Skip to main content

Advertisement

SpringerLink
Log in

Characterization of Bifidobacterium spp. strains for the treatment of enteric disorders in newborns

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Several studies support the use of probiotics for the treatment of minor gastrointestinal problems in infants. Positive effects on newborn colics have been evidenced after administration of Lactobacillus strains, whereas no studies have been reported regarding the use of bifidobacteria for this purpose. This work was therefore aimed at the characterization of Bifidobacterium strains capable of inhibiting the growth of pathogens typical of the infant gastrointestinal tract and of coliforms isolated from colic newborns. Among the 46 Bifidobacterium strains considered, 16 showed high antimicrobial activity against potential pathogens; these strains were further characterized from a taxonomic point of view, for the presence and transferability of antibiotic resistances, for citotoxic effects and adhesion to nontumorigenic gut epithelium cell lines. Moreover, their ability to stimulate gut health by increasing the metabolic activity and the immune response of epithelial cells was also studied. The examination of all these features allowed to identify three Bifidobacterium breve strains and a Bifidobacterium longum subsp. longum strain as potential probiotics for the treatments of enteric disorders in newborns such as infantile colics. A validation clinical trial involving the selected strains is being planned.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aires J, Doucet-Populaire F, Butel MJ (2007) Tetracycline resistance mediated by tet(W), tet(M), and tet(O) genes of Bifidobacterium isolates from humans. Appl Environ Microbiol 73:2751–2754

    Article  CAS  Google Scholar 

  • Ammor MS, Flórez AB, Van Hoek AHAM, De Los Reyes-Gavilán CG, Aarts HJM, Margolles A, Mayo B (2008) Molecular characterization of intrinsic and acquired antibiotic resistance in lactic acid bacteria and bifidobacteria. J Mol Microbiol Biotechnol 14:6–15

    Article  CAS  Google Scholar 

  • Arboleya S, Ruas-Madiedo P, Margolles A, Solis G, Salminen S, De los Reyes-Gavilan CG, Gueimonde M (2011) Characterization and in vitro properties of potentially probiotic Bifidobacterium strains isolated from breast-milk. Int J Food Microbiol 149:28–36

    Article  CAS  Google Scholar 

  • Benzecri JP (1992) Correspondence analyses handbook. CRC Press, Boca Raton

    Google Scholar 

  • Biavati B, Mattarelli P (2006) The Family Bifidobacteriaceae prokaryotes: a handbook on the biology of bacteria, 3rd ed, vol 3. Springer, New York, pp 322–382

    Google Scholar 

  • Burrus V, Waldor MK (2003) Control of SXT integration and excision. J Bacteriol 185:5045–5054

    Article  CAS  Google Scholar 

  • Cencic A, Langerholc T (2010) Functional cell models of the gut and their applications in food microbiology—a review. Int J Food Microbiol 141:S4–S14

    Article  Google Scholar 

  • D’Aimmo MR, Modesto M, Biavati B (2007) Antibiotic resistance of lactic acid bacteria and Bifidobacterium spp. isolated from dairy and pharmaceutical products. Int J Food Microbiol 115:35–42

    Article  Google Scholar 

  • EFSA (2005) Opinion of the scientific committee on a request from EFSA related to a generic approach to the safety assessment by EFSA of microorganisms used in food/feed and the production of food/feed additives. EFSA J 226:1–12

    Google Scholar 

  • EFSA (2008) Opinion of the Scientific Panel on Additives and Products or Substances used in Animal Feed on the updating of the criteria used in the assessment of bacteria for resistance to antibiotics of human or veterinary importance. EFSA Journal 223:1–12

    Google Scholar 

  • Guarner F (2006) Enteric flora in health and disease. Digestion 73:5–12

    Article  Google Scholar 

  • Hammerman C, Bin-Nun A, Kaplan M (2006) Safety of probiotics: comparision of two popular strains. BMJ 333:1006–1008

