Supplemental thymol and carvacrol increases ileum Lactobacillus population and reduces effect of necrotic enteritis caused by Clostridium perfringes in chickens

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Yin, Dafei ^a   Du, Encun ^a   Yuan, Jianmin ^a   Gao, Jinxin ^a   Wang, YouLi ^a   Aggrey, Samuel E ^b   Guo, Yuming ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARVACROL; TERPENE; THYMOL;

ANIMAL; BIRD DISEASE; CHICKEN; CLOSTRIDIUM INFECTION; CLOSTRIDIUM PERFRINGENS; DIETARY SUPPLEMENT; DRUG EFFECT; GENETICS; ILEUM; INTESTINE FLORA; LACTOBACILLUS; MALE; METAGENOME; METAGENOMICS; MICROBIOLOGY; MORTALITY; NECROTIZING ENTEROCOLITIS; PATHOLOGY; PROCEDURES; VETERINARY MEDICINE;

ANIMALS; CHICKENS; CLOSTRIDIUM INFECTIONS; CLOSTRIDIUM PERFRINGENS; DIETARY SUPPLEMENTS; ENTEROCOLITIS, NECROTIZING; GASTROINTESTINAL MICROBIOME; ILEUM; LACTOBACILLUS; MALE; METAGENOME; METAGENOMICS; MONOTERPENES; POULTRY DISEASES; THYMOL;

EID: 85026784608     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-07420-4     Document Type: Article

References (63)

