Use of the potential probiotic strain Lactobacillus salivarius SMXD51 to control Campylobacter jejuni in broilers

International Journal of Food Microbiology

Volumn 247, Issue , 2017, Pages 9-17

  Saint Cyr, Manuel Jimmy ^a   Haddad, Nabila ^a   Taminiau, Bernard ^b   Poezevara, Typhaine ^c   Quesne, Ségolène ^c   Amelot, Michel ^c   Daube, Georges ^b   Chemaly, Marianne ^c   Dousset, Xavier ^a   Guyard Nicodème, Muriel ^c  

^a LUNAM UNIVERSITÉ   (France)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c FRENCH AGENCY FOR FOOD   (France)

Author keywords

Avian gut microbiota; Broiler chickens; Campylobacter; Immune response; Lactobacillus

Indexed keywords

BACTERIOCIN; INTERLEUKIN 8; PROBIOTIC AGENT; PROTEIN; PROTEIN K60; RNA 16S; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BROILER; CAMPYLOBACTER JEJUNI; CAMPYLOBACTERIOSIS; CECAL TONSIL; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GROWTH INHIBITION; IN VITRO STUDY; IN VIVO STUDY; INFECTION CONTROL; INNATE IMMUNITY; INTESTINE FLORA; LACTOBACILLUS SALIVARIUS; MALE; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; CAMPYLOBACTER INFECTIONS; CECUM; CHICKEN; HUMAN; MICROBIOLOGY; PHYSIOLOGY; POULTRY DISEASES; VETERINARY;

ANIMALS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CECUM; CHICKENS; HUMANS; LACTOBACILLUS SALIVARIUS; POULTRY DISEASES; PROBIOTICS;

EID: 85015440061     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2016.07.003     Document Type: Article

References (72)

1. Arsi, K., Donoghue, A., Woo-Ming, A., Blore, P., Donoghue, D., The efficacy of selected probiotic and prebiotic combinations in reducing Campylobacter colonization in broiler chickens. The Journal of Applied Poultry Research, 2015, pfv032, 10.3382/japr/pfv032.
2. Audisio, M.C., Oliver, G., Apella, M.C., 2000. Protective effect of Enterococcus faecium J96, a potential probiotic strain, on chicks infected with Salmonella pullorum. J. Food Prot.® 63, 1333–1337.
3. Baffoni, L., Gaggìa, F., Di Gioia, D., Santini, C., Mogna, L., Biavati, B., A Bifidobacterium-based synbiotic product to reduce the transmission of C. jejuni along the poultry food chain. Int. J. Food Microbiol. 157 (2012), 156–161.
4. Barker, K.A., Hampe, A., Stoeckle, M.Y., Hanafusa, H., Transformation-associated cytokine 9E3/CEF4 is chemotactic for chicken peripheral blood mononuclear cells. J. Virol. 67 (1993), 3528–3533.
5. Berndt, A., Wilhelm, A., Jugert, C., Pieper, J., Sachse, K., Methner, U., Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect. Immun. 75 (2007), 5993–6007.
6. Borrmann, E., Berndt, A., Hänel, I., Köhler, H., Campylobacter-induced interleukin-8 responses in human intestinal epithelial cells and primary intestinal chick cells. Vet. Microbiol. 124 (2007), 115–124.
7. Brisbin, J.T., Davidge, L., Roshdieh, A., Sharif, S., Characterization of the effects of three Lactobacillus species on the function of chicken macrophages. Res. Vet. Sci. 100 (2015), 39–44.
8. Brisbin, J.T., Gong, J., Orouji, S., Esufali, J., Mallick, A.I., Parvizi, P., Shewen, P.E., Sharif, S., Oral treatment of chickens with lactobacilli influences elicitation of immune responses. Clin. Vaccine Immunol. 18 (2011), 1447–1455.
9. Brisbin, J.T., Gong, J., Parvizi, P., Sharif, S., Effects of lactobacilli on cytokine expression by chicken spleen and cecal tonsil cells. Clin. Vaccine Immunol. 17 (2010), 1337–1343.
10. Brulc, J.M., Antonopoulos, D.A., Miller, M.E.B., Wilson, M.K., Yannarell, A.C., Dinsdale, E.A., Edwards, R.E., Frank, E.D., Emerson, J.B., Wacklin, P., Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc. Natl. Acad. Sci. 106 (2009), 1948–1953.
11. Cean, A., Stef, L., Simiz, E., Julean, C., Dumitrescu, G., Vasile, A., Pet, E., Drinceanu, D., Corcionivoschi, N., Effect of human isolated probiotic bacteria on preventing Campylobacter jejuni colonization of poultry. Foodborne Pathog. Dis. 12 (2015), 122–130.
12. Croghan, C., Egeghy, P., Methods of Dealing with Values below the Limit of Detection Using SAS. 2003, Southeastern SAS User Group, St. Petersburg, FL, 22–24.
13. EFSA, The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J., 12, 2014, 3547.
14. EFSA, The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA J., 13, 2015, 3991.
15. FASS, Guide for the care and use of agricultural animals in research and teaching. http://www.fass.org/docs/agguide3rd/Ag_Guide_3rd_ed.pdf, 2010.
16. Fleckenstein, J.M., Kopecko, D.J., Breaching the mucosal barrier by stealth: an emerging pathogenic mechanism for enteroadherent bacterial pathogens. J. Clin. Invest. 107 (2001), 27–30, 10.1172/JCI11792.
17. Ghareeb, K., Awad, W., Mohnl, M., Porta, R., Biarnes, M., Böhm, J., Schatzmayr, G., Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens. Poult. Sci. 91 (2012), 1825–1832.
18. Gracia, M., Millán, C., Sánchez, J., Guyard-Nicodème, M., Mayot, J., Carre, Y., Csorbai, A., Chemaly, M., Medel, P., Efficacy of feed additives against Campylobacter in live broilers during the entire rearing period: PartB. Poult. Sci. 95 (2016), 886–892, 10.3382/ps/pev346.
19. Guinane, C.M., Piper, C., Draper, L.A., O'Connor, P.M., Hill, C., Ross, R.P., Cotter, P.D., Impact of environmental factors on bacteriocin promoter activity in gut-derived Lactobacillus salivarius. Appl. Environ. Microbiol. 81 (2015), 7851–7859.
20. Guyard-Nicodème, M., Keita, A., Quesne, S., Amelot, M., Poezevara, T., Le Berre, B., Sánchez, J., Vesseur, P., Martín, Á., Medel, P., Chemaly, M., Efficacy of feed additives against Campylobacter in live broilers during the entire rearing period. Poult. Sci. 95 (2016), 298–305, 10.3382/ps/pev303.
