Can prebiotics and probiotics improve therapeutic outcomes for undernourished individuals?

Paul O Sheridan, Laure B Bindels, Delphine M Saulnier, Gregor Reid, Esther Nova, Kerstin Holmgren, Paul W O'Toole, James Bunn, Nathalie Delzenne, Karen P Scott, Paul O Sheridan, Laure B Bindels, Delphine M Saulnier, Gregor Reid, Esther Nova, Kerstin Holmgren, Paul W O'Toole, James Bunn, Nathalie Delzenne, Karen P Scott

Abstract

It has become clear in recent years that the human intestinal microbiota plays an important role in maintaining health and thus is an attractive target for clinical interventions. Scientists and clinicians have become increasingly interested in assessing the ability of probiotics and prebiotics to enhance the nutritional status of malnourished children, pregnant women, the elderly, and individuals with non-communicable disease-associated malnutrition. A workshop was held by the International Scientific Association for Probiotics and Prebiotics (ISAPP), drawing on the knowledge of experts from industry, medicine, and academia, with the objective to assess the status of our understanding of the link between the microbiome and under-nutrition, specifically in relation to probiotic and prebiotic treatments for under-nourished individuals. These discussions led to four recommendations: (1) The categories of malnourished individuals need to be differentiated To improve treatment outcomes, subjects should first be categorized based on the cause of malnutrition, additional health-concerns, differences in the gut microbiota, and sociological considerations. (2) Define a baseline "healthy" gut microbiota for each category Altered nutrient requirement (for example, in pregnancy and old age) and individual variation may change what constitutes a healthy gut microbiota for the individual. (3) Perform studies using model systems to test the effectiveness of potential probiotics and prebiotics against these specific categories These should illustrate how certain microbiota profiles can be altered, as members of different categories may respond differently to the same treatment. (4) Perform robust well-designed human studies with probiotics and/or prebiotics, with appropriate, defined primary outcomes and sample size These are critical to show efficacy and understand responder and non-responder outcomes. It is hoped that these recommendations will lead to new approaches that combat malnutrition. This report is the result of discussion during an expert workshop titled "How do the microbiota and probiotics and/or prebiotics influence poor nutritional status?" held during the 10th Meeting of the International Scientific Association for Probiotics and Prebiotics (ISAPP) in Cork, Ireland from October 1-3, 2012. The complete list of workshop attendees is shown in Table 1.

Keywords: ISAPP; malnutrition; microbiota; prebiotics; probiotics; undernutrition.

References

    1. FAO. WFP, IFAD. The state of food insecurity in the world 2012. Economic growth is necessary but not sufficient to accelerate reduction of hunger and malnutrition. Rome: FAO; 2012.
    1. Joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Córdoba, Argentina.October 2001:1-4.
    1. Gibson GR, Scott KP, Rastall RA, Tuohy KM, Hotchkiss A, Dubert-Ferrandon A, et al. Dietary prebiotics: Current status and new definition. Food Science & Technology Bulletin: Functional Foods. 2010;7:1–19.
    1. Brownawell AM, Caers W, Gibson GR, Kendall CW, Lewis KD, Ringel Y, Slavin JL. Prebiotics and the health benefits of fiber: current regulatory status, future research, and goals. J Nutr. 2012;142:962–74. doi: 10.3945/jn.112.158147.
    1. Flint HJ. The impact of nutrition on the human microbiome. Nutr Rev. 2012;70(Suppl 1):S10–3. doi: 10.1111/j.1753-4887.2012.00499.x.
    1. Gibson GR, Probert HM, Loo JV, Rastall RA, Roberfroid MB. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev. 2004;17:259–75. doi: 10.1079/NRR200479.
    1. Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacol Res. 2013;69:52–60. doi: 10.1016/j.phrs.2012.10.020.
    1. Macfarlane S, Macfarlane GT, Cummings JH. Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther. 2006;24:701–14. doi: 10.1111/j.1365-2036.2006.03042.x.
    1. Ritchie ML, Romanuk TN. A meta-analysis of probiotic efficacy for gastrointestinal diseases. PLoS One. 2012;7:e34938. doi: 10.1371/journal.pone.0034938.
    1. Allen SJ, Martinez EG, Gregorio GV, Dans LF. Probiotics for treating acute infectious diarrhoea. Cochrane Database Syst Rev. 2010:CD003048.