1. Wade, B. & Keyburn, A. The true cost of necrotic enteritis. http://www. poultryworld. net/Meat/Articles/2015/10/The-true-cost-ofnecrotic-enteritis-2699819W/#comments (2016) (Date of access:09/10/2015).
2. Van Immerseel, F. et al. Clostridium perfringens in poultry: An emerging threat for animal and public health. Avian Pathol. 33, 537-549 (2004).
3. Van Immerseel, F. et al. Rethinking our understanding of the pathogenesis of necrotic enteritis in chickens. Trends Microbiol. 17, 32-36 (2009).
4. Stackebrandt, E. & Rainey, F. A. Phylogenetic relationships. In The Clostridia-molecular biology and pathogenesis (ed. Rood, J. I., McClane, B. A., Songer, G. & Titball. R. W.) Chapter 17 (1997).
5. Bryant, A. E. & Stevens, L. S. The Pathogenesis of Gas Gangrene. Academic Press. San Diego. 186-187 (1997).
6. Songer, J. G. & Meer, R. R. Genotyping of Clostridium perfringens bypolymerase chain reaction is a useful adjunct to diagnosis of clostridial enteric disease in animals. Anaerobe 2, 197-203 (1996).
7. Keyburn, A. L. et al. NetB, a new toxin that is associated with avian necrotic enteritis caused by Clostridium perfringens. PLoS Pathog. 4, e26 (2008).
8. Amimoto, K., Noro, T., Oishi, E. & Shimizu, M. A novel toxin homologous to large clostridial cytotoxins found in culture supernatant of Clostridium perfringens type C. Microbiology 4, 1198-1206 (2007).
9. Prescott, J. F., Parreira, V. R., Mehdizadeh, G. I., Lepp, D. & Gong, J. The pathogenesis of necrotic enteritis in chickens: what we know and what we need to know: a review. Avian Pathol. 45, 288-294 (2016).
10. Liu, D. et al. Exogenous lysozyme influences Clostridium perfringens colonization and intestinal barrier function in broiler chickens. Avian Pathol. 39, 17-24 (2010).
11. Du, E. et al. In vitro antibacterial activity of thymol and carvacrol and their effects on broiler chickens challenged with Clostridium perfringens. J. Anim. Sci. Biotech. 6, 58-71 (2015).
12. Du, E. et al. Effects of thymol and carvacrol supplementation on intestinal integrity and immune responses of broiler chickens challenged with Clostridium perfringens. J. Anim. Sci. Biotechnol. 7, 19-29 (2016).
13. Collier, C. T. et al. Coccidia-induced mucogenesis promotes the onset of necrotic enteritis by supporting Clostridium perfringens growth. Vet. Immun. Immunopathol. 122, 104-115 (2008).
14. Dahiya, J. P. et al. Potential strategies for controlling necrotic enteritis in broiler chickens in post-antibiotic era. Anim. Feed Sci. Technol. 129, 60-88 (2006).
15. Guo, S. et al. Inflammatory responses to a Clostridium perfringens type a strain and alpha-toxin in primary intestinal epithelial cells of chicken embryos. Avian Pathol. 44, 81-91 (2015).
16. Windisch, W. et al. Use of phytogenic products as feed additives for swine and poultry. J. Anim. Sci. 86, E140-E148 (2008).
17. Brenes, A. & Roura, E. Essential oils in poultry nutrition: Main effects and modes of action. Anim. Feed Sci. Technol. 158, 1-14 (2010).
18. Placha., I. et al. Effect of thyme essential oil and selenium on intestine integrity and antioxidant status of broilers. Br. Poult. Sci. 55, 105-114 (2014).
19. Wlodarska, M. et al. Phytonutrient diet supplementation promotes beneficial clostridia species and intestinal mucus secretion resulting in protection against enteric infection. Sci. Rep. 5, 9253 (2015).
20. Lee, S. H. et al. Effects of dietary supplementation with phytonutrients on vaccine-stimulated immunity against infection with eimeria tenella. Vet. Parasitol. 181, 97-105 (2011).
21. Awaad, M. H. H., Elmenawey, M. & Ahmed, K. A. Effect of a specific combination of carvacrol, cinnamaldehyde, and capsicum oleoresin on the growth performance, carcass quality and gut integrity of broiler chickens. Vet. World 7, 284-290 (2014).
22. Kim, D. K. et al. High-throughput gene expression analysis of intestinal intraepithelial lymphocytes after oral feeding of carvacrol, cinnamaldehyde, or capsicum oleoresin. Poult. Sci. 89, 68-81 (2010).
23. Bassole, I. H. & Juliani, H. R. Essential oils in combination and their antimicrobial properties. Molecules 17, 3989-4006 (2012).
24. Riella, K. R. et al. Anti-inflammatory and cicatrizing activities of thymol, a monoterpene of the essential oil from Lippia gracilis, in rodents. J. Ethnopharmacol. 143, 656-663 (2012).
25. Guimaraes, A. G. et al. Carvacrol attenuates mechanical hypernociception and inflammatory response. Naunyn-Schmiedebergs Arc. Pharmacol. 385, 253-263 (2012).
26. Amann, R. I., Ludwig, W. & Schleifer, K. H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59, 143-169 (1995).
27. Waite, D. W. & Taylor, M. W. Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front Microbiol. 5, 223 (2014).
28. Wu, H., Wang, A. H. & Jennings, M. P. Discovery of virulence factors of pathogenic bacteria. Curr. Opin. Chem. Biol. 12, 1-9 (2008).
29. Si, W. et al. Antimicrobial activity of essential oils and structurally related synthetic food additives towards Clostridium perfringens. J. Appl. Microbiol. 106, 213-220 (2009).
30. Burt, S. Essential oils: their antibacterial properties and potential applications in foods-a review. Int. J. Food Microbiol. 94, 223-253 (2004).
