African Journal of
Microbiology Research

  • Abbreviation: Afr. J. Microbiol. Res.
  • Language: English
  • ISSN: 1996-0808
  • DOI: 10.5897/AJMR
  • Start Year: 2007
  • Published Articles: 5254

Full Length Research Paper

In vitro evaluation of probiotic potential of five lactic acid bacteria and their antimicrobial activity against some enteric and food-borne pathogens

Sameh Ali Gad
  • Sameh Ali Gad
  • Department of Microbiology and Immunology, Faculty of Pharmacy, Minia University, 61519-Minia, Egypt.
  • Google Scholar
Rehab Mahmoud Abd El-Baky
  • Rehab Mahmoud Abd El-Baky
  • Department of Microbiology and Immunology, Faculty of Pharmacy, Minia University, 61519-Minia, Egypt.
  • Google Scholar
Abo Bakr F Ahmed
  • Abo Bakr F Ahmed
  • Faculty of Pharmacy, Hail University, KSA.
  • Google Scholar
Gamal Fadl Mahmoud Gad
  • Gamal Fadl Mahmoud Gad
  • Department of Microbiology and Immunology, Faculty of Pharmacy, Minia University, 61519-Minia, Egypt.
  • Google Scholar


  •  Received: 27 September 2015
  •  Accepted: 18 February 2016
  •  Published: 28 March 2016

References

Ammor S, Tauveron G, Dofour E, Chevallier I (2006). Antibacterial activity of lactic acid bacteria against spoilage and pathogenic bacteria isolated from the same meat small-scale facility: 1 Screening and characterization of the antibacterial compounds. Food Contr. 17:454-461.
Crossref

 

Andersson DI, Hughes D (2010). Antibiotic resistance and its cost: Is it possible to reverse resistance? Nat. Rev. Microbiol. 8(4):260-271.
Crossref

 
 

Ashokkumar S, Sree Krishna R, Pavithra V, Hemalatha V, Ingale P (2011). Production and antibacterial activity of bacteriocin by Lactobacillus paracasei isolated from donkey milk. Int. J. Curr. Sci. 1:109-115.

 
 

Asoodeh A, Chamani J, Lagziana M (2010). A novel thermostable, acidophilic α-amylase from a new thermophilic "Bacillus sp. ferdowsicous" isolated from Ferdows hot mineral spring in Iran: Purification and biochemical characterization. Int. J. Biol. Macromol. 46:289-297.
Crossref

 
 

Aureli P, Capurso L, Castellazzi AM, Clerici M, Giovannini M, Morelli L, Poli A, Pregliasco F, Salvini F, Zuccotti GV (2011). Probiotics and health: An evidence-based review. Pharmacol. Res. 63:366-376.
Crossref

 
 

Begley M, Cormac GMG, Hill C (2005). The interaction between bacteria and bile. FEMS Microbiol. Rev. 29:625-651.
Crossref

 
 

Bendali F, Durand A, Hébraud M, Sadoun D (2011). Lactobacillus paracasei subsp. paracasei: an Algerian isolate with antibacterial activity against enteric pathogens and probiotic fitness. J. Food Nutr. Res. 50(3):139-149.

 
 

Bernbom N, Licht TR, Saadbye P, Vogensen FK, Nørrung B (2006). Lactobacillus plantarum inhibits growth of Listeria monocytogenes in an in-vitro continuous flow gut model, but promotes invasion of L. monocytogenes in the gut of gnotobiotic rats. Int. J. Food Microbiol. 108:10-14.
Crossref

 
 

Black RE, Morris SS, Bryce J (2003). Where and why are 10 million children dying every year? Lancet 361:2226-2234.
Crossref

 
 

Charteris WP, Kelly PM, Morelli L, Collins JK (1998). Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J. Appl. Microbiol. 84(5):759-768.
Crossref

 
 

Christensen JE, Dudley EG, Pederson JA, Steele JL (1999). Peptidases and amino acid catabolism in lactic acid bacteria. Antonie Van Leeuwenhoek. 76:217-246.
Crossref

 
 

Chung H, Yousef AE (2010). Synergistic effect of high pressure processing and Lactobacillus casei antimicrobial activity against pressure resistant Listeria monocytogenes. New Biotechnol. 27(4):403-408.
Crossref

 
 

Clark PA, Cotton LN, Martin JH (1993). Selection of Bifidobacterium sp. for use as dietary adjuncts in cultured dairy foods: II-Tolerance to simulated pH of human stomachs. Cult. Dairy Prod. J. 28:11-14.