21. Guyard-Nicodème, M., Rivoal, K., Houard, E., Rose, V., Quesne, S., Mourand, G., Rouxel, S., Kempf, I., Guillier, L., Gauchard, F., Chemaly, M., Prevalence and characterization of Campylobacter jejuni from chicken meat sold in French retail outlets. Int. J. Food Microbiol. 203 (2015), 8–14.
22. Haghighi, H.R., Gong, J., Gyles, C.L., Hayes, M.A., Zhou, H., Sanei, B., Chambers, J.R., Sharif, S., Probiotics stimulate production of natural antibodies in chickens. Clin. Vaccine Immunol. 13 (2006), 975–980.
23. Hald, B., Wedderkopp, A., Madsen, M., Thermophilic Campylobacter spp. in Danish broiler production: a cross-sectional survey and a retrospective analysis of risk factors for occurrence in broiler flocks. Avian Pathology 29 (2000), 123–131.
24. Hermans, D., Pasmans, F., Messens, W., Martel, A., Van Immerseel, F., Rasschaert, G., Heyndrickx, M., Van Deun, K., Haesebrouck, F., Poultry as a host for the zoonotic pathogen Campylobacter jejuni. Vector-Borne and Zoonotic Diseases 12 (2012), 89–98.
25. Hermans, D., Van Deun, K., Messens, W., Martel, A., Van Immerseel, F., Haesebrouck, F., Rasschaert, G., Heyndrickx, M., Pasmans, F., Campylobacter control in poultry by current intervention measures ineffective: urgent need for intensified fundamental research. Vet. Microbiol. 152 (2011), 219–228.
26. Hugas, M., Tsigarida, E., Robinson, T., Calistri, P., The EFSA Scientific Panel on Biological Hazards first mandate: May 2003–May 2006. Insight into foodborne zoonoses. Trends Food Sci. Technol. 20 (2009), 188–193.
27. Humphrey, S., Chaloner, G., Kemmett, K., Davidson, N., Williams, N., Kipar, A., Humphrey, T., Wigley, P., Campylobacter jejuni is not merely a commensal in commercial broiler chickens and affects bird welfare. MBio 5 (2014), e01314–e01364.
28. International Organization for Standardization, Microbiology of Food and Animal Feeding Stuffs Horizontal Method for Detection and Enumeration of Campylobacter spp.—Part 1: Detection Method. 2006 ISO 10272-1:2006.
29. Kaakoush, N.O., Sodhi, N., Chenu, J.W., Cox, J.M., Riordan, S.M., Mitchell, H.M., The interplay between Campylobacter and Helicobacter species and other gastrointestinal microbiota of commercial broiler chickens. Gut Pathogens 6 (2014), 1–10.
30. Kaiser, P., Hughes, S., Bumstead, N., The chicken 9E3/CEF4 CXC chemokine is the avian orthologue of IL8 and maps to chicken Chromosome 4 syntenic with genes flanking the mammalian chemokine cluster. Immunogenetics 49 (1999), 673–684, 10.1007/s002510050664.
31. Keener, K., Bashor, M., Curtis, P., Sheldon, B., Kathariou, S., Comprehensive review of Campylobacter and poultry processing. Compr. Rev. Food Sci. Food Saf. 3 (2004), 105–116.
32. Kergourlay, G., Messaoudi, S., Dousset, X., Prévost, H., Genome sequence of Lactobacillus salivarius SMXD51, a potential probiotic strain isolated from chicken cecum, showing anti-campylobacter activity. J. Bacteriol. 194 (2012), 3008–3009.
33. Koenen, M., Kramer, J., Van Der Hulst, R., Heres, L., Jeurissen, S., Boersma, W., Immunomodulation by probiotic lactobacilli in layer-and meat-type chickens. Br. Poult. Sci. 45 (2004), 355–366.
34. Lee, S., Lillehoj, H., Dalloul, R., Park, D., Hong, Y., Lin, J., Influence of Pediococcus-based probiotic on coccidiosis in broiler chickens. Poult. Sci. 86 (2007), 63–66.
35. Lesuffleur, T., Porchet, N., Aubert, J.-P., Swallow, D., Gum, J.R., Kim, Y.S., Real, F.X., Zweibaum, A., Differential expression of the human mucin genes MUC1 to MUC5 in relation to growth and differentiation of different mucus-secreting HT-29 cell subpopulations. J. Cell Sci. 106 (1993), 771–783.
36. Li, Y.-P., Ingmer, H., Madsen, M., Bang, D.D., Cytokine responses in primary chicken embryo intestinal cells infected with Campylobacter jejuni strains of human and chicken origin and the expression of bacterial virulence-associated genes. BMC Microbiol., 8, 2008, 107.
