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Short-chain fatty acids and commensal microbiota in the faeces of severely malnourished children with cholera rehydrated with three different carbohydrates

Abstract

Background:

Short-chain fatty acids (SCFAs) liberated by fermentation of complex carbohydrates might stimulate water and salt absorption, and provide energy. The aim of the study was to assess the number and proportion of faecal bacteria and the concentration of SCFAs of severely malnourished children with cholera receiving oral rehydration solution (ORS) containing glucose, amylase-resistant starch (ARS) or rice.

Methods:

Serial faecal samples were collected from 30 malnourished children with cholera until rehydration and partial nutritional recovery. SCFAs were identified and quantitated by high-performance liquid chromatography. In situ hybridization combined with flow cytometry was used to analyse the microbiota in the faeces.

Results:

Before treatment the concentration of total SCFA in faecal sample of cholera children was found to be 4.7±0.6 mmol/kg and it increased steadily until 95.0±8.7 mmol/kg at day 28. Among different ORS groups, concentration was significantly higher in the Rice-ORS group at day 1 (P<0.011) and at day 2 (P<0.025). During recovery faecal output was significantly reduced and the number of bacteria also increased faster in the Rice-ORS group than in the glucose-ORS group at day 1 and day 2 (P<0.01), and a modest increase in bacterial number was observed in the glucose-ORS plus ARS group (day 1, P=0.07; day 2, P=0.09).

Conclusion:

Clinical recovery was associated with an increase in bacterial and SCFA concentrations with all three carbohydrates in ORS. However, the increases were significantly higher in children receiving Rice-ORS.

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References

  • Alam NH, Islam S, Sattar S, Monira S, Desjeux JF (2009). Safety of rapid intravenous rehydration and comparative efficacy of 3 oral rehydration solutions in the treatment of severely malnourished children with dehydrating cholera. J Pediatr Gastroenterol Nutr 48, 318–327.

    Article  CAS  Google Scholar 

  • Amann RI, Ludwig W, Schleifer KH (1995). Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59, 143–169.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Argenzio RA, Whipp SC (1979). Inter-relationship of sodium, chloride, bicarbonate and acetate transport by the colon of the pig. J Physiol 295, 365–381.

    Article  CAS  Google Scholar 

  • Balamurugan R, Janardhan HP, George S, Raghava MV, Muliyil J, Ramakrishna BS (2008). Molecular studies of faecal anaerobic commensal bacteria in acute diarrhea in children. J Pediatr Gastroenterol Nutr 46, 514–519.

    Article  Google Scholar 

  • Binder HJ, Mehta P (1989). Short-chain fatty acids stimulate active sodium and chloride absorption in vitro in the rat distal colon. Gastroenterology 96, 989–996.

    Article  CAS  Google Scholar 

  • Cummings JH, Macfarlane GT (1997). Role of intestinal bacteria in nutrient metabolism. J Parenter Enteral Nutr 21, 357–365.

    Article  CAS  Google Scholar 

  • Desjeux JF, Nath SK, Taminiau J (1994). Organic substrate and electrolyte solutions for oral rehydration in diarrhea. Annu Rev Nutr 14, 321–342.

    Article  CAS  Google Scholar 

  • Dore J, Sghir A, Hannequart-Gramet G, Corthier G, Pochart P (1998). Design and evaluation of a 16S rRNA-targeted oligonucleotide probe for specific detection and quantitation of human faecal Bacteroides populations. Syst Appl Microbiol 21, 65–71.

    Article  CAS  Google Scholar 

  • Dutta D, Bhattacharya MK, Deb AK, Sarkar D, Chatterjee A, Biswas AB et al. (2000). Evaluation of oral hypo-osmolar glucose-based and rice-based oral rehydration solutions in the treatment of cholera in children. Acta Paediatr 89, 787–790.

    Article  CAS  Google Scholar 

  • Falony G, Vlachou A, Verbrugghe K, De Vuyst L (2006). Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl Environ Microbiol 72, 7835–7841.

    Article  CAS  Google Scholar 

  • Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW (1998). Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 64, 3336–3345.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gore SM, Fontaine O, Pierce NF (1992). Impact of rice based oral rehydration solution on stool output and duration of diarrhoea: meta-analysis of 13 clinical trials. BMJ 304, 287–291.