    1. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8. doi: 10.1126/science.1110591.
    1. Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5:220–30. doi: 10.1038/ismej.2010.118.
    1. Tap J, Mondot S, Levenez F, Pelletier E, Caron C, Furet JP, Ugarte E, Muñoz-Tamayo R, Paslier DL, Nalin R, et al. Towards the human intestinal microbiota phylogenetic core. Environ Microbiol. 2009;11:2574–84. doi: 10.1111/j.1462-2920.2009.01982.x.
    1. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, et al. MetaHIT Consortium A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65. doi: 10.1038/nature08821.
    1. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107:14691–6. doi: 10.1073/pnas.1005963107.
    1. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–7.
    1. DellaPenna D. Nutritional genomics: manipulating plant micronutrients to improve human health. Science. 1999;285:375–9. doi: 10.1126/science.285.5426.375.
    1. Initiative M. Investing in the future: A united call to action on vitamin and mineral deficiencies. Ottawa, Canada: Micronutrient Initiative; 2009.
    1. Gewa CA, Weiss RE, Bwibo NO, Whaley S, Sigman M, Murphy SP, Harrison G, Neumann CG. Dietary micronutrients are associated with higher cognitive function gains among primary school children in rural Kenya. Br J Nutr. 2009;101:1378–87. doi: 10.1017/S0007114508066804.
    1. Benton D. Micro-nutrient supplementation and the intelligence of children. Neurosci Biobehav Rev. 2001;25:297–309. doi: 10.1016/S0149-7634(01)00015-X.
    1. Chhagan MK, Van den Broeck J, Luabeya KK, Mpontshane N, Tomkins A, Bennish ML. Effect on longitudinal growth and anemia of zinc or multiple micronutrients added to vitamin A: a randomized controlled trial in children aged 6-24 months. BMC Public Health. 2010;10:145. doi: 10.1186/1471-2458-10-145.
    1. Rivera JA, Hotz C, González-Cossío T, Neufeld L, García-Guerra A. The effect of micronutrient deficiencies on child growth: a review of results from community-based supplementation trials. J Nutr. 2003;133(Suppl 2):4010S–20S.
    1. Allen LH, Peerson JM, Olney DK. Provision of multiple rather than two or fewer micronutrients more effectively improves growth and other outcomes in micronutrient-deficient children and adults. J Nutr. 2009;139:1022–30. doi: 10.3945/jn.107.086199.
    1. Scholz-Ahrens KE, Ade P, Marten B, Weber P, Timm W, Açil Y, Glüer CC, Schrezenmeir J. Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J Nutr. 2007;137(Suppl 2):838S–46S.
    1. Legette LL, Lee W, Martin BR, Story JA, Campbell JK, Weaver CM. Prebiotics enhance magnesium absorption and inulin-based fibers exert chronic effects on calcium utilization in a postmenopausal rodent model. J Food Sci. 2012;77:H88–94. doi: 10.1111/j.1750-3841.2011.02612.x.
    1. Martin BR, Braun MM, Wigertz K, Bryant R, Zhao Y, Lee W, Kempa-Steczko A, Weaver CM. Fructo-oligosaccharides and calcium absorption and retention in adolescent girls. J Am Coll Nutr. 2010;29:382–6. doi: 10.1080/07315724.2010.10719855.
    1. Weaver CM, Martin BR, Nakatsu CH, Armstrong AP, Clavijo A, McCabe LD, McCabe GP, Duignan S, Schoterman MH, van den Heuvel EG. Galactooligosaccharides improve mineral absorption and bone properties in growing rats through gut fermentation. J Agric Food Chem. 2011;59:6501–10. doi: 10.1021/jf2009777.
    1. Whisner CM, Martin BR, Schoterman MH, Nakatsu CH, McCabe LD, McCabe GP, Wastney ME, van den Heuvel EG, Weaver CM. Galacto-oligosaccharides increase calcium absorption and gut bifidobacteria in young girls: a double-blind cross-over trial. Br J Nutr. 2013;110:1292–303. doi: 10.1017/S000711451300055X.
    1. Kelleher SL, Casas I, Carbajal N, Lönnerdal B. Supplementation of infant formula with the probiotic lactobacillus reuteri and zinc: impact on enteric infection and nutrition in infant rhesus monkeys. J Pediatr Gastroenterol Nutr. 2002;35:162–8. doi: 10.1097/00005176-200208000-00011.
