Skip to main content Accessibility help
×
Home

Dietary supplementation with Bifidobacterium lactis NCC2818 from weaning reduces local immunoglobulin production in lymphoid-associated tissues but increases systemic antibodies in healthy neonates

  • Marie C. Lewis (a1), Dilip V. Patel (a1), Jenni Fowler (a1), Swantje Duncker (a2), Adrian W. Zuercher (a2), Annick Mercenier (a2) and Mick Bailey (a1)...

Abstract

Weaning is associated with a major shift in the microbial community of the intestine, and this instability may make it more acquiescent than the adult microbiota to long-term changes. Modulation achieved through dietary interventions may have potentially beneficial effects on the developing immune system, which is driven primarily by the microbiota. The specific aim of the present study was to determine whether immune development could be modified by dietary supplementation with the human probiotic Bifidobacterium lactis NCC2818 in a tractable model of weaning in infants. Piglets were reared by their mothers before being weaned onto a solid diet supplemented with B. lactis NCC2818, while sibling controls did not receive supplementation. Probiotic supplementation resulted in a reduction in IgA (P< 0·0005) and IgM (P< 0·009) production by mucosal tissues but had no effect on IgG production (P>0·05). Probiotic-supplemented pigs had more mast cells than unsupplemented littermates (P< 0·0001), although numbers in both groups were low. In addition, the supplemented piglets made stronger serum IgG responses to fed and injected antigens (P< 0·05). The present findings are consistent with B. lactis NCC2818 reducing intestinal permeability induced by weaning, and suggest that the piglet is a valuable intermediate between rodent models and human infants. The results also strongly suggest that measures of the effect of probiotic supplementation on the immune system need to be interpreted carefully as proxy measures of health benefit. However, they are useful in developing an understanding of the mechanism of action of probiotic strains, an important factor in predicting favourable health outcomes of nutritional intervention.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Dietary supplementation with Bifidobacterium lactis NCC2818 from weaning reduces local immunoglobulin production in lymphoid-associated tissues but increases systemic antibodies in healthy neonates
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Dietary supplementation with Bifidobacterium lactis NCC2818 from weaning reduces local immunoglobulin production in lymphoid-associated tissues but increases systemic antibodies in healthy neonates
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Dietary supplementation with Bifidobacterium lactis NCC2818 from weaning reduces local immunoglobulin production in lymphoid-associated tissues but increases systemic antibodies in healthy neonates
      Available formats
      ×

Copyright

Corresponding author

*Corresponding author: Dr M. C. Lewis, fax +44 1179 289 505, email marie.lewis@bristol.ac.uk

References

Hide All
1Falk, PG, Hooper, LV, Midtvedt, T, et al. (1998) Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol Mol Biol Rev 62, 11571170.
2Stecher, B & Hardt, WD (2008) The role of microbiota in infectious disease. Trends Microbiol 16, 107114.
3Lewis, MC, Inman, CF, Patel, D, et al. (2012) Direct experimental evidence that early-life farm environment influences regulation of immune responses. Pediatr Aller Immunol 23, 265269.
4Mulder, I, Schmidt, B, Stokes, C, et al. (2009) Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biol 7, 79.
5Mulder, IE, Schmidt, B, Lewis, M, et al. (2011) Restricting microbial exposure in early life negates the immune benefits associated with gut colonization in environments of high microbial diversity. PLoS One 6, e28279.
6Schmidt, B, Mulder, IE, Musk, CC, et al. (2011) Establishment of normal gut microbiota is compromised under excessive hygiene conditions. PLoS One 6, e28284.
7Noverr, MC & Huffnagle, GB (2004) Does the microbiota regulate immune responses outside the gut? Trends Microbiol 12, 562568.
8Moore, WEC & Moore, LH (1995) Intestinal floras of populations that have a high-risk of colon-cancer. Appl Environ Microbiol 61, 32023207.
9Palmer, C, Bik, EM, DiGiulio, DB, et al. (2007) Development of the human infant intestinal microbiota. PLoS Biol 5, 15561573.
10West, CE, Hammarstrom, ML & Hernell, O (2009) Probiotics during weaning reduce the incidence of eczema. Pediatr Aller Immunol 20, 430437.
11Cox, MJ, Huang, YJ, Fujimura, KE, et al. (2010) Lactobacillus casei abundance is associated with profound shifts in the infant gut microbiome. PLoS One 5, e8745.
12Carter, PB & Pollard, M (1971) Host responses to normal microbial flora in germ-free mice. J Reticuloendothel Soc 9, 580587.
13Cebra, JJ (1999) Influences of microbiota on intestinal immune system development. Am J Clin Nutr 69, 1046S1051S.
14Cebra, JJ, Periwal, SB, Lee, G, et al. (1998) Development and maintenance of the gut-associated lymphoid tissue (GALT): the roles of enteric bacteria and viruses. Dev Immunol 6, 1318.
15Talham, GL, Jiang, HQ, Bos, NA, et al. (1999) Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect Immun 67, 19922000.
16Butler, JE, Weber, P, Sinkora, M, et al. (2000) Antibody repertoire development in fetal and neonatal piglets. II. Characterization of heavy chain complementarity-determining region 3 diversity in the developing fetus. J Immunol 165, 69997010.
17Ivanov, II, Frutos Rde, L, Manel, N, et al. (2008) Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337349.
18Bjorksten, B, Sepp, E, Julge, K, et al. (2001) Allergy development and the intestinal microflora during the first year of life. J Aller Clin Immunol 108, 516520.
19Sekirov, I, Tam, NM, Jogova, M, et al. (2008) Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun 76, 47264736.
20Iannitti, T & Palmieri, B (2010) Therapeutical use of probiotic formulations in clinical practice. Clin Nutr 29, 701725.
21Kalliomaki, M, Antoine, JM, Herz, U, et al. (2010) Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of allergic diseases by probiotics. J Nutr 140, 713s721s.
22Paton, AW, Morona, R & Paton, JC (2000) A new biological agent for treatment of Shiga toxigenic Escherichia coli infections and dysentery in humans. Nat Med 6, 265270.
23Villena, J, Oliveira, MLS, Ferreira, PCD, et al. (2011) Lactic acid bacteria in the prevention of pneumococcal respiratory infection: future opportunities and challenges. Int Immunopharmacol 11, 16331645.
24Zakostelska, Z, Kverka, M, Klimesova, K, et al. (2011) Lysate of probiotic Lactobacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS One 6, e27961.
25Magne, F, Hachelaf, W, Suau, A, et al. (2006) A longitudinal study of infant faecal microbiota during weaning. FEMS Microbiol Ecol 58, 563571.
26Konstantinov, SR, Awati, AA, Williams, BA, et al. (2006) Post-natal development of the porcine microbiota composition and activities. Environ Microbiol 8, 11911199.
27Gandarillas, M & Bas, F (2009) The domestic pig (Sus scrofa domestica) as a model for evaluating nutritional and metabolic consequences of bariatric surgery practiced on morbid obese humans. Cienc Investig Agraria 36, 163176.
28Kararli, TT (1995) Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory-animals. Biopharm Drug Dispos 16, 351380.
29Merrifield, CA, Lewis, M, Claus, SP, et al. (2011) A metabolic system-wide characterisation of the pig: a model for human physiology. Mol BioSyst 7, 25772588.
30Pittner, A, Nalos, M, Asfar, P, et al. (2003) Mechanisms of inducible nitric oxide synthase (iNOS) inhibition-related improvement of gut mucosal acidosis during hyperdynamic porcine endotoxemia. Intensive Care Med 29, 312316.
31Tadros, T, Traber, DL, Heggers, JP, et al. (2003) Effects of interleukin-1 alpha administration on intestinal ischemia and reperfusion injury, mucosal permeability, and bacterial translocation in burn and sepsis. Ann Surg 237, 101109.
32Thompson, CL, Hofer, MJ, Campbell, IL, et al. (2010) Community dynamics in the mouse gut microbiota: a possible role for IRF9-regulated genes in community homeostasis. PLoS One 5, e10335.
33Wernersson, R, Schierup, MH, Jorgensen, FG, et al. (2005) Pigs in sequence space: a 0.66X coverage pig genome survey based on shotgun sequencing. BMC Genomics 6, 70.
34Jorgensen, FG, Hobolth, A, Hornshoj, H, et al. (2005) Comparative analysis of protein coding sequences from human, mouse and the domesticated pig. BMC Biol 3, 2.
35Logan, AC, Chow, KPN, George, A, et al. (1991) Use of Peyer patch and lymph-node fragment cultures to compare local immune-responses to Morganella morganii. Infect Immun 59, 10241031.
36Bailey, M, Haverson, K, Miller, B, et al. (2004) Effects of infection with transmissible gastroenteritis virus on concomitant immune responses to dietary and injected antigens. Clin Diagn Lab Immunol 11, 337343.
37Inman, CF, Rees, LEN, Barker, E, et al. (2005) Validation of computer-assisted, pixel-based analysis of multiple-colour immunofluorescence histology. J Immunol Methods 302, 156167.
38Ishibashi, N & Shimamura, S (1993) Bifidobacteria – research and development in Japan. Food Technology [Proceedings Paper] 47, 126135.
39Harata, G, He, F, Takahashi, K, et al. (2010) Bifidobacterium suppresses IgE-mediated degranulation of rat basophilic leukemia (RBL-2H3) cells. Microbiol Immunol 54, 5457.
40Mohan, R, Koebnick, C, Schildt, J, et al. (2008) Effects of Bifidobacterium lactis Bb12 supplementation on body weight, fecal pH, acetate, lactate, calprotectin, and IgA in preterm infants. Pediatr Res 64, 418422.
41Park, JH, Um, JI, Lee, BJ, et al. (2002) Encapsulated Bifidobacterium bifidum potentiates intestinal IgA production. Cell Immunol 219, 2227.
42Kukkonen, K, Kuitunen, M, Haahtela, T, et al. (2010) High intestinal IgA associates with reduced risk of IgE-associated allergic diseases. Pediatr Aller Immunol 21, 6773.
43Berstad, AE, Kilian, M, Valnes, KN, et al. (1999) Increased mucosal production of monomeric IgA1 but no IgA1 protease activity in Helicobacter pylori gastritis. Am J Pathol 155, 10971104.
44Kett, K, Scott, H, Fausa, O, et al. (1990) Secretory immunity in celiac-disease – cellular expression of immunoglobulin – a subclass and joining chain. Gastroenterology 99, 386392.
45Valnes, K, Brandtzaeg, P, Elgjo, K, et al. (1986) Quantitative distribution of immunoglobulin-producing cells in gastric-mucosa – relation to chronic gastritis and glandular atophy. Gut 27, 505514.
46Sun, P, Li, DF, Li, ZJ, et al. (2008) Effects of glycinin on IgE-mediated increase of mast cell numbers and histamine release in the small intestine. J Nutr Biochem 19, 627633.
47Smith, F, Clark, JE, Overman, BL, et al. (2010) Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am J Physiol Gastrointest Liver Physiol 298, G352GG63.
48Che, C, Pang, X, Hua, X, et al. (2009) Effects of human fecal flora on intestinal morphology and mucosal immunity in human flora-associated piglet. Scand J Immunol 69, 223233.
49Duncker, SC, Lorentz, A, Schroeder, B, et al. (2006) Effect of orally administered probiotic E-coli strain Nissle 1917 on intestinal mucosal immune cells of healthy young pigs. Vet Immunol Immunopathol; 111, 239250.
50Gelbmann, CM, Mestermann, S, Gross, V, et al. (1999) Strictures in Crohn's disease are characterised by an accumulation of mast cells colocalised with laminin but not with fibronectin or vitronectin. Gut 45, 210217.
51Crowe, SE, Luthra, GK & Perdue, MH (1997) Mast cell mediated ion transport in intestine from patients with and without inflammatory bowel disease. Gut 41, 785792.
52Li, DF, Nelssen, JL, Reddy, PG, et al. (1991) Interrelationship between hypersensitivity to soybean proteins and growth-performance in early-weaned pigs. J Anim Sci 69, 40624069.
53Strait, RT, Mahler, A, Hogan, S, et al. (2011) Ingested allergens must be absorbed systemically to induce systemic anaphylaxis. J Allergy Clin Immunol 127, 982–9e1.
54Snoeck, V, Verfaillie, T, Verdonck, F, et al. (2006) The jejunal Peyer's patches are the major inductive sites of the F4-specific immune response following intestinal immunisation of pigs with F4 (K88) fimbriae. Vaccine 24, 38123820.
55Hadis, U, Wahl, B, Schulz, O, et al. (2011) Intestinal tolerance requires gut homing and expansion of FoxP3(+) regulatory t cells in the lamina propria. Immunity 34, 237246.
56Resta-Lenert, S & Barrett, KE (2006) Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterology 130, 731746.
57Otte, JM & Podolsky, DK (2004) Functional modulation of enterocytes by gram-positive and gram-negative microorganisms. Am J Physiol Gastrointest Liver Physiol 286, G613G626.
58Khailova, L, Dvorak, K, Arganbright, KM, et al. (2009) Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 2009 297, G940G949.

Keywords

Metrics

Altmetric attention score

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