    Article  Google Scholar 

  • Indrio F, Riezzo G, Raimondi F, Bisceglia M, Cavallo L, Francavilla R (2008) The effects of probiotics on feeling tolarance, bowel habitus and gastrointestinal motility in preterm newborns. J Pediatr 152:801–806

    Article  Google Scholar 

  • Ivec M, Botic T, Koren S, Jakobsen M, Weingartl H, Cencic A (2007) Interaction of macrophages with probiotic bacteria lead to increase antiviral response against vesicular stomatitis virus. Antiviral Res 75:266–274

    Article  CAS  Google Scholar 

  • Kiwaki M, Sato T (2009) Antimicrobial susceptibility of Bifidobacterium breve strains and genetic analysis of streptomycin resistance of probiotic B. breve strain Yakult. Int J Food Microbiol 134:211–215

    Article  CAS  Google Scholar 

  • Lampkowska J, Feld L, Monaghan A, Toomey N, Schjørring S, Jacobsen B (2008) A standardized conjugation protocol to asses antibiotic resistance transfer between lactococcal species. Int J Food Microbiol 127:172–175

    Article  CAS  Google Scholar 

  • Li Y, Shimizu T, Hosaka A, Kaneko N, Ohtsuka Y, Yamashiro Y (2004) Effects of Bifidobacterium breve supplementation on intestinal flora of low birth weight infants. Pediatr Int 46:509–515

    Article  Google Scholar 

  • Lin J (2004) Too much short chain fatty acids cause neonatal necrotizing enterocolitis. Med Hypotheses 62:291–293

    Article  CAS  Google Scholar 

  • Maragkoudakis PA, Chingwaru W, Gradisnik L, Tsakalidou E, Cencic A (2010) Lactic acid bacteria efficiently protect human and animal epithelial and immune cells from enteric virus infection. Int J Food Microbiol 141:S91–S97

    Article  Google Scholar 

  • Masco L, Van Hoorde K, De Brandt E, Swings J, Huys G (2006) Antimicrobial susceptibility of Bifidobacterium strains from humans, animals and probiotic products. J Antimicrob Chemother 58:85–94

    Article  CAS  Google Scholar 

  • Matsuki T, Watanabe K, Tanaka R, Fukuda M, Oyaizu H (1999) Distribution of bifidobacterial species in human intestinal microflora examined with 16S rRNA-gene-targeted species-specific primers. Appl Environ Microbiol 65:4506–4512

    CAS  Google Scholar 

  • Matto J, Vanhoek A, Domig K, Saarela M, Florez A, Brockmann E (2007) Susceptibility of human and probiotic Bifidobacterium spp. to selected antibiotics as determined by the Etest method. Int Diary J 17:1123–1131

    Article  CAS  Google Scholar 

  • Mohan R, Koebnick C, Schildt J, Schmidt S, Mueller M, Possner M (2006) Effects of Bifidobacterium lactis Bb12 supplementation on intestinal microbiota of preterm infants: a double-blind, placebo-controlled, randomized study. J Clin Microbiol 44:4025–4031

    Article  Google Scholar 

  • Nissen L, Chingwaru W, Sgorbati B, Biavati B, Cencic A (2009) Gut health promoting activity of new putative probiotic/protective Lactobacillus spp. strains: a functional study in the small intestinal cell model. Int J Food Microbiol 135:288–294

    Article  CAS  Google Scholar 

  • Ouoba L, Lei V, Jensen LB (2008) Resistance of potential probiotic lactic acid bacteria and bifidobacteria of African and European origin to antimicrobials: determination and transferability of the resistance genes to other bacteria. Int J Food Microbiol 121:217–224

    Article  CAS  Google Scholar 

  • Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:1556–1573

    Article  CAS  Google Scholar 

  • Park SY, Ji GE, Ko YT, Jung HK, Ustunol Z, Pestka JJ (1999) Potential of hydrogen peroxide, nitric oxide and cytokine production in RAW 264.7 macrophage cells exposed to human and commercial isolates of Bifidobacterium. Int J Food Microbiol 46:231–241

    Article  CAS  Google Scholar 

  • Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, Van Den Brandt PA (2006) Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118:511–521

    Article  Google Scholar 

  • Pipenbaher N, Moeller PL, Dolinšek J, Jakobsen M, Weingartl H, Cencic A (2009) Nitric oxide (NO) production in mammalian nontumorigenic epithelia cells of the small intestine and macrophages induced by individual strains of lactobacilli and bifidobacteria. Int Dairy J 19:166–171

    Article  CAS  Google Scholar 

  • Roessler A, Friedrich U, Vogelsang H, Bauer A, Kaatz M, Hipler UC, Schmidt I, Jahreis G (2008) The immune system in healthy adults and patients with atopic dermatitis seems to be affected differently by a probiotic intervention. Clin Exp Allergy 38:93–102

    CAS  Google Scholar 

  • Roncaglia L, Amaretti A, Raimondi S, Leonardi A, Rossi M (2011) Role of bifidobacteria in the activation of the lignan secoisolariciresinol diglucoside. Appl Microbiol Biotechnol 92:159–168

    Article  CAS  Google Scholar 

  • Rowland IR (2008) Prebiotics in human medicine. In: Versalovic J, Wilson M (eds) Therapeutic microbiology: probiotics and related strategies. American Society for Microbiology, Washington DC, pp 299–306

    Google Scholar 

  • Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J, Hörmannsperger G, Huys G, Levy DD, Lutgendorff F, Mack D, Phothirath P, Solano-Aguilar G, Vaughan E (2010) Safety assessment of probiotics for human use. Gut Microbes 1:164–185

    Article  Google Scholar 

  • Santini C, Baffoni L, Gaggia F, Granata M, Gasbarri R, Di Gioia D (2010) Characterization of probiotic strains: an application as feed additives in poultry against Campylobacter jejuni. Int J Food Microbiol 141:S98–S108

    Article  Google Scholar 

  • SAS STAT (1988) User’s guide. Release 6.03 edition. SAS Institute, Cary

    Google Scholar 

  • Satokari RM, Vaughan EE, Akkermans ADL, Saarela M (2001) Bifidobacterial diversity in human feces detected by genus-specific PCR and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67:504–513

    Article  CAS  Google Scholar 

  • Savino F, Cordisco L, Tarasco V, Calabrese R, Palumeri E, Matteuzzi D (2009) Molecular identification of coliform bacteria from colicky breastfed infants. Acta Paediatr 98:1582–1588

    Article  CAS  Google Scholar 

  • Savino F, Cordisco L, Tarasco V, Palumeri E, Calabrese R, Oggero R, Roos S, Matteuzzi D (2010) Lactobacillus reuteri DSM 17939 in infantile colic: a randomized, double-blind, placebo-controlled trial. Pediatrics 126:526–533

    Article  Google Scholar 

  • Savino F, Cordisco L, Tarasco V, Locatelli E, Di Gioia D, Oggero R (2011) Antagonistic effect of Lactobacillus strains against gas-producing coliforms isolated from colicky infants. BMC Microbiol 11:157

    Article  Google Scholar 

  • Scardovi V, Casalicchio F, Vincenzi N (1979) Multiple electrophoretic forms of transaldolase and 6-phosphogluconic dehydrogenase and their relationships to the taxonomy and ecology of the bifidobacteria. Int J Syst Bacteriol 29:312–327

    Article  CAS  Google Scholar 

  • Serikov I, Russel SL, Antunes LCM, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904

    Article  Google Scholar 

  • Taylor AL, Hale J, Wiltschut J, Lehmann H, Dunstan JA, Prescott SL (2006) Effects of probiotic supplementation for the first 6 months of life on allergen- and vaccine-specific immune responses. Clin Exp Allergy 36:1227–1235

    Article  CAS  Google Scholar 

  • Tremblay LN, Slutsky AS (2007) Ventilator- induced lung inujury: from the bench to the bedside. Intensive Care Med 32:24–33

    Article  Google Scholar 

  • Van Hoek AH, Mayrhofer S, Domig K, Florez A, Ammor M, Mayo B, Aarts HM (2008) Mosaic tetracycline resistance genes and their flanking regions in Bifidobacterium thermophilum and Lactobacillus johsonii. Antimicrob Agents Chemother 52:248–252

    Article  Google Scholar 

  • Van Niel CW, Feudtner C, Garrison MM, Christakis DA (2002) Lactobacillus therapy for acute infectious diarrhea in children: a meta-analysis. Pediatrics 109:678–684

    Article  Google Scholar 

  • Ventura M, Meylan V, Zink R (2003) Identification and tracing of Bifidobacterium species by use of enterobacterial repetitive intergenic consensus sequences. Appl Environ Microbiol 69:4296–4301

    Article  CAS  Google Scholar 

  • Ventura M, Van Sinderen D, Fitzgerald GF, Zink R (2004) Insights into the taxonomy, genetics and physiology of bifidobacteria. Antonie Van Leeuwenhoek 86:205–223

    Article  CAS  Google Scholar 

  • Ventura M, Turroni F, Ribbera A, Foroni E, Van Sideren D (2008) Bifidobacteria: the model human gut commensal. In: Versalovic J, Wilson M (eds) Therapeutic microbiology: probiotics and related strategies. American Society for Microbiology, Washington, DC, pp 35–50

    Google Scholar 

  • Wada M, Nagata S, Saito M, Shimizu T, Yamashiro Y, Matsuki T (2010) Effects of the enteral administration of Bifidobacterium breve on patients undergoing chemotherapy for pediatric malignancies. Support Care Cancer 18:751–757

    Article  Google Scholar 

  • Wang C, Shoji H, Sato H, Nagata S, Ohtsuka Y, Shimizu T (2007) Effects of oral administration of Bifidobacterium breve on fecal lactic acid and short-chain fatty acids in low birth weight infants. J Pediatr Gastroenterol Nutr 44:252–257

    Article  CAS  Google Scholar 

Download references

Aknowledgments

The study was funded by the University of Bologna, Program RFO number J61J10000790001, assigned to Prof. Bruno Biavati. The authors are grateful to Dr. Giovanni Mogna and Dr. Paolo Strozzi of Probiotical SpA for fruitful discussions.

Author information

Authors and Affiliations

  1. Department of Agroenvironmental Sciences and Technologies, University of Bologna, viale Fanin 42, 40127, Bologna, Italy

    Irene Aloisio, Cecilia Santini, Bruno Biavati, Giovanni Dinelli & Diana Di Gioia

  2. Department of Microbiology, Biochemistry, and Biotechnology, Faculty of Agriculture and Life Sciences, University of Maribor, Pivola 10, 2311, Hoče, Slovenia

    Avrelija Cencič & Walter Chingwaru

  3. Department of Biochemistry and Nutrition, Faculty of Medicine, University of Maribor, Slomškov trg 15, 2000, Maribor, Slovenia

    Avrelija Cencič

  4. Probiotical SpA, via E. Mattei 3, 28100, Novara, Italy

    Luca Mogna

Authors
  1. Irene Aloisio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cecilia Santini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruno Biavati
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Giovanni Dinelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Avrelija Cencič
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Walter Chingwaru
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luca Mogna
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Diana Di Gioia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Diana Di Gioia.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

PDF 15 kb

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aloisio, I., Santini, C., Biavati, B. et al. Characterization of Bifidobacterium spp. strains for the treatment of enteric disorders in newborns. Appl Microbiol Biotechnol 96, 1561–1576 (2012). https://doi.org/10.1007/s00253-012-4138-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-012-4138-5

Keywords

Search

Navigation