Skip to main content Accessibility help
×
×
Home

Supplementation with Lactobacillus paracasei or Pediococcus pentosaceus does not prevent diarrhoea in neonatal pigs infected with Escherichia coli F18

  • Anders D. Andersen (a1) (a2), Malene S. Cilieborg (a1) (a2), Charlotte Lauridsen (a3), Anne Louise Mørkbak (a4) and Per Torp Sangild (a1) (a5)...

Abstract

Infectious diarrhoea is a worldwide problem in newborns. Optimal bacterial colonisation may enhance gut maturation and protect against pathogenic bacteria after birth. We hypothesised that lactic acid bacteria (LAB) administration prevents pathogen-induced diarrhoea in formula-fed newborns. Newborn caesarean-delivered, colostrum-deprived term piglets on parenteral nutrition for the first 15 h, were used as models for sensitive newborn infants. A commercially available probiotic strain, Lactobacillus paracasei F19 (LAP, 2·6×108 colony-forming units (CFU)/kg per d) and a novel LAB isolate, Pediococcus pentosaceus (PEP, 1·3×1010 CFU/kg per d), were administered for 5 d with or without inoculation of the porcine pathogen, Escherichia coli F18 (F18, 1010 CFU/d). This resulted in six treatment groups: Controls (n 9), LAP (n 10), PEP (n 10), F18 (n 10), F18–LAP (n 10) and F18–PEP (n 10). The pathogen challenge increased diarrhoea and density of F18 in the intestinal mucosa (P<0·05). LAB supplementation further increased the diarrhoea score, relative to F18 alone (P<0·01). Intestinal structure and permeability were similar among groups, whereas brush border enzymes were affected in variable intestinal regions with decreased activities in most cases after F18 and LAB inoculation. Bacterial density in colon mucosa increased after F18 inoculation (P<0·05) but was unaffected by LAB supplementation. In colon contents, acetic and butyric acids were increased by PEP (P<0·05). The LAB used in this study failed to reduce E. coli-induced diarrhoea in sensitive newborn pigs. In vulnerable newborns there may be a delicate balance among bacterial composition and load, diet and the host. Caution may be required when administering LAB to compromised newborns suffering from enteric infections.

Copyright

Corresponding author

* Corresponding author: P. T. Sangild, fax+45 3533 2469, email pts@sund.ku.dk

Footnotes

Hide All

Contributed equally and should be considered joint first authors.