    1. McCabe LR, Irwin R, Schaefer L, Britton RA. Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice. J Cell Physiol. 2013;228:1793–8. doi: 10.1002/jcp.24340.
    1. Narva M, Nevala R, Poussa T, Korpela R. The effect of Lactobacillus helveticus fermented milk on acute changes in calcium metabolism in postmenopausal women. Eur J Nutr. 2004;43:61–8. doi: 10.1007/s00394-004-0441-y.
    1. Silva MR, Dias G, Ferreira CL, Franceschini SC, Costa NM. Growth of preschool children was improved when fed an iron-fortified fermented milk beverage supplemented with Lactobacillus acidophilus. Nutr Res. 2008;28:226–32. doi: 10.1016/j.nutres.2008.02.002.
    1. Bering S, Suchdev S, Sjøltov L, Berggren A, Tetens I, Bukhave K. A lactic acid-fermented oat gruel increases non-haem iron absorption from a phytate-rich meal in healthy women of childbearing age. Br J Nutr. 2006;96:80–5. doi: 10.1079/BJN20061683.
    1. Sazawal S, Dhingra U, Hiremath G, Sarkar A, Dhingra P, Dutta A, Menon VP, Black RE. Effects of Bifidobacterium lactis HN019 and prebiotic oligosaccharide added to milk on iron status, anemia, and growth among children 1 to 4 years old. J Pediatr Gastroenterol Nutr. 2010;51:341–6.
    1. Agustina R, Bovee-Oudenhoven IM, Lukito W, Fahmida U, van de Rest O, Zimmermann MB, Firmansyah A, Wulanti R, Albers R, van den Heuvel EG, et al. Probiotics Lactobacillus reuteri DSM 17938 and Lactobacillus casei CRL 431 modestly increase growth, but not iron and zinc status, among Indonesian children aged 1-6 years. J Nutr. 2013;143:1184–93. doi: 10.3945/jn.112.166397.
    1. Saulnier DM, Santos F, Roos S, Mistretta TA, Spinler JK, Molenaar D, Teusink B, Versalovic J. Exploring metabolic pathway reconstruction and genome-wide expression profiling in Lactobacillus reuteri to define functional probiotic features. PLoS One. 2011;6:e18783. doi: 10.1371/journal.pone.0018783.
    1. Rossi M, Amaretti A, Raimondi S. Folate production by probiotic bacteria. Nutrients. 2011;3:118–34. doi: 10.3390/nu3010118.
    1. Pero J. Perkins J, Sloma A. Riboflavin-overproducing strains of bacteria. European patent EP0405370 1991.
    1. Burgess C, O’connell-Motherway M, Sybesma W, Hugenholtz J, van Sinderen D. Riboflavin production in Lactococcus lactis: potential for in situ production of vitamin-enriched foods. Appl Environ Microbiol. 2004;70:5769–77. doi: 10.1128/AEM.70.10.5769-5777.2004.
    1. Burgess CM, Smid EJ, Rutten G, van Sinderen D. A general method for selection of riboflavin-overproducing food grade micro-organisms. Microb Cell Fact. 2006;5:24. doi: 10.1186/1475-2859-5-24.
    1. LeBlanc JG, Laiño JE, del Valle MJ, Vannini V, van Sinderen D, Taranto MP, de Valdez GF, de Giori GS, Sesma F. B-group vitamin production by lactic acid bacteria--current knowledge and potential applications. J Appl Microbiol. 2011;111:1297–309. doi: 10.1111/j.1365-2672.2011.05157.x.
    1. LeBlanc JG, Burgess C, Sesma F, Savoy de Giori G, van Sinderen D. Ingestion of milk fermented by genetically modified Lactococcus lactis improves the riboflavin status of deficient rats. J Dairy Sci. 2005;88:3435–42. doi: 10.3168/jds.S0022-0302(05)73027-7.
    1. Collins S, Dent N, Binns P, Bahwere P, Sadler K, Hallam A. Management of severe acute malnutrition in children. Lancet. 2006;368:1992–2000. doi: 10.1016/S0140-6736(06)69443-9.
    1. Schofield C, Ashworth A. Why have mortality rates for severe malnutrition remained so high? Bull World Health Organ. 1996;74:223–9.
    1. DeBoer MD, Lima AA, Oría RB, Scharf RJ, Moore SR, Luna MA, Guerrant RL. Early childhood growth failure and the developmental origins of adult disease: do enteric infections and malnutrition increase risk for the metabolic syndrome? Nutr Rev. 2012;70:642–53. doi: 10.1111/j.1753-4887.2012.00543.x.
    1. Agarwal KN, Bhasin SK. Feasibility studies to control acute diarrhoea in children by feeding fermented milk preparations Actimel and Indian Dahi. Eur J Clin Nutr. 2002;56(Suppl 4):S56–9. doi: 10.1038/sj.ejcn.1601664.
    1. Saran S, Gopalan S, Krishna TP. Use of fermented foods to combat stunting and failure to thrive. Nutrition. 2002;18:393–6. doi: 10.1016/S0899-9007(01)00790-0.
    1. Sur D, Manna B, Niyogi SK, Ramamurthy T, Palit A, Nomoto K, Takahashi T, Shima T, Tsuji H, Kurakawa T, et al. Role of probiotic in preventing acute diarrhoea in children: a community-based, randomized, double-blind placebo-controlled field trial in an urban slum. Epidemiol Infect. 2011;139:919–26. doi: 10.1017/S0950268810001780.
    1. Kerac M, Bunn J, Seal A, Thindwa M, Tomkins A, Sadler K, Bahwere P, Collins S. Probiotics and prebiotics for severe acute malnutrition (PRONUT study): a double-blind efficacy randomised controlled trial in Malawi. Lancet. 2009;374:136–44. doi: 10.1016/S0140-6736(09)60884-9.
    1. Diop HI, Dossou NI, Ndour MM, Briend A, Wade S. Comparison of the efficacy of a solid ready-to-use food and a liquid, milk-based diet for the rehabilitation of severely malnourished children: a randomized trial. Am J Clin Nutr. 2003;78:302–7.
    1. Land MH, Rouster-Stevens K, Woods CR, Cannon ML, Cnota J, Shetty AK. Lactobacillus sepsis associated with probiotic therapy. Pediatrics. 2005;115:178–81.
    1. Reid G, Gaudier E, Guarner F, Huffnagle GB, Macklaim JM, Munoz AM, Martini M, Ringel-Kulka T, Sartor B, Unal R, et al. International Scientific Association for Probiotics and Prebiotics Responders and non-responders to probiotic interventions: how can we improve the odds? Gut Microbes. 2010;1:200–4. doi: 10.4161/gmic.1.3.12013.
    1. Smith MI, Yatsunenko T, Manary MJ, Trehan I, Mkakosya R, Cheng J, Kau AL, Rich SS, Concannon P, Mychaleckyj JC, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013;339:548–54. doi: 10.1126/science.1229000.
    1. Picciano MF. Pregnancy and lactation: physiological adjustments, nutritional requirements and the role of dietary supplements. J Nutr. 2003;133:1997S–2002S.
    1. Rayco-Solon P, Fulford AJ, Prentice AM. Differential effects of seasonality on preterm birth and intrauterine growth restriction in rural Africans. Am J Clin Nutr. 2005;81:134–9.
    1. Huffman SL, Zehner E, Harvey P, Martin L, Piwoz E, Ndure K, et al. Essential Health Sector Actions to Improve Maternal Nutrition in Africa. LINKAGES Project, Academy for Educational Development, 2001.
    1. Yang Z, Huffman SL. Review of fortified food and beverage products for pregnant and lactating women and their impact on nutritional status. Matern Child Nutr. 2011;7(Suppl 3):19–43. doi: 10.1111/j.1740-8709.2011.00350.x.
    1. Hummelen R, Hemsworth J, Changalucha J, Butamanya NL, Hekmat S, Habbema JDF, Reid G. Effect of micronutrient and probiotic fortified yogurt on immune-function of anti-retroviral therapy naive HIV patients. Nutrients. 2011;3:897–909. doi: 10.3390/nu3100897.
    1. Hemsworth JC, Hekmat S, Reid G. Micronutrient supplemented probiotic yogurt for HIV-infected adults taking HAART in London, Canada. Gut Microbes. 2012;3:414–9. doi: 10.4161/gmic.21248.
    1. Van Tienen A, Hullegie YM, Hummelen R, Hemsworth J, Changalucha J, Reid G. Development of a locally sustainable functional food for people living with HIV in Sub-Saharan Africa: laboratory testing and sensory evaluation. Benef Microbes. 2011;2:193–8. doi: 10.3920/BM2011.0024.