31. Qiu, J. et al. Subinhibitory concentrations of Perilla Oil affect the expression of secreted virulence factor genes in Staphylococcus aureus. PLoS ONE 6, e16160 (2011).
32. Rood, J. I. Virulence genes of Clostridium perfringens. Annu. Rev. Microbiol. 52, 333-60 (1998).
33. Shimizu, T. et al. Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc. Natl. Acad. Sci. USA 99, 996-1001 (2002).
34. Granum, P. E. Clostridium perfringens toxins involved in food poisoning. Inter. J. Food Microbiol. 10, 101-112 (1990).
35. McClane, B. A. The complex interactions between Clostridium perfringens enterotoxin and epithelial tight junctions. Toxicon 39, 1781-1791 (2001).
36. Chalmers, G. et al. Multilocus sequence typing analysis of Clostridium perfringens isolates from necrotic enteritis outbreaks in broiler chicken populations. J. Clin. Microbiol. 46, 3957-3964 (2008).
37. Coursodon, C. F., Glock, R. D., Moore, K. L., Cooper, K. K. & Songer, J. G. TpeL-producing strains of Clostridium perfringens type A are highly virulent for broiler chicks. Anaerobe 18, 117-121 (2012).
38. Ohtani, K. & Shimizu, T. Regulation of Toxin Production in Clostridium perfringens. Toxins 8, 207 (2016).
39. Ohtani, K. & Shimizu, T. Regulation of toxin gene expression in Clostridium perfringens. Res. Microbiol. 166, 280-289 (2015).
40. Honda, K. & Littman, D. R. The microbiome in infectious disease and inflammation. Immunology 30, 759-795 (2012).
41. Lassen, K. G. et al. Atg16l1 t300a variant decreases selective autophagy resulting in altered cytokine signaling and decreased antibacterial defense. Proc. Nat. Acad. Sci. USA 111, 7741-7747 (2014).
42. Coccia, M. et al. IL-1beta mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4 (+) Th17 cells. J. Exp. Med. 209, 1595-1609 (2012).
43. Schirmer, M. et al. Linking the human gut microbiome to inflammatory cytokine production capacity. Cell 167, 1125-1136 (2016).
44. Clemente, J. C., Ursell, L. K., Parfrey, L. W. & Knight, R. The impact of the gut microbiota on human health: an integrative view. Cell 148, 1258-1270 (2012).
45. Round, J. L. et al. The toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332, 974-977 (2011).
46. Tezuka, H. et al. Regulation of iga production by naturally occurring tnf/inos-producing dendritic cells. Nature 448, 929-933 (2007).
47. Turner, J. R. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809 (2009).
48. Shipitsyna., E. et al. Composition of the vaginal microbiota in women of reproductive age-sensitive and specific molecular diagnosis of bacterial vaginosis is possible? PLoS ONE 8, e60670 (2013).
49. Abramov, V. et al. Melnikov probiotic properties of Lactobacillus crispatus 2, 029: Homeostatic interaction with cervicovaginal epithelial cells and antagonistic activity to genitourinary pathogens. Probiotics Antimicro. Proteins 6, 165-176 (2014).
50. Drissi, F., Labas, N., Merhej, V. & Raoult, D. Draft Genome Sequence of the Lactobacillus agilis Strain Marseille. Genome Announc. 3, e00840-15 (2015).
51. Gudina, E. J., Fernandes, E. C., Teixeira, J. A. & Rodrigues, L. R. Antimicrobial and anti-adhesive activities of cellbound biosurfactant from Lactobacillus agilis CCUG31450. RSC Adv. 5, 90960-90968 (2015).
52. Meimandipour, A. et al. Selected microbial groups and short-chain fatty acids profile in a simulated chicken cecum supplemented with two strains of Lactobacillus. Poult. Sci. 89, 470-476 (2010).
53. Liu, X. et al. Lactobacillus salivarius isolated from patients with rheumatoid arthritis suppresses collagen-induced arthritis and increases treg frequency in mice. J. Interferon Cytokine Res. 36, 706-712 (2016).
54. Pasciak, M., Orska, S. G., Jawiarczyk, N. & Gamian, A. Lactobacillus johnsonii glycolipids, their structure and immunoreactivity with sera from inflammatory bowel disease patients. Microb. Biotechnol. 0, 000-000 (2016).
55. Dahiya, J. P., Hoehler, D., Wilkie, D. C., Van Kessel, A. G. & Drew, M. D. Dietary glycine concentration affects intestinal Clostridium perfringens and Lactobacilli populations in broiler chickens. Poult. Sci. 84, 1875-1885 (2005).
56. Deplancke, B. et al. Selective growth of mucolytic bacteria including Clostridium perfringens in a neonatal piglet model of total parenteral nutrition. Am. J. Clin. Nutr. 76, 1117-1125 (2002).
57. Malinen, E., Kassinen, A., Rinttila, T. & Palva, A. Comparison of real-time PCR with SYBR Green I or 5'-nuclease assays and dotblot hybridization with rDNAtargeted oligonucleotide probes in quantification of selected faecal bacteria. Microbiology 149, 269-277 (2003).
58. Steed, H. et al. Bacterial translocation in cirrhosis is not caused by an abnormal small bowel gut microbiota. FEMS Immunol. Med. Mic. 63, 346-354 (2011).
59. Luo, R., Liu, B., Xie, Y., Li, Z. & Huang, W. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18 (2012).
60. Zhu, W., Lomsadze, A. & Borodovsky, M. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 38, e132 (2010).
61. Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150-3152 (2012).
62. Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59-60 (2015).
63. Huson, D. H., Mitra, S., Ruscheweyh, H., Weber, N. & Schuster, S. C. Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21, 1552-1560 (2011).