receiving long-term parenteral nutrition,” Archives of Surgery, vol. 131, no. 2, pp. 176–179, 1996. View at Scopus
  48. W. Manzanares and G. Hardy, “The role of prebiotics and synbiotics in critically ill patients,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 11, no. 6, pp. 782–789, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. G. R. Gibson and M. B. Roberfroid, “Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics,” Journal of Nutrition, vol. 125, no. 6, pp. 1401–1412, 1995. View at Scopus
  50. G. R. Gibson, H. M. Probert, J. Van Loo, R. A. Rastall, and M. B. Roberfroid, “Dietary modulation of the human colonic microbiota: updating the concept of prebiotics,” Nutrition Research Reviews, vol. 17, no. 2, pp. 259–275, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Kolida, K. Tuohy, and G. R. Gibson, “Prebiotic effects of inulin and oligofructose,” British Journal of Nutrition, vol. 87, supplement 2, pp. S193–S197, 2002. View at Scopus
  52. S. Kolida and G. R. Gibson, “Prebiotic capacity of inulin-type fructans,” Journal of Nutrition, vol. 137, no. 11, pp. 2503S–2506S, 2007. View at Scopus
  53. J. Van Loo, “The specificity of the interaction with intestinal bacterial fermentation by prebiotics determines their physiological efficacy,” Nutrition Research Reviews, vol. 17, no. 1, pp. 89–98, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. C. C. Roy, C. L. Kien, L. Bouthillier, and E. Levy, “Short-chain fatty acids: ready for prime time?” Nutrition in Clinical Practice, vol. 21, no. 4, pp. 351–366, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. D. J. Morrison, W. G. Mackay, C. A. Edwards, T. Preston, B. Dodson, and L. T. Weaver, “Butyrate production from oligofructose fermentation by the human faecal flora: what is the contribution of extracellular acetate and lactate?” British Journal of Nutrition, vol. 96, no. 3, pp. 570–577, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. M. L. Forchielli and W. A. Walker, “The role of gut-associated lymphoid tissues and mucosal defence,” British Journal of Nutrition, vol. 93, supplement 1, pp. S41–S48, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. B. Watzl, S. Girrbach, and M. Roller, “Inulin, oligofructose and immunomodulation,” British Journal of Nutrition, vol. 93, supplement 1, pp. S49–S55, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. F. Guarner, “Inulin and oligofructose: impact on intestinal diseases and disorders,” British Journal of Nutrition, vol. 93, supplement 1, pp. S61–S65, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. S. Chen, S. Srionnual, T. Onda, and F. Yanagida, “Effects of prebiotic oligosaccharides and trehalose on growth and production of bacteriocins by lactic acid bacteria,” Letters in Applied Microbiology, vol. 45, no. 2, pp. 190–193, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Roller, G. Rechkemmer, and B. Watzl, “Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats,” Journal of Nutrition, vol. 134, no. 1, pp. 153–156, 2004. View at Scopus
  61. E. Bruzzese, M. Volpicelli, M. Squaglia, A. Tartaglione, and A. Guarino, “Impact of prebiotics on human health,” Digestive and Liver Disease, vol. 38, 2, pp. S283–S287, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Macfarlane, G. T. Macfarlane, and J. H. Cummings, “Review article: prebiotics in the gastrointestinal tract,” Alimentary Pharmacology and Therapeutics, vol. 24, no. 5, pp. 701–714, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. S. Bengmark, “Synbiotics and the mucosal barrier in critically ill patients,” Current Opinion in Gastroenterology, vol. 21, no. 6, pp. 712–716, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. C. Alberda, L. Gramlich, J. Meddings et al., “Effects of probiotic therapy in critically ill patients: a randomized, double-blind, placebo-controlled trial,” American Journal of Clinical Nutrition, vol. 85, no. 3, pp. 816–823, 2007. View at Scopus