    1. Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK, Gonzalez A, Werner JJ, Angenent LT, Knight R, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150:470–80. doi: 10.1016/j.cell.2012.07.008.
    1. Kinsella K, He W. Census bureau, international population reports. An Aging World: 2008, Washington: US Government Printing Office, DC 2009:1-209.
    1. European Commission. White Paper on a Strategy for Europe on Nutrition, Overweight and Obesity Related Health Issues. OOPEC, 2007.
    1. Mathus-Vliegen EM. Obesity and the elderly. J Clin Gastroenterol. 2012;46:533–44. doi: 10.1097/MCG.0b013e31825692ce.
    1. Biagi E, Nylund L, Candela M, Ostan R, Bucci L, Pini E, Nikkïla J, Monti D, Satokari R, Franceschi C, et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One. 2010;5:e10667. doi: 10.1371/journal.pone.0010667.
    1. Claesson MJ, Cusack S, O’Sullivan O, Greene-Diniz R, de Weerd H, Flannery E, Marchesi JR, Falush D, Dinan T, Fitzgerald G, et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4586–91. doi: 10.1073/pnas.1000097107.
    1. O'Toole PW, Claesson MJ. Gut microbiota: Changes throughout the lifespan from infancy to elderly. Int Dairy J. 2010;20:281–91. doi: 10.1016/j.idairyj.2009.11.010.
    1. Woodmansey EJ, McMurdo MET, Macfarlane GT, Macfarlane S. Comparison of compositions and metabolic activities of fecal microbiotas in young adults and in antibiotic-treated and non-antibiotic-treated elderly subjects. Appl Environ Microbiol. 2004;70:6113–22. doi: 10.1128/AEM.70.10.6113-6122.2004.
    1. Schiffrin EJ, Morley JE, Donnet-Hughes A, Guigoz Y. The inflammatory status of the elderly: the intestinal contribution. Mutat Res. 2010;690:50–6. doi: 10.1016/j.mrfmmm.2009.07.011.
    1. Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HM, Coakley M, Lakshminarayanan B, O’Sullivan O, et al. Gut microbiota composition correlates with diet and health in the elderly. Nature. 2012;488:178–84. doi: 10.1038/nature11319.
    1. Bunout D, Hirsch S, Pía de la Maza M, Muñoz C, Haschke F, Steenhout P, Klassen P, Barrera G, Gattas V, Petermann M. Effects of prebiotics on the immune response to vaccination in the elderly. JPEN J Parenter Enteral Nutr. 2002;26:372–6. doi: 10.1177/0148607102026006372.
    1. Bartosch S, Woodmansey EJ, Paterson JCM, McMurdo MET, Macfarlane GT. Microbiological effects of consuming a synbiotic containing Bifidobacterium bifidum, Bifidobacterium lactis, and oligofructose in elderly persons, determined by real-time polymerase chain reaction and counting of viable bacteria. Clin Infect Dis. 2005;40:28–37. doi: 10.1086/426027.
    1. Pitkala KH, Strandberg TE, Finne Soveri UH, Ouwehand AC, Poussa T, Salminen S. Fermented cereal with specific bifidobacteria normalizes bowel movements in elderly nursing home residents. A randomized, controlled trial. J Nutr Health Aging. 2007;11:305–11.
    1. Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR. Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. Am J Clin Nutr. 2008;88:1438–46.
    1. Zaharoni H, Rimon E, Vardi H, Friger M, Bolotin A, Shahar DR. Probiotics improve bowel movements in hospitalized elderly patients--the PROAGE study. J Nutr Health Aging. 2011;15:215–20. doi: 10.1007/s12603-010-0323-3.
    1. Schiffrin EJ, Thomas DR, Kumar VB, Brown C, Hager C, Van’t Hof MA, Morley JE, Guigoz Y. Systemic inflammatory markers in older persons: the effect of oral nutritional supplementation with prebiotics. J Nutr Health Aging. 2007;11:475–9.
    1. Oudshoorn C, van der Cammen TJ, McMurdo ME, van Leeuwen JP, Colin EM. Ageing and vitamin D deficiency: effects on calcium homeostasis and considerations for vitamin D supplementation. Br J Nutr. 2009;101:1597–606. doi: 10.1017/S0007114509338842.