 
 

Coconnier MH, Liévin V, Bernet-Camard MF, Hudault S, Servin AL (1997). Antibacterial effect of the adhering human Lactobacillus acidophilus strain LB. Antimicrob. Agents Chemother. 41:1046-1052.

 
 

Collado MC, Gonz'alez A, Gonz'alez R, Hern'andez M, Ferr'us MA, Sanz Y (2005). Antimicrobial peptides are among the antagonistic metabolites produced by Bifidobacterium against Helicobacter pylori. Int. J. Antimicrob. Agents. 25:385-391.
Crossref

 
 

Collee JG, Miles RS, Watt B (1996). Tests for identification of bacteria In: Collee JG, Fraser AG, Marmion BP, Simmons A (ed): Mackie and McCarteny Practical Medical Microbiology, 14th ed, Churchill livingstone In, New York. pp.131:149.

 
 

Collins B, Caitriona M, Guinane PD, Cotter CH (2012). Assessing the contributions of the LiaS histidine kinase to the innate resistance of Listeria monocytogenes to nisin, cephalosporins, and disinfectants. Appl. Environ. Microbiol. 78(8):2923-2929.
Crossref

 
 

Condon S (1987). Responses of lactic acid bacteria to oxygen. FEMS Microbiol. Lett. 46:269-280.
Crossref

 
 

Conway PL, Gorbach SL, Goldin BR (1987). Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells. J. Dairy Sci. 70:1-12.
Crossref

 
 

Crittenden R, Saarela M, Mättö J, Ouwehand AC, Salminen S, Pelto L, Vaughan EE, de Vos WM, von Wright A, Fondén R, Mattila-Sandholm T (2002). Lactobacillus paracasei subsp. paracasei F19: Survival, Ecology and Safety in the Human Intestinal Tract - A Survey of Feeding Studies within the PROBDEMO Project. Microbial Ecol. Health Dis. Suppl. 3:22-26.
Crossref

 
 

Dave RI, Shah NP (1998). Ingredient supplementation effects on viability of probiotic bacteria in yoghurt. J. Dairy Sci. 81:2804-2816.
Crossref

 
 

Doron S, Gorbach SL (2006). Probiotics: their role in the treatment and prevention of disease. Exp. Rev. Anti-Infect. Ther. 4:261-275.

 
 

Duangchitchareon Y (2006). Selection of probiotic lactic acid bacteria from pickles and fermented plant products. Master of Science Degree Thesis, Chiang Mai University.

 
 

FAO/WHO (2002). Guidelines for the evaluation of probiotics in food. Food and Agriculture Organization of the United Nations and World Health Organization Working Group Report. pp. 5-8.

 
 

Farnworth E (2008). Handbook of fermented functional foods (2nd ed) Boca Raton, USA: CRC Press. pp. 26-33.

 
 

Forestier C, De Champs C, Vatoux C, Joly B (2001). Probiotic activities of Lactobacillus casei rhamnosus: in vitro adherence to intestinal cells and antimicrobial properties. Res. Microbiol. 152(2):167-173.
Crossref

 
 

Fossi BT, Tavea F (2013). Application of Amylolytic Lactobacillus fermentum 04BBA19 in Fermentation for Simultaneous Production of Thermostable Alpha-Amylase and Lactic Acid In: Kongo M (ed): Lactic Acid Bacteria – R & D for Food, Health and Livestock Purposes, 1st ed, In Tech, Rijeka, Croatia. pp. 633-658.