    Article  CAS  Google Scholar 

  • Gregorio GV, Gonzales ML, Dans LF, Martinez EG (2009). Polymer-based oral rehydration solution for treating acute watery diarrhoea. Cochrane Database Syst Rev CD006519.

  • Guerrant GO, Moss CW, Lambert MA (1982). Analysis of short-chain acids from anaerobic bacteria by high-performance liquid chromatography. J Clin Microbiol 16, 355–360.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harmsen HJ, Wildeboer-Veloo AC, Grijpstra J, Knol J, Degener JE, Welling GW (2000). Development of 16S rRNA-based probes for the Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human feces from volunteers of different age groups. Appl Environ Microbiol 66, 4523–4527.

    Article  CAS  Google Scholar 

  • Harmsen HJM, Elfferich P, Schut F, Welling GW (1999). A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Microb Ecol Health Dis 11, 3–12.

    Article  Google Scholar 

  • Hoekstra JH, Szajewska H, Zikri MA, Micetic-Turk D, Weizman Z, Papadopoulou A et al. (2004). ‘Oral rehydration solution containing a mixture of non-digestible carbohydrates in the treatment of acute diarrhea: a multicenter randomized placebo controlled study on behalf of the ESPGHAN working group on intestinal infections’. J Pediatr Gastroenterol Nutr 39, 239–245.

    Article  CAS  Google Scholar 

  • Krishnan S, Ramakrishna BS, Binder HJ (1999). Stimulation of sodium chloride absorption from secreting rat colon by short-chain fatty acids. Dig Dis Sci 44, 1924–1930.

    Article  CAS  Google Scholar 

  • Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH et al. (1995). Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in faecal samples. Appl Environ Microbiol 61, 3069–3075.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Macfarlane S, Macfarlane GT, Cummings JH (2006). Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther 24, 701–714.

    Article  CAS  Google Scholar 

  • Macleod RJ, Bennett HP, Hamilton JR (1995). Inhibition of intestinal secretion by rice. Lancet 346, 90–92.

    Article  CAS  Google Scholar 

  • Magne F, Hachelaf W, Suau A, Boudraa G, Bouziane-Nedjadi K, Rigottier-Gois L et al. (2008). Effects on faecal microbiota of dietary and acidic oligosaccharides in children during partial formula feeding. J Pediatr Gastroenterol Nutr 46, 580–588.

    Article  CAS  Google Scholar 

  • Mathews CJ, MacLeod RJ, Zheng SX, Hanrahan JW, Bennett HP, Hamilton JR (1999). Characterization of the inhibitory effect of boiled rice on intestinal chloride secretion in guinea pig crypt cells. Gastroenterology 116, 1342–1347.

    Article  CAS  Google Scholar 

  • Molla AM, Sarker SA, Hossain M, Molla A, Greenough III WB (1982). Rice-powder electrolyte solution as oral-therapy in diarrhoea due to Vibrio cholerae and Escherichia coli. Lancet 1, 1317–1319.

    Article  CAS  Google Scholar 

  • Murphy C, Hahn S, Volmink J (2004). Reduced osmolarity oral rehydration solution for treating cholera. Cochrane Database Syst Rev CD003754.

  • Nath SK, Rautureau M, Heyman M, Reggio H, L’Helgoualc’h A, Desjeux JF (1989). Emergence of Na+-glucose cotransport in an epithelial secretory cell line sensitive to cholera toxin. Am J Physiol 256 (2 Part 1), G335–G341.

    CAS  PubMed  Google Scholar 

  • Raghupathy P, Ramakrishna BS, Oommen SP, Ahmed MS, Priyaa G, Dziura J et al. (2006). Amylase-resistant starch as adjunct to oral rehydration therapy in children with diarrhea. J Pediatr Gastroenterol Nutr 42, 362–368.

    Article  CAS  Google Scholar 

  • Ramakrishna BS, Roediger WE (1990). Bacterial short chain fatty acids: their role in gastrointestinal disease. Dig Dis 8, 337–345.