  65. B. Klarin, M. L. Johansson, G. Molin, A. Larsson, and B. Jeppsson, “Adhesion of the probiotic bacterium Lactobacillus plantarum 299v onto the gut mucosa in critically ill patients: a randomised open trial,” Critical Care, vol. 9, no. 3, pp. R285–293, 2005. View at Scopus
  66. M. C. Urdaci, P. Bressollier, and I. Pinchuk, “Bacillus clausii probiotic strains: antimicrobial and immunomodulatory activities,” Journal of Clinical Gastroenterology, vol. 38, no. 6, supplement, pp. S86–S90, 2004. View at Scopus
  67. C. M. C. Chapman, G. R. Gibson, and I. Rowland, “Health benefits of probiotics: are mixtures more effective than single strains?” European Journal of Nutrition, vol. 50, no. 1, pp. 1–17, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. P. Manzoni, G. Lista, E. Gallo et al., “Routine Lactobacillus rhamnosus GG administration in VLBW infants: a retrospective, 6-year cohort study,” Early Human Development, vol. 87, supplement 1, pp. S35–S38, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. T. D. Braga, G. A. P. da Silva, P. I. C. de Lira, and M. de Carvalho Lima, “Efficacy of Bifidobacterium breve and Lactobacillus casei oral supplementation on necrotizing enterocolitis in very-low-birth-weight preterm infants: a double-blind, randomized, controlled trial,” American Journal of Clinical Nutrition, vol. 93, no. 1, pp. 81–86, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Bin-Nun, R. Bromiker, M. Wilschanski et al., “Oral probiotics prevent necrotizing enterocolitis in very low birth weight neonates,” Journal of Pediatrics, vol. 147, no. 2, pp. 192–196, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. H. C. Lin, C. H. Hsu, H. L. Chen et al., “Oral probiotics prevent necrotizing enterocolitis in very low birth weight preterm infants: a Multicenter, Randomized, Controlled trial,” Pediatrics, vol. 122, no. 4, pp. 693–700, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. M. G. Romeo, D. M. Romeo, L. Trovato et al., “Role of probiotics in the prevention of the enteric colonization by Candida in preterm newborns: incidence of late-onset sepsis and neurological outcome,” Journal of Perinatology, vol. 31, no. 1, pp. 63–69, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Dani, R. Biadaioli, G. Bertini, E. Martelli, and F. F. Rubaltelli, “Probiotics feeding in prevention of urinary tract infection, bacterial sepsis and necrotizing enterocolitis in preterm infants: a prospective double-blind study,” Biology of the Neonate, vol. 82, no. 2, pp. 103–108, 2002. View at Publisher · View at Google Scholar · View at Scopus
  74. F. N. Sari, E. A. Dizdar, S. Oguz, O. Erdeve, N. Uras, and U. Dilmen, “Oral probiotics: lactobacillus sporogenes for prevention of necrotizing enterocolitis in very low-birth weight infants: a randomized, controlled trial,” European Journal of Clinical Nutrition, vol. 65, no. 4, pp. 434–439, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. N. Simakachorn, R. Bibiloni, P. Yimyaem et al., “Tolerance, safety, and effect on the faecal microbiota of an enteral formula supplemented with pre- and probiotics in critically ill children,” Journal of Pediatric Gastroenterology and Nutrition, vol. 53, no. 2, pp. 174–181, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. T. C. B. Honeycutt, M. El Khashab, R. M. Wardrop III et al., “Probiotic administration and the incidence of nosocomial infection in pediatric intensive care: a randomized placebo-controlled trial,” Pediatric Critical Care Medicine, vol. 8, no. 5, pp. 452–458, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. P. J. Watkinson, V. S. Barber, P. Dark, and J. D. Young, “The use of pre- pro- and synbiotics in adult intensive care unit patients: systematic review,” Clinical Nutrition, vol. 26, no. 2, pp. 182–192, 2007. View at Publisher · View at Google Scholar · View at Scopus