 
 

Furtado DN, Todorov SD, Chiarini E, Destro MT, Landgraf M, Franco BD (2009). Goat milk and cheeses may be a good source for anti-listerial bacteriocin-producing lactic acid bacteria. Biotechnol. Biotechnol. Equip. 23:775-778.
Crossref

 
 

Furtado DN, Todorov SD, Landgraf M, Destro MT, Franco BD (2014). Bacteriocinogenic Lactococcus lactis subsp. lactis DF04Mi isolated from goat milk: Evaluation of the probiotic potential. Braz. J. Microbiol. 45(3):1047-1054.
Crossref

 
 

Gilliland SE, Speck ML (1977). Antagonistic action of Lactobacillus acidophilus toward intestinal and food borne pathogens in associative cultures. J. Food Prot. 40:820-823.

 
 

González L, Sandoval H, Sacristán N, Castro JM, Fresno JM, Tornadijo ME (2007). Identification of lactic acid bacteria isolated from Genestoso cheese throughout ripening and study of their antimicrobial activity. Food Contr. 18:716-722.
Crossref

 
 

Gotcheva V, Hristozova E, Hristozova T, Guo M, Roshkova Z and Angelov A (2002). Assessment of potential probiotic properties of lactic acid bacteria and yeast strains. J. Food Biotechnol. 16:211-225.
Crossref

 
 

Guglielmetti S, Taverniti V, Minuzzo M, Arioli S, Zanoni I, Stuknyte M, Granucci F, Karp M, Mora D (2010). A dairy bacterium displays in-vitro probiotic properties for the pharyngeal mucosa by antagonizing group A Streptococci and modulating the immune response. Infect. Immun. 78:4734-4743.
Crossref

 
 

Hamon E, Horvatovich P, Izquierdo E, Bringel F, Marchionil E, Aoudé-Werner D, Ennahar S (2011). Comparative proteomic analysis of Lactobacillus plantarum for the identification of key proteins in bile tolerance. BMC Microbiol. 11:63.
Crossref

 
 

Jacobsen CN, Roesnfeldt Nielsen AE, Moller PL, Michaelsen KF, Paerregaard A, Sandstrom B, Tvede M, Jacobsen M (1999). Screening of probiotic activities of forty-seven strains of Lactobacillus sp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl. Environ. Microbiol. 65:4949-4956.

 
 

Ji GE, Han HK, Yun SW, Rhim SL (1992). Isolation of amylolytic Bifidobacterium sp. Int-57 and characterization of amylase. J. Microbiol. Biotechnol. 2:85-91.

 
 

Kailasapathy K, Chin J (2000). Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol. Cell Biol. 78(1):80-88.
Crossref

 
 

Karasu N, ÅžimÅŸek Ő, Çon AH (2010). Technological and probiotic characteristics of Lactobacillus plantarum strains isolated from traditionally produced fermented vegetables. Ann. Microbiol. 60:227-234.
Crossref

 
 

Kawai Y, Tacokoro K, Konomi R, Itoh K, Saito T, Kitazawa H, Itoh T (1999). A novel method for the detection of protease and the development of extracellular protease in early growth stages of Lactobacillus delbrueckii ssp. bulgaricus. J. Dairy Sci. 82:481-485.
Crossref

 
 

Klaver FAM, Kingma F, Weerkamp AH (1993). Growth and survival of Bifidobacterium lactis in milk. Neth. Milk Dairy J. 47:151-164.

 

Kong S, Davison AJ (1980). The role of interactions between O2, H2O2, OH, e- and O2- in free radical damage to biological systems. Arch. Biochem. Biophys. 204:18-29.
Crossref

 

Kosek M, Bern C, Guerrant RL (2003). The global burden of diarrheal disease, as estimated from studies published between 1992 and 2000. Bull. World Health Organ. 81:197-204.

 
 

Kunji ER, Mierau I, Hagting A, Poolman B, Konings WN (1996). The proteolytic systems of lactic acid bacteria. Antonie Van Leeuwenhoek. 70:187-221.
Crossref

 
 

Lankaputhra WEV, Shah NP (1995). Survival of Lactobacillus acidophilus and Bifidobacterium sp. in the presence of acid and bile salts. Cult. Dairy Prod. J. 30:2-7.

 
 

Lee SK, Kim YB, Ji GE (1997). Purification of amylase secreted from Bifidobacterium adolescentis. J. Appl. Microbiol. 83:267-272.
Crossref

 
 

Lindgren SE, Dobrogosz WJ (1990). Antagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiol. Rev. 7:149-163.
Crossref

 
 

MacFaddin JF (2000). Biochemical tests for identification of medical bacteria. 3rd ed, Lippincott Williams and Wilkins, Philadelphia, USA.

 
 

Makras L, Vuyst LD (2006). The in vitro inhibition of Gram-negative pathogenic bacteria by bifidobacteria is caused by the production of organic acids. Int. Dairy J. 16:1049-1057.
Crossref

 
 

Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E (2006). Probiotic potential of Lactobacillus strains isolated from dairy products. Int. Dairy J. 16:189-199.
Crossref

 
 

McFarland LV (2009). Evidence-based review of probiotics for antibiotic-associated diarrhea and Clostridium difficile infections. Anaerobe 15(6):274-280.
Crossref

 
 

Mishra V, Prasad DN (2005). Application of in vitro methods for selection of Lactobacillus casei strains as potential probiotics. Int. J. Food Microbiol. 103:109-115.
Crossref

 
 

Moser SA, Savage DC (2001). Bile salt hydrolase activity and resistance to toxicity of conjugated bile salts are unrelated properties in lactobacilli. Appl. Environ. Microbiol. 67:3476-3480.
Crossref

 
 

Musikasang H, Tani A, H-kittikun A, Maneerat S (2009). Probiotic potential of lactic acid bacteria isolated from chicken gastrointestinal digestive tract. World J. Microbiol. Biotechnol. 25:1337-1345.
Crossref

 
 

Nouri M, Rahbarizadeh F, Ahmadvand D, Moosakhani F, Sadeqzadeh E, Lavasani S, Vishteh VK (2010). Inhibitory effects of Lactobacillus salivarius and Lactobacillus crispatus isolated from chicken gastrointestinal tract on Salmonella enteritidis and Escherichia coli growth. Iran. J. Biotechnol. 8:32-37.

 
 

Oca-a VS, Pesce De Ruiz Holgado AA, Nader-Macias ME (1999). Characterization of a bacteriocins-like substance produced by a vaginal Lactobacillus salivarius strain. Appl. Environ. Microbiol. 65:5631-5635.

 
 

Oezbas ZY, Aytac SA (1995). Behaviour of Yersinia enterocolitica and Aeromonas hydrophila in yogurt made with probiotic bacteria: Bifidobacterium infantis and Lactobacillus acidophilus. Milchwissenschaft. 50:626-629.

 
 

Olkowski AA, Wojnarowicz C, Nain S, Ling B, Alcorn JM, Laarveld B (2008). A study on pathogenesis of sudden death syndrome in broiler chickens. Res. Vet. Sci. 85:131-140.
Crossref

 
 

Ouwehand AC, Salminen S, Isolauri E (2002). Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek. 82:279-289.
Crossref

 
 

Parashar UD, Hummelman EG, Bresee JS, Miller MA, Glass RI (2003). Global illness and deaths caused by rotavirus disease in children. Emerg. Infect. Dis. 9:565-572.
Crossref

 
 

Pehrson MESF, Mancilha IM, Perrira CAS (2015). Antimicrobial activity of probiotic Lactobacillus strains towards Gram-negative enteropathogens. Eur. Int. J. Sci. Technol. 4(3):136-149.

 
 

Petri Jr. WA, Miller M, Binder HJ, Levine MM, Dillingham R, Guerrant RL (2008). Enteric infections, diarrhea, and their impact on function and development. J. Clin. Invest. 118(4):1277-1290.
Crossref

 
 

Piard JC, Desmazeaud M (1991). Inhibiting factors produced by lactic acid bacteria. 1. Oxygen metabolites and catabolism end-products. Le Lait. 71:525-541.
Crossref

 
 

Psomas E, Andrighetto C, Litopoulou-Tzanetaki E, Lombardi A, Tzanetakis N (2001). Some probiotic properties of yeast isolates from infant faeces and Feta cheese. Int. J. Food Microbiol. 69:125-133.
Crossref

 
 

Reddy G, Altaf M, Naveena BJ, Ventkateshwar M, Kumar EV (2008). Amylolytic bacterial lactic acid fermentation - a review. Biotechnol. Adv. 26(1):22-34.
Crossref

 
 

Ryan KJ (2004). Enteric Infections and Food Poisoning In: Ryan KJ, Ray CG (ed): Sherris medical microbiology: an introduction to infectious diseases, 4th ed, McGraw-Hill Companies, USA. pp. 853- 863.