    1. Rea MC, O’Sullivan O, Shanahan F, O’Toole PW, Stanton C, Ross RP, Hill C. Clostridium difficile carriage in elderly subjects and associated changes in the intestinal microbiota. J Clin Microbiol. 2012;50:867–75. doi: 10.1128/JCM.05176-11.
    1. O’Sullivan O, Coakley M, Lakshminarayanan B, Conde S, Claesson MJ, Cusack S, Fitzgerald AP, O’Toole PW, Stanton C, Ross RP, ELDERMET Consortium Alterations in intestinal microbiota of elderly Irish subjects post-antibiotic therapy. J Antimicrob Chemother. 2013;68:214–21. doi: 10.1093/jac/dks348.
    1. Sullivan PF. Mortality in anorexia nervosa. Am J Psychiatry. 1995;152:1073–4.
    1. Nova E, Toro O, Varela P, López-Vidriero I, Morandé G, Marcos A. Effects of a nutritional intervention with yogurt on lymphocyte subsets and cytokine production capacity in anorexia nervosa patients. Eur J Nutr. 2006;45:225–33. doi: 10.1007/s00394-006-0589-8.
    1. Solis B, Nova E, Gómez S, Samartín S, Mouane N, Lemtouni A, Belaoui H, Marcos A. The effect of fermented milk on interferon production in malnourished children and in anorexia nervosa patients undergoing nutritional care. Eur J Clin Nutr. 2002;56(Suppl 4):S27–33. doi: 10.1038/sj.ejcn.1601659.
    1. Armougom F, Henry M, Vialettes B, Raccah D, Raoult D. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PLoS One. 2009;4:e7125. doi: 10.1371/journal.pone.0007125.
    1. Fearon KC, Glass DJ, Guttridge DC. Cancer cachexia: mediators, signaling, and metabolic pathways. Cell Metab. 2012;16:153–66. doi: 10.1016/j.cmet.2012.06.011.
    1. Evans WJ, Morley JE, Argilés J, Bales C, Baracos V, Guttridge D, Jatoi A, Kalantar-Zadeh K, Lochs H, Mantovani G, et al. Cachexia: a new definition. Clin Nutr. 2008;27:793–9. doi: 10.1016/j.clnu.2008.06.013.
    1. Baracos VE, Pichard C, Attaix D. Survival: the relevant primary outcome for nutrition therapy in cancer patients. Curr Opin Clin Nutr Metab Care. 2012;15:211–2. doi: 10.1097/MCO.0b013e328352dc41.
    1. van Vliet MJ, Tissing WJ, Dun CA, Meessen NE, Kamps WA, de Bont ES, Harmsen HJ. Chemotherapy treatment in pediatric patients with acute myeloid leukemia receiving antimicrobial prophylaxis leads to a relative increase of colonization with potentially pathogenic bacteria in the gut. Clin Infect Dis. 2009;49:262–70. doi: 10.1086/599346.
    1. Bindels LB, Beck R, Schakman O, Martin JC, De Backer F, Sohet FM, Dewulf EM, Pachikian BD, Neyrinck AM, Thissen JP, et al. Restoring specific lactobacilli levels decreases inflammation and muscle atrophy markers in an acute leukemia mouse model. PLoS One. 2012;7:e37971. doi: 10.1371/journal.pone.0037971.
    1. Lin XB, Dieleman LA, Ketabi A, Bibova I, Sawyer MB, Xue H, Field CJ, Baracos VE, Gänzle MG. Irinotecan (CPT-11) chemotherapy alters intestinal microbiota in tumour bearing rats. PLoS One. 2012;7:e39764. doi: 10.1371/journal.pone.0039764.
    1. Xue H, Sawyer MB, Wischmeyer PE, Baracos VE. Nutrition modulation of gastrointestinal toxicity related to cancer chemotherapy: from preclinical findings to clinical strategy. JPEN J Parenter Enteral Nutr. 2011;35:74–90. doi: 10.1177/0148607110377338.
    1. Schulz KF, Altman DG, Moher D, CONSORT Group CONSORT 2010 statement: updated guidelines for reporting parallel group randomized trials. Ann Intern Med. 2010;152:726–32. doi: 10.7326/0003-4819-152-11-201006010-00232.
    1. Hoveyda N, Heneghan C, Mahtani KR, Perera R, Roberts N, Glasziou P. A systematic review and meta-analysis: probiotics in the treatment of irritable bowel syndrome. BMC Gastroenterol. 2009;9:15. doi: 10.1186/1471-230X-9-15.

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