    Article  CAS  Google Scholar 

  • Ramakrishna BS, Venkataraman S, Srinivasan P, Dash P, Young GP, Binder HJ (2000). Amylase-resistant starch plus oral rehydration solution for cholera. N Engl J Med 342, 308–313.

    Article  CAS  Google Scholar 

  • Ramakrishna BS, Subramanian V, Mohan V, Sebastian BK, Young GP, Farthing MJ et al. (2008). A randomized controlled trial of glucose versus amylase resistant starch hypo-osmolar oral rehydration solution for adult acute dehydrating diarrhea. PLoS ONE 3, e1587.

    Article  Google Scholar 

  • Rigottier-Gois L, Rochet V, Garrec N, Suau A, Doré J (2003). Enumeration of Bacteroides species in human faeces by fluorescent in situ hybridisation combined with flow cytometry using 16S rRNA probes. Syst Appl Microbiol 26, 110–118.

    Article  Google Scholar 

  • Roediger WE (1986). Metabolic basis of starvation diarrhoea: implications for treatment. Lancet 1, 1082–1084.

    Article  CAS  Google Scholar 

  • Roediger WE (1994). Famine, fiber, fatty acids, and failed colonic absorption: does fiber fermentation ameliorate diarrhea? J Parenter Enteral Nutr 18, 4–8.

    Article  CAS  Google Scholar 

  • Roediger WE, Moore A (1981). Effect of short-chain fatty acid on sodium absorption in isolated human colon perfused through the vascular bed. Dig Dis Sci 26, 100–106.

    Article  CAS  Google Scholar 

  • Scheppach W (1994). Effects of short chain fatty acids on gut morphology and function. Gut 35 (1 Suppl), S35–S38.

    Article  CAS  Google Scholar 

  • Sghir A, Gramet G, Suau A, Rochet V, Pochart P, Dore J (2000). Quantification of bacterial groups within human faecal flora by oligonucleotide probe hybridization. Appl Environ Microbiol 66, 2263–2266.

    Article  CAS  Google Scholar 

  • Sonnenburg JL, Chen CT, Gordon JI (2006). Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol 4, e413.

    Article  Google Scholar 

  • Suau A, Rochet V, Sghir A, Gramet G, Brewaeys S, Sutren M et al. (2001). Fusobacterium prausnitzii and related species represent a dominant group within the human faecal flora. Syst Appl Microbiol 24, 139–145.

    Article  CAS  Google Scholar 

  • Topping DL, Clifton PM (2001). Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 81, 1031–1064.

    Article  CAS  Google Scholar 

  • Van Amelsvoort JM, Weststrate JA (1992). Amylose–amylopectin ratio in a meal affects postprandial variables in male volunteers. Am J Clin Nutr 55, 712–718.

    Article  CAS  Google Scholar 

  • Wallner G, Amann R, Beisker W (1993). Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14, 136–143.

    Article  CAS  Google Scholar 

  • World Health Organization (2009a). Management of Acute Diarrhea in Children: a Manual for Physicians and Other Health Workers. World Health Organization: Geneva, Switzerland. Report.

  • World Health Organization (2009b). Management of Severe Malnutrition: A Manual for Physicians And Other Senior Health Workers. World Health Organization: Geneva, Switzerland. Report.

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Acknowledgements

This study was conducted at the International Centre for Diarrhoeal Disease Research, Bangladesh, with support from Nestle Foundation, Lausanne, Switzerland (Grant no. 00332). ICDDR, B acknowledges the commitment of the Nestle Foundation to the centre's research efforts. We acknowledge the service and assistance of the physicians and nurses at the Dhaka Hospital of ICDDR, B. We are thankful to Dr GB Nair for assistance in conducting the study. We are also thankful to Professor Abu Sara Shamsur Rouf, Faculty of Pharmacy, University of Dhaka, for help with laboratory procedures.

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Monira, S., Hoq, M., Chowdhury, A. et al. Short-chain fatty acids and commensal microbiota in the faeces of severely malnourished children with cholera rehydrated with three different carbohydrates. Eur J Clin Nutr 64, 1116–1124 (2010). https://doi.org/10.1038/ejcn.2010.123

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