37. Meimandipour, A., Shuhaimi, M., Hair-Bejo, M., Azhar, K., Kabeir, B., Rasti, B., Yazid, A., In vitro fermentation of broiler cecal content: the role of lactobacilli and pH value on the composition of microbiota and end products fermentation. Lett. Appl. Microbiol. 49 (2009), 415–420.
38. Menconi, A., Wolfenden, A., Shivaramaiah, S., Terraes, J., Urbano, T., Kuttel, J., Kremer, C., Hargis, B., Tellez, G., Effect of lactic acid bacteria probiotic culture for the treatment of Salmonella enterica serovar Heidelberg in neonatal broiler chickens and turkey poults. Poult. Sci. 90 (2011), 561–565.
39. Messaoudi, S., Kergourlay, G., Dalgalarrondo, M., Choiset, Y., Ferchichi, M., Prévost, H., Pilet, M.-F., Chobert, J.-M., Manai, M., Dousset, X., Purification and characterization of a new bacteriocin active against Campylobacter produced by Lactobacillus salivarius SMXD51. Food Microbiol. 32 (2012), 129–134.
40. Messaoudi, S., Kergourlay, G., Rossero, A., Ferchichi, M., Prévost, H., Drider, D., Manai, M., Dousset, X., Identification of lactobacilli residing in chicken ceca with antagonism against Campylobacter. Int. Microbiol. 14 (2011), 103–110.
41. Messaoudi, S., Madi, A., Prevost, H., Feuilloley, M., Manai, M., Dousset, X., Connil, N., In vitro evaluation of the probiotic potential of Lactobacillus salivarius SMXD51. Anaerobe 18 (2012), 584–589.
42. Meunier, M., Guyard-Nicodème, M., Dory, D., Chemaly, M., Control strategies against Campylobacter at the poultry production level: biosecurity measures, feed additives and vaccination. J. Appl. Microbiol. 120 (2016), 1139–1173, 10.1111/jam.12986.
43. Morishita, T.Y., Aye, P.P., Harr, B.S., Cobb, C.W., Clifford, J.R., Evaluation of an avian-specific probiotic to reduce the colonization and shedding of Campylobacter jejuni in broilers. Avian Dis., 1997, 850–855.
44. Nadeau, É., Messier, S., Quessy, S., Comparison of Campylobacter isolates from poultry and humans: association between in vitro virulence properties, biotypes, and pulsed-field gel electrophoresis clusters. Appl. Environ. Microbiol. 69 (2003), 6316–6320.
45. Neal-McKinney, J.M., Lu, X., Duong, T., Larson, C.L., Call, D.R., Shah, D.H., Konkel, M.E., Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS One, 7, 2012, e43928, 10.1371/journal.pone.0043928.
46. Newell, D., Fearnley, C., Sources of Campylobacter colonization in broiler chickens. Appl. Environ. Microbiol. 69 (2003), 4343–4351.
47. Nishiyama, K., Nakazato, A., Ueno, S., Seto, Y., Kakuda, T., Takai, S., Yamamoto, Y., Mukai, T., Cell surface-associated aggregation-promoting factor from Lactobacillus gasseri SBT2055 facilitates host colonization and competitive exclusion of Campylobacter jejuni. Mol. Microbiol. 98 (2015), 712–726.
48. Nishiyama, K., Seto, Y., Yoshioka, K., Kakuda, T., Takai, S., Yamamoto, Y., Mukai, T., Lactobacillus gasseri SBT2055 reduces infection by and colonization of Campylobacter jejuni. PLoS One, 9, 2014, e108827, 10.1371/journal.pone.0108827.
49. Parks, D.H., Beiko, R.G., Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26 (2010), 715–721.
50. Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res., 29, 2001, e45.
51. Rodriguez, C., Taminiau, B., Brévers, B., Avesani, V., Van Broeck, J., Leroux, A., Gallot, M., Bruwier, A., Amory, H., Delmée, M., Faecal microbiota characterisation of horses using 16 rdna barcoded pyrosequencing, and carriage rate of Clostridium difficile at hospital admission. BMC Microbiol., 15, 2015, 181, 10.1186/s12866-015-0514-5.
52. Romero-Barrios, P., Hempen, M., Messens, W., Stella, P., Hugas, M., Quantitative microbiological risk assessment (QMRA) of food-borne zoonoses at the European level. Food Control 29 (2013), 343–349.
53. Rosenquist, H., Nielsen, N.L., Sommer, H.M., Nørrung, B., Christensen, B.B., Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int. J. Food Microbiol. 83 (2003), 87–103.
54. Saint-Cyr, M.J., Guyard-Nicodème, M., Messaoudi, S., Chemaly, M., Cappelier, J.-M., Dousset, X., Haddad, N., Recent advances in screening of anti-Campylobacter activity in probiotics for use in poultry. Front. Microbiol., 7, 2016, 553, 10.3389/fmicb.2016.00553.
55. Santini, C., Baffoni, L., Gaggia, F., Granata, M., Gasbarri, R., Di Gioia, D., Biavati, B., Characterization of probiotic strains: an application as feed additives in poultry against Campylobacter jejuni. Int. J. Food Microbiol. 141 (2010), S98–S108.
56. Sasaki, Y., Maruyama, N., Zou, B., Haruna, M., Kusukawa, M., Murakami, M., Asai, T., Tsujiyama, Y., Yamada, Y., Campylobacter cross-contamination of chicken products at an abattoir. Zoonoses Public Health 60 (2013), 134–140.
57. Schoeni, J.L., Wong, A., Inhibition of Campylobacter jejuni colonization in chicks by defined competitive exclusion bacteria. Appl. Environ. Microbiol. 60 (1994), 1191–1197.
58. Scupham, A., Jones, J., Rettedal, E., Weber, T., Antibiotic manipulation of intestinal microbiota to identify microbes associated with Campylobacter jejuni exclusion in poultry. Appl. Environ. Microbiol. 76 (2010), 8026–8032.
59. Shaughnessy, R.G., Meade, K.G., Cahalane, S., Allan, B., Reiman, C., Callanan, J.J., O'Farrelly, C., Innate immune gene expression differentiates the early avian intestinal response between Salmonella and Campylobacter. Vet. Immunol. Immunopathol. 132 (2009), 191–198.
60. Silva, J., Leite, D., Fernandes, M., Mena, C., Gibbs, P.A., Teixeira, P., Campylobacter spp. as a foodborne pathogen: a review. Frontiers in Microbiology, 2, 2011, 10.3389/fmicb.2011.00200.
61. Sofka, D., Pfeifer, A., Gleiss, B., Paulsen, P., Hilbert, F., Changes within the intestinal flora of broilers by colonisation with Campylobacter jejuni. Berl. Munch. Tierarztl. Wochenschr. 128 (2015), 104–110.
62. Sokol, H., Seksik, P., Furet, J., Firmesse, O., Nion-Larmurier, I., Beaugerie, L., Cosnes, J., Corthier, G., Marteau, P., Doré, J., Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm. Bowel Dis. 15 (2009), 1183–1189.
63. Stanley, D., Geier, M.S., Chen, H., Hughes, R.J., Moore, R.J., Comparison of fecal and cecal microbiotas reveals qualitative similarities but quantitative differences. BMC Microbiol., 15, 2015, 51, 10.1186/s12866-015-0388-6.
64. Stanley, D., Geier, M.S., Hughes, R.J., Denman, S.E., Moore, R.J., Highly variable microbiota development in the chicken gastrointestinal tract. PLoS One, 8, 2013, e84290, 10.1371/journal.pone.0084290.
65. Stern, N.J., Eruslanov, B.V., Pokhilenko, V.D., Kovalev, Y.N., Volodina, L.L., Perelygin, V.V., Mitsevich, E.V., Mitsevich, I.P., Borzenkov, V.N., Levchuk, V.P., Bacteriocins reduce Campylobacter jejuni colonization while bacteria producing bacteriocins are ineffective. Microb. Ecol. Health Dis. 20 (2008), 74–79.
66. Thibodeau, A., Fravalo, P., Yergeau, É., Arsenault, J., Lahaye, L., Letellier, A., Chicken caecal microbiome modifications induced by Campylobacter jejuni colonization and by a non-antibiotic feed additive. PLoS One, 10, 2015, e0131978, 10.1371/journal.pone.0131978.
67. Torok, V., Dyson, C., McKay, A., Ophel-Keller, K., Quantitative molecular assays for evaluating changes in broiler gut microbiota linked with diet and performance. Anim. Prod. Sci. 53 (2013), 1260–1268.
68. Tsai, C.-C., Hsih, H.-Y., Chiu, H.-H., Lai, Y.-Y., Liu, J.-H., Yu, B., Tsen, H.-Y., Antagonistic activity against Salmonella infection in vitro and in vivo for two Lactobacillus strains from swine and poultry. Int. J. Food Microbiol. 102 (2005), 185–194.
69. Van de Giessen, A., Tilburg, J., Ritmeester, W., Van Der Plas, J., Reduction of Campylobacter infections in broiler flocks by application of hygiene measures. Epidemiol. Infect. 121 (1998), 57–66.
70. Waite, D.W., Taylor, M.W., Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front. Microbiol., 5, 2014, 10.3389/fmicb.2014.00223.
71. Westrell, T., Ciampa, N., Boelaert, F., Helwigh, B., Korsgaard, H., Chriél, M., Ammon, A., Mäkelä, P., Zoonotic infections in Europe in 2007: a summary of the EFSA-ECDC annual report. Euro surveillance: bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin, 14, 2009, 785–794.
72. Willis, W., Reid, L., Investigating the effects of dietary probiotic feeding regimens on broiler chicken production and Campylobacter jejuni presence. Poult. Sci. 87 (2008), 606–611.