Footnotes

References

Hide All
1. Kosek, M, Bern, C & Guerrant, RL (2000) The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ 81, 197204.
2. Liu, L, Oza, S, Hogan, D, et al. (2015) Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet 385, 430440.
3. World Health Organization (2006) Week Epidemiol Rec 81, 97104.
4. Nagy, B & Fekete, PZ (2005) Enterotoxigenic Escherichia coli in veterinary medicine. Int J Med Microbiol 295, 443454.
5. Guarner, F & Malagelada, JR (2003) Gut flora in health and disease. Lancet 361, 512519.
6. Clemente, JC, Ursell, LK, Parfrey, LW, et al. (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148, 12581270.
7. Barbosa, T & Rescigno, M (2010) Host-bacteria interactions in the intestine: homeostasis to chronic inflammation. Wiley Interdiscip Rev Syst Biol Med 2, 8097.
8. Carlisle, EM & Morowitz, MJ (2013) The intestinal microbiome and necrotizing enterocolitis. Curr Opin Pediatr 25, 382387.
9. Morelli, L & Capurso, L (2012) FAO/WHO Guidelines on Probiotics: 10 Years Later. J Clin Gastroenterol 46, S1S2.
10. Freedman, SB, Ali, S, Oleszczuk, M, et al. (2013) Treatment of acute gastroenteritis in children: an overview of systematic reviews of interventions commonly used in developed countries. Evid Based Child Health 8, 11231137.
11. Bernaola Aponte, G, Bada Mancilla, CA, Carreazo, NY, et al. (2013) Probiotics for treating persistent diarrhoea in children. The Cochrane Database of Systematic Reviews 2013 20, CD007401.
12. Sangild, PT, Cranwell, PD & Hilsted, L (1992) Ontogeny of gastric function in the pig: acid secretion and the synthesis and secretion of gastrin. Biol Neonate 62, 363372.
13. Alakomi, HL, Skyttä, E, Saarela, M, et al. (2000) Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol 66, 20012005.
14. Shu, Q, Freeman, Q & Gill, HS (2001) Probiotic treatment using Bifidobacterium lactis HN019 reduces weanling diarrhea associated with rotavirus and Escherichia coli infection in a piglet model. J Pediatr Gastroenterol Nutr 33, 171177.
15. Zeyner, A & Boldt, E (2005) Effects of a probiotic Enterococcus faecium strain supplemented from birth to weaning on diarrhoea patterns and performance of piglets. J Anim Physiol Anim Nutr (Berl) 90, 2531.
16. Taras, D, Vahjen, W, Macha, M, et al. (2006) Performance, diarrhea incidence, and occurrence of Escherichia coli virulence genes during long-term administration of a probiotic Enterococcus faecium strain to sows and piglets. J Anim Sci 84, 608617.
17. Fairbrother, JM, Nadeau, É & Gyles, CL (2005) Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Anim Health Res Rev 6, 1739.
18. Frydendahl, K, Kåre Jensen, T, Strodl Andersen, J, et al. (2003) Association between the porcine Escherichia coli F18 receptor genotype and phenotype and susceptibility to colonisation and postweaning diarrhoea caused by E. coli O138:F18. Vet Microbiol 93, 3951.
19. Jensen, ML, Cilieborg, MS, Østergaard, MV, et al. (2012) Escherichia coli challenge in newborn pigs. J Anim Sci 90, 4345.
20. Cilieborg, MS, Sangild, PT, Jensen, ML, et al. (2017) α1,2-Fucosyllactose does not improve intestinal function or prevent Escherichia coli F18 diarrhea in newborn pigs. J Pediatr Gastroenterol Nutr 64, 310318.
21. Sangild, PT, Thymann, T, Schmidt, M, et al. (2013) Invited review: the preterm pig as a model in pediatric gastroenterology. J Anim Sci 91, 47134729.
22. Di Cerbo, A & Palmieri, B (2013) Lactobacillus Paracasei subsp. Paracasei F19; a farmacogenomic and clinical update. Nutr Hosp 28, 18421850.
23. Zampieri, N, Pietrobelli, A, Biban, P, et al. (2013) Lactobacillus paracasei subsp. paracasei F19 in Bell’s stage 2 of necrotizing enterocolitis. Minerva Pediatr 65, 353360.
24. Manurung, SI (2012) Fermented whey permeate for piglets – as a strategy to reduce post weaning diarrhea. PhD Thesis, Technical University of Denmark, Kgs Lyngby.
25. European Food Safety Authority (2010) Scientific Opinion on the maintenance of the list of QPS biological agents intentionally added to food and feed (2010 update). EFSA J 8, 156.
26. Cilieborg, MS, Thymann, T, Siggers, R, et al. (2011) The incidence of necrotizing enterocolitis is increased following probiotic administration to preterm pigs. J Nutr 141, 223230.
27. Wittig, W, Prager, R, Stamm, M, et al. (1994) Expression and plasmid transfer of genes coding for the fimbrial antigen F107 in porcine Escherichia coli strains. Zentralbl Bakteriol 281, 130139.
28. Jensen, ML, Sangild, PT, Lykke, M, et al. (2013) Similar efficacy of human banked milk and bovine colostrum to decrease incidence of necrotizing enterocolitis in preterm piglets. Am J Physiol Regul Integr Comp Physiol 305, R4R12.
29. Ståhl, M, Kokotovic, B, Hjulsager, CK, et al. (2011) The use of quantitative PCR for identification and quantification of Brachyspira pilosicoli, Lawsonia intracellularis and Escherichia coli fimbrial types F4 and F18 in pig feces. Vet Microbiol 151, 307314.
30. Hermann-Bank, ML, Skovgaard, K, Stockmarr, A, et al. (2013) The gut microbiotassay: a high-throughput qPCR approach combinable with next generation sequencing to study gut microbial diversity. BMC Genomics 14, 788.
31. Hermann-Bank, ML, Skovgaard, K, Stockmarr, A, et al. (2015) Characterization of the bacterial gut microbiota of piglets suffering from new neonatal porcine diarrhoea. BMC Veterinary Research 11, 139.
32. Canibe, N, Hojberg, O, Badsberg, JH, et al. (2007) Effect of feeding fermented liquid feed and fermented grain on gastrointestinal ecology and growth performance in piglets. J Anim Sci 85, 29592971.
33. Thymann, T, Møller, HK, Stoll, B, et al. (2009) Carbohydrate maldigestion induces necrotizing enterocolitis in preterm pigs. Am J Physiol Gastrointest Liver Physiol 297, G1115G1125.
34. Lin, J (2004) Too much short chain fatty acids cause neonatal necrotizing enterocolitis. Med Hypotheses 62, 291293.
35. Trevisi, P, Casini, L, Coloretti, F, et al. (2011) Dietary addition of Lactobacillus rhamnosus GG impairs the health of Escherichia coli F4-challenged piglets. Animal 5, 13541360.
36. Konstantinov, SR, Smidt, H, Akkermans, ADL, et al. (2008) Feeding of Lactobacillus sobrius reduces Escherichia coli F4 levels in the gut and promotes growth of infected piglets. FEMS Microbiol Ecol 66, 599607.
37. Zhu, YH, Li, XQ, Zhang, W, et al. (2014) Dose-dependent effects of Lactobacillus rhamnosus on serum interleukin-17 production and intestinal T-cell responses in pigs challenged with Escherichia coli . Appl Environ Microbiol 80, 17871798.
38. Li, XQ, Zhu, YH, Zhang, HF, et al. (2012) Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PLOS ONE 7, e40666.
39. Daudelin, JF, Lessard, M, Beaudoin, F, et al. (2011) Administration of probiotics influences F4 (K88)-positive enterotoxigenic Escherichia coli attachment and intestinal cytokine expression in weaned pigs. Vet Res 42, 69.
40. Siggers, RH, Siggers, J, Boye, M, et al. (2008) Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs. J Nutr 138, 14371444.
41. Jensen, ML, Thymann, T, Cilieborg, MS, et al. (2014) Antibiotics modulate intestinal immunity and prevent necrotizing enterocolitis in preterm neonatal piglets. Am J Physiol Regul Integr Comp Physiol 306, G59G71.
42. Lau, CSM & Chamberlain, RS (2015) Probiotic administration can prevent necrotizing enterocolitis in preterm infants: a meta-analysis. J Pediatr Surg 50, 14051412.
43. Repa, A, Thanhaeuser, M, Endress, D, et al. (2015) Probiotics (Lactobacillus acidophilus and Bifidobacterium bifidum) prevent NEC in VLBW infants fed breast milk but not formula. Pediatr Res 77, 381388.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed