Effect of some plant extracts on growth performance, intestinal morphology, microflora composition and activity in broiler chickens
J. K. Vidanarachchi B , A. V. Elangovan C , L. L. Mikkelsen A , M. Choct A and P. A. Iji A DA School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.
B Department of Animal Science, University of Peradeniya, Peradeniya 20400, Sri Lanka.
C National Institute of Animal Nutrition and Physiology, Adugodi, Bangalore 560 030, India.
D Corresponding author. Email: piji@une.edu.au
Animal Production Science 50(9) 880-889 https://doi.org/10.1071/AN10011
Submitted: 14 January 2010 Accepted: 22 May 2010 Published: 29 September 2010
Abstract
An experiment was conducted to study the effects of water-soluble carbohydrate extracts from Cabbage tree (Cordyline australis), Acacia (Acacia pycnantha), and Undaria seaweed (Undaria pinnatifida) (at 5 or 10 g/kg diet) on the performance and gut microbiota of broilers. The plant extracts had no negative effect on growth performance, except that a high level of Undaria extract in the diet suppressed the growth of broiler chicks. Ileal digesta viscosity was increased (P < 0.05) and apparent ileal digestibility of fat was depressed (P < 0.05) in birds fed the higher level of Undaria extract compared with the negative control. The plant extracts increased (P < 0.05) the numbers of lactobacilli in the ileum and caeca. The high levels of Acacia extract and Undaria extract significantly (P < 0.05) reduced the population of coliform bacteria in the ileum compared with the negative control group. The population of Clostridium perfringens in caeca, but not the ileum, was reduced (P < 0.05) by the plant extracts. An antibiotic positive control reduced the population of C. perfringens in both the ileum and caeca compared with the negative control group. The plant extracts altered microbial fermentation patterns in the ileum and caeca. The higher level of Undaria extract reduced villus height in the ileum while the antibiotic diet resulted in higher (P < 0.05) villus height and villus height : crypt depth ratio compared with the negative control group. The results of the study suggest that prebiotic plant extracts had no negative effect on performance of broilers except at a high level (10 g/kg diet) of Undaria extract. The plant extracts beneficially modulated the composition of the microflora in the ileum and caeca by increasing the number of lactobacilli and reducing harmful bacteria, such as potential pathogenic coliforms and C. perfringens.
Aarestrup FM
(1999) Association between the consumption of antimicrobial agents in animal husbandry and the occurrence of resistant bacteria among food animals. International Journal of Antimicrobial Agents 12, 279–285.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Adams MR, Hall CJ
(1988) Growth inhibition of food-borne pathogens by lactic and acetic acids and their mixtures. International Journal of Food Science & Technology 23, 287–292.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Anderson DB,
McCracken VJ,
Aminov RI,
Simpson JM,
Mackie RI,
Verstegen MWA, Gaskins HR
(1999) Gut microbiology and growth-promoting antibiotics in swine. Pig News and Information 20, 115N–122N.
Ao Z, Choct M
(2003) Early nutrition for broilers – a two edged sword? Australian Poultry Science Symposium 15, 149–152.
Butaye P,
Devriese LA, Haesebrouck F
(2003) Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on Gram-positive bacteria. Clinical Microbiology Reviews 16, 175–188.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Byrd JA,
Hargis BM,
Caldwell DJ,
Bailey RH, Herron KL , et al.
(2001) Effect of lactic acid administration in the drinking water during preslaughter feed withdrawal on Salmonella and Campylobacter contamination of broilers. Poultry Science 80, 278–283.
|
CAS |
PubMed |
Choct M,
Annison G, Trimble RP
(1992) Soluble wheat pentosans exhibit different anti-nutritive activities in intact and cecectomized broiler chickens. The Journal of Nutrition 122, 2457–2465.
|
CAS |
PubMed |
Choct M,
Hughes RJ,
Wang J,
Bedford MR,
Morgan AJ, Annison G
(1996) Increased small intestinal fermentation is partly responsible for the anti-nutritive activity of non-starch polysaccharides in chickens. British Poultry Science 37, 609–621.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Courtin CM,
Swennen K,
Broekaert WF,
Swennen Q,
Buyse J,
Decuypere E,
Michiels CW,
Ketelaere BD, Delcour JA
(2008) Effects of dietary inclusion of xylooligosaccharides, arabinoxylooligosaccharides and soluble arabinoxylan on the microbial composition of caecal contents of chickens. Journal of the Science of Food and Agriculture 88, 2517–2522.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Dibner JJ, Richards JD
(2005) Antibiotic growth promoters in agriculture: history and mode of action. Poultry Science 84, 634–643.
|
CAS |
PubMed |
Engberg RM,
Hedemann MS, Jensen BB
(2002) The influence of grinding and pelleting of feed on the microbial composition and activity in the digestive tract of broiler chickens. British Poultry Science 43, 569–579.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Flickinger EA,
Loo JV, Fahey GCJ
(2003) Nutritional responses to the presence of inulin and oligofructose in the diets of domesticated animals: a review. Critical Reviews in Food Science and Nutrition 43, 19–60.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Fuller R
(1977) The importance of lactobacilli in maintaining normal microbial balance in the crop. British Poultry Science 18, 85–94.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gajewska J,
Niemiec J, Rekosz-burlaga H
(2002) Effect of addition of ‘Greenline’ preparations to feed mixtures for broilers on the composition of their intestinal microflora. Acta Microbiologica Polonica 51, 71–78.
| PubMed |
Geier MS,
Torok VA,
Allison GE,
Ophel-Keller K, Hughes RJ
(2009) Indigestible carbohydrates alter the intestinal microbiota but do not influence the performance of broiler chickens. Journal of Applied Microbiology 106, 1540–1548.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gong J,
Forster RJ,
Yu H,
Chambers JR,
Wheatcroft R,
Sabour PM, Chen S
(2002) Molecular analysis of bacterial populations in the ileum of broiler chickens and comparison with bacteria in the cecum. FEMS Microbiology Ecology 41, 171–179.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Griggs JP, Jacob JP
(2005) Alternatives to antibiotics for organic poultry production. Journal of Applied Poultry Research 14, 750–756.
Guban J,
Korver DR,
Allison GE, Tannock GW
(2006) Relationship of dietary antimicrobial drug administration with broiler performance, decreased population levels of Lactobacillus salivarius, and reduced bile salt deconjugation in the ileum of broiler chickens. Poultry Science 85, 2186–2194.
|
CAS |
PubMed |
Guo FC,
Williams BA,
Kwakkel RP,
Li HS,
Li XP,
Luo JY,
Li WK, Verstegen MWA
(2004) Effects of mushroom and herb polysaccharides, as alternatives for an antibiotic, on the cecal microbial ecosystem in broiler chickens. Poultry Science 83, 175–182.
|
CAS |
PubMed |
Harrow SA,
Ravindran V,
Butler RC,
Marshall JW, Tannock GW
(2007) Real-time quantitative PCR measurement of ileal Lactobacillus salivarius populations from broiler chickens to determine the influence of farming practices. Applied and Environmental Microbiology 73, 7123–7127.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Iji PA, Tivey DR
(1998) Natural and synthetic oligosaccharides in broiler chicken diets. World’s Poultry Science Journal 54, 129–143.
| Crossref | GoogleScholarGoogle Scholar |
Iji PA,
Saki AA, Tivey DR
(2001) Intestinal structure and function of broiler chickens on diets supplemented with a mannan oligosaccharide. Journal of the Science of Food and Agriculture 81, 1186–1192.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Jamroz D,
Wiliczkiewicz A,
Wertelecki T,
Orda J, Skorupinska J
(2005) Use of active substances of plant origin in chicken diets based on maize and locally grown cereals. British Poultry Science 46, 485–493.
|
CAS |
Crossref |
PubMed |
Kleessen B,
Elsayed NAAE,
Loehren U,
Schroedl W, Krueger RM
(2003) Jerusalem artichokes stimulate growth of broiler chickens and protect them against endotoxins and potential cecal pathogens. Journal of Food Protection 11, 2171–2175.
Lan Y,
Xun S,
Tamminga S,
Williams BA,
Verstegen MWA, Erdi G
(2004) Real-time PCR detection of lactic acid bacteria in cecal contents of Eimeria tenella-infected broilers fed soybean oligosaccharides and soluble soybean polysaccharides. Poultry Science 83, 1696–1702.
|
CAS |
PubMed |
Lan Y,
Verstegen MWA,
Tamminga S, Williams BA
(2005) The role of the commensal gut microbial community in broiler chickens. World’s Poultry Science Journal 61, 95–104.
| Crossref | GoogleScholarGoogle Scholar |
Le Blay G,
Michel C,
Blottiere HM, Cherbut C
(1999) Prolonged intake of fructo-oligosaccharides induces a short-term elevation of lactic acid-producing bacteria and a persistent increase in cecal butyrate in rats. The Journal of Nutrition 129, