Skip to main content
SpringerLink
Log in

Benefits of combinative application of probiotic, enterocin M-producing strain Enterococcus faecium AL41 and Eleutherococcus senticosus in rabbits

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

This study presents the effects of the probiotic and enterocin M-producing strain Enterococcus faecium AL41 on microbiota, phagocytic activity (PA), oxidative stress, performance and biochemical parameters when applied individually or in combination with Eleutherococcus senticosus in rabbits. The novelty of the study lies in the use of our non-rabbit-derived strain (AL41 = CCM8558) which produces new enterocin M. Ninety-six post-weaned rabbits (Hyplus breed) aged 5 weeks were divided into three experimental groups, 24 in each: E. senticosus (ES, 30 g/100 kg) in feed, E. faecium AL41 (109 CFU/mL marked by rifampicin to differentiate it from other enterococci) in water, and ES + AL. AL41 colonized sufficiently in rabbits to reduce coliforms, staphylococci, pseudomonads and clostridia. Slight decrease in bacteria was also found in the caecum and appendix. Phagocytic activity was significantly increased in the experimental groups compared to the control group (CG) (p < 0.001; p < 0.05). Applications did not evoke oxidative stress. Biochemical parameters in blood and caecal organic acids were slightly influenced. Average daily weight gain was slightly higher in ES and AL + ES. Combinative application of E. faecium with E. senticosus can be beneficial in rabbits. AL41 strain alone and in combination with ES produced reduction in spoilage bacteria; the highest stimulation of PA was in the AL41 + ES group.

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

Similar content being viewed by others

References

  • Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783–801

    Article  CAS  PubMed  Google Scholar 

  • Chrastinová Ľ, Chrenková M, Polačiková M, Lauková A, Simonová M, Szabóová R, Strompfová V, Ondruška Ľ, Rafay J, Vasilková Z, Plachá I, Faix Š, Haviarová M, Mojto J (2009) Utilization of an extract product from ginseng supplementation in diets and different energy levels of granulated feed in the nutrition of rabbits. Arch Zootech 12:72–79

    Google Scholar 

  • Chytilová M (2013) Modulation of immune response in pigs by the use of probiotic lactobacilli and natural substances. PhD thesis. University of Veterinary Medicine and Pharmacy, Košice, Slovakia, pp 1–100

    Google Scholar 

  • Drozd J, Sawicka T, Prosinska J (2002) Estimation of humoral activity of Eleutherococcus senticosus. Acta Pol Pharm 59:395–401

    PubMed  Google Scholar 

  • Favaro L, Basaglia M, Casella S, Hue I, Doussel X, de Melo G, Franco BD, Todorov SD (2014) Bacteriocinogenic potential and safety evaluation of non-starter Enterococcus faecium strains isolated from home made white brine cheese. Food Microbiol 38:228–239

    Article  CAS  PubMed  Google Scholar 

  • Foulquié Moreno MR, Sarantinopoulos P, Tsakalidou E, de Vuyst L (2006) The role and application of enterococci in food and health. Int J Food Microbiol 106:1–24

    Article  PubMed  Google Scholar 

  • Girrafa G (2002) Enterococci from food. FEMS Microbiol Rev 26:163–171

    Article  Google Scholar 

  • Husáková E, Bobíková K, Stašová D (2014) Total IgA in spleen, bursa and intestine of chickens pretreated with E. faecium AL41 and challenged with Salmonella Enteritidis PT4. Food Agric Immunol 26:366–370

    Article  Google Scholar 

  • Kandričáková A (2014) Additive bacteria and their utilization for health (in Slovak), PhD thesis. University of Veterinary Medicine and Pharmacy, Košice Slovakia and Institute of Animal Physiology Slovak Academy of Sciences, Košice, Slovakia, pp 1–157

    Google Scholar 

  • Karaffová V, Bobíková K, Husáková E, Levkut M, Herich R, Revajová V, Levkutová M, Levkut M (2015) Interaction of TGF-β4 and IL-17 with IgA secretion in the intestine of chickens fed with E. faecium AL41 and challenged with S. Enteritidis. Res Vet Sci 100:75–79

    Article  PubMed  Google Scholar 

  • Kullisaar T, Shepetova J, Zilme K, Songisepp E, Rehema A, Mikelsaar M, Zimler M (2011) An antioxidant probiotic reduces postprandial lipemia and oxidative stress. Cent Eur J Biol 6:32–40

    Google Scholar 

  • Lauková A, Czikková S, Vasilková Z, Juriš P, Mareková M (1998) Occurrence of bacteriocin production among environmental enterococci. Lett Appl Microbiol 27:178–182

    Article  PubMed  Google Scholar 

  • Lauková A, Strompfová V, Ouwehand AC (2004) Adhesion properties of enterococci to intestinal mucus of different hosts. Vet Res Commun 28:647–655

  • Lauková A, Plachá I, Chrastinová Ľ, Simonová M, Szabóová R, Strompfová V, Jurčík R, Poráčová J (2008) Vplyv extraktu z rastliny Eleutherococcus senticosus na fagocytárnu aktivitu králikov. (Effect of Eleutherococcus senticosus extract on phagocytic ativity in rabbits (in Slovak). Slov Vet Res 33:251–252

    Google Scholar 

  • Lauková A, Chrastinová Ľ, Pogány Simonová M, Strompfová V, Plachá I, Čobanová K, Formelová Z, Chrenková M, Ondruška Ľ (2012) Enterococcus faecium AL 41: its enterocin M and their beneficial use in rabbits husbandry. Prob Antimicrob Prot 4:243–249

    Article  Google Scholar 

  • Lauková A, Kandričáková A, Ščerbová J (2015) Use of bacteriocin-producing, probiotic strain Enterococcus faecium AL41 to control intestinal microbiota in farm ostriches. Lett Appl Microbiol 60:531–535

    Article  PubMed  Google Scholar 

  • Levkut M, Revajová V, Lauková A, Ševčíková Z, Spišáková V, Faixová Z, Levkutová M, Strompfová V, Pistl J, Levkut M (2012) Leukocytic responses and intestinal mucin dynamics of broilers protected with Enterococcus faecium EF55 and challenged with Salmonella Enteritidis. Res Vet Sci 93:195–201

    Article  CAS  PubMed  Google Scholar 

  • Mareková M, Lauková A, Skaugen M, Nes IF (2007) Isolation and characterization of a new bacteriocin, termed enterocin M, produced by environmental isolate Enterococcus faecium AL41. J Ind Microbiol Biotechnol 34:533–537

    Article  PubMed  Google Scholar 

  • Müller T, Ulrich A, Ott EM, Müller M (2001) Identification of plant-associated enterococci. J Appl Microbiol 91:268–278

    Article  PubMed  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    CAS  PubMed  Google Scholar 

  • Plachá I, Pogány Simonová M, Čobanová K, Lauková A, Faix Š (2010) Effect of Enterococcus faecium AL41 and Thymus vulgaris essential oil on small intestine integrity and antioxidative status of laying hens. Res Vet Sci 89:257–261

    Article  PubMed  Google Scholar 

  • Poeta P, Costa D, Rojo-Bezares B, Zarazaga M, Klibi N, Rodrigues J, Torres C (2007) Detection of antimicrobial activities and bacteriocin structural genes in faecal enterococci of wild animals. Microbiol Res 162:257–263

    Article  CAS  PubMed  Google Scholar 

  • Pogány Simonová M, Lauková A, Chrastinová Ľ, Strompfová V, Faix Š, Vasilková Z, Ondruška Ľ, Jurčík R, Rafay J (2009) Enterococcus faecium CCM7420, bacteriocin PPB CCM7420 and their effect in the digestive tract of rabbits. Czech J Anim Sci 54:376–386

  • Pogány Simonová M, Lauková A, Chrastinová Ľ, Plachá I, Strompfová V, Čobanová K, Formelová Z, Chrenková M (2013) Combined administration of bacteriocin- producing, probiotic strain Enterococcus faecium CCM7420 with Eleutherococcus senticosus and their effect in rabbits. Pol J Vet Sci 16:619–627

    PubMed  Google Scholar 

  • Rinkinen M, Mätto J, Salminen S, Westermarck E, Ouwehand AC (2000) In vitro adhesion of lactic acid bacteria to canine small intestinal mucus. J Anim Physiol Anim Nutr 84:43–47

    Article  Google Scholar 

  • Rogala E, Skopinska-Rózewska E, Sawicka T, Sommer E, Prosinska J, Drozd J (2003) The influence of Eleuterococcus senticosus on cellular and humoral immunological response of mice. Pol J Vet Sci 6:37–39

    CAS  PubMed  Google Scholar 

  • Schirru S, Dimitrov Todorov S, Favaro L, Mangia NP, Basaglia M, Casella S, Comunian R, de Melo Franco Gombossy BD, Deiana P (2012) Sardinian goat’s milk as source of bacteriocinogenic potential protective cultures. Food Control 25:309–320

    Article  CAS  Google Scholar 

  • Schmolz MW, Sacher F, Aicher B (2001) The synthesis of Rantes, G-CSF, IL-4, IL-5, IL-6, IL-12 and IL-13 in human whole-blood cultures is modulated by an extract from Eleutherococcus senticosus L. roots. Phytother Res 15:268–270

    Article  CAS  PubMed  Google Scholar 

  • Simonová M, Marciňáková M, Strompfová V, Čobanová K, Gancarčíková S, Vasilková Z, Lauková A (2008) Effect of probiotics Lactobacillus rhamnosus GG and new isolate Enterococcus faecium EF2019 (CCM7420) on growth, blood parameters, microbiota and coccidia oocysts excretion in rabbits. Int J Prob Preb 3:7–14

    Google Scholar 

  • Siwicki AK, Skopinska-Rózewska E, Nartowska J, Malaczewska J, Wójcik R, Sommer E, Trapkowska S, Filewska M, Skurzak H (2004) Effect of immunostim plus—a standardized fixed combination of Schizandra chinensis with Eleutherococcus senticosus extracts on granulocyte activity and tumour angiogenesis in mice. Bull Vet Inst Pulawy 48:489–492

    Google Scholar 

  • Steimann GG, Esperester A, Joller P (2001) Immunopharmacological in vitro effects of Eleutherococcus senticosus extracts. Drug Res 51:76–83

    Google Scholar 

  • Szabóová R, Chrastinová Ľ, Lauková A, Strompfová V, Pogány Simonová M, Strompfová V, Vasilková Z, Plachá I, Čobanová K, Chrenková M (2012) Effect of combinative administration of bacteriocin-producing and probiotic strain Enterococcus faecium CCM 4231 and sage plant extract on rabbits. Afr J Microbiol Res 23:4868–4873

    Google Scholar 

  • Szolomicki S, Samochowiec L, Wójcicki J (2000) The influence of active components of Eleutherococcus senticosus on cellular defence and physical fitness in man. Phytother Res 14:30–35

    Article  CAS  PubMed  Google Scholar 

  • Vetvička V, Fornousek L, Kopeček J, Kaminková J, Kašparek L, Vránova M (1982) Phagocytosis of human blood leukocytes, a simple micro-method. Immunol Lett 97:100

    Google Scholar 

  • Wagner H, Proksch A, Riess-Maurer I, Vollmar A, Oodenthal S, Stuppner H, Jurcic K, Le Turdu M, Fang IN (1985) Immunostimulating action of polysaccharides (heteroglycans) from higher plants. Drug Res 35:1069–1075

    CAS  Google Scholar 

Download references

Acknowledgments

This work was partially supported by VEGA projects 2/0002/11 and 2/0004/14. We are grateful to Mrs. Margita Bodnárová for her skillful technical assistance. We would like to thank Dr. Rastislav Jurčík and Dr. Vladimír Párkányi for their kindness and help in blood sampling. Partial information concerning faeces microflora and biochemical values (lipids, proteins, etc.) was presented at the 8th International Conference on Biotechnology and Quality of Raw Material and Foodstuffs in Journal of Microbiology, Biotechnology and Food Sciences Vol. 2, 2013, 20672073—Chrenková, M., Chrastinová, Ľ., Lauková, A., Poláčiková, M., Formelová, Z., Plachá, I., Pogány Simonová, M., Szabóová, R., Ondruška, Ľ., Parkányi, V., Rafay, J., Jurčík, R., Strompfová, V.: The effect of dietary supplementation with herbal extracts on growth performance and health status of rabbits.

Author information

Authors and Affiliations

  1. Institute of Animal Physiology Slovak Academy of Sciences, Šoltésovej 4-6, 04001, Košice, Slovakia

    Andrea Lauková, Monika Pogány Simonová, Iveta Plachá, Klaudia Čobanová & Viola Strompfová

  2. National Agricultural and Food Centre, Hlohovecká 2, 95141, Nitra-Lužianky, Slovakia

    Ľubica Chrastinová, Zuzana Formelová, Mária Chrenková & Ľubomír Ondruška

Authors
  1. Andrea Lauková
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monika Pogány Simonová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ľubica Chrastinová
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Iveta Plachá
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Klaudia Čobanová
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zuzana Formelová
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mária Chrenková
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ľubomír Ondruška
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Viola Strompfová
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Lauková.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lauková, A., Simonová, M.P., Chrastinová, Ľ. et al. Benefits of combinative application of probiotic, enterocin M-producing strain Enterococcus faecium AL41 and Eleutherococcus senticosus in rabbits. Folia Microbiol 61, 169–177 (2016). https://doi.org/10.1007/s12223-015-0423-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-015-0423-x

Keywords

Search

Navigation