 
 

Samona A, Robinson RK (1994). Effect of yogurt cultures on the survival of bifidobacteria in fermented milks. Int. J. Dairy Technol. 47:58-60.
Crossref

 
 

Santos A, San Mauro M, Sanchez A, Torres JM, Marquina D (2003). The antimicrobial properties of different strains of Lactobacillus spp. isolated from kefir. Syst. Appl. Microbiol. 26:434-437.
Crossref

 
 

Savadogo A, Ouattara CAT, BassolÄ— IHN, Traore A (2004). Antimicrobial activities of lactic acid bacteria strains isolated from Burkina faso fermented milk. Pak. J. Nutr. 3:174-179.
Crossref

 
 

Savijoki K, Ingmer H, Varmanen P (2006). Proteolytic systems of lactic acid bacteria. Appl. Microbiol. Biotechnol. 71:394-406.
Crossref

 
 

Schillinger U, Geisen R, Holzapfell WH (1996). Potential of antagonistic microorganisms and bacteriocins for the biological preservation of foods. Trends Food Sci. Technol.7:158-164.
Crossref

 
 

Silva M, Jacobus NV, Deneke C, Gorbach SL (1987). Antimicrobial substance from a human Lactobacillus strain. Antimicrob. Agents Chemother. 31(8):1231-1233.
Crossref

 
 

Singh R, Sivasubramani K, Jayalakshmi S, Satheesh kumar S, Selvi C (2013). Isolation and production of bacteriocin by marine Lactobacillus fermentum SBS001. Int. J. Curr. Microbiol. Appl. Sci. 2(4):67-73.

 
 

Smid EJ, Poolman B, Konings WN (1991). Casein utilization by lactococci. Appl. Environ. Microbiol. 57(9):2447-2452.

 
 

Strompfová V, Lauková A (2007). In vitro study on bacteriocin production of Enterococci associated with chickens. Anaerobe 13:228-237.
Crossref

 
 

Taranto MP, Perez-Martinez G, de Valdez GF (2006). Effect of bile acid on the cell membrane functionality of lactic acid bacteria for oral administration. Res. Microbiol. 157:720-725.
Crossref

 
 

Taverniti V, Guglielmetti S (2012). Health-promoting properties of Lactobacillus helveticus. Front. Microbiol. 3:392.
Crossref

 
 

Thongsom M (2004). Lactic acid bacteria in digestive tract of black tiger prawn (Penaeus monodon). Master of Science Degree Thesis, Prince of Songkla University.

 
 

Upadhyay N, Moudgal V (2012). Probiotics: a review. J. Clin. Outcomes Manage. 19:76-84.

 
 

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.
Crossref

 
 

Wang G, Zhao Y, Tian F, Jin X, Chen H, Liu X, Zhang Q, Zhao J, Chen Y, Zhang H, Chen W (2014). Screening of adhesive lactobacilli with antagonistic activity against Campylobacter jejuni. Food Control 44:49-57.
Crossref

 
 

Wong S, Jamous A, O'Driscoll J, Sekhar R, Weldon M, Yau CY, Hirani SP, Grimble G, Forbes A (2013). A Lactobacillus casei Shirota probiotic drink reduces antibiotic-associated diarrhea in patients with spinal cord injuries: A randomised controlled trial. Br. J. Nutr. 111(4):672-678.
Crossref

 
 

Yateem A, Balba MT, Al-Surrayai T, Al-Mutairi B, Al-Daher R (2008). Isolation of lactic acid bacteria with probiotic potential from camel milk. Int. J. Dairy Sci. 3(4):194-199.
Crossref

 
 

Yu Z, Zhang X, Li S, Li C, Li D, Yang Z. (2013). Evaluation of probiotic properties of Lactobacillus plantarum strains isolated from Chinese sauerkraut. World J. Microbiol. Biotechnol. 29(3):489-498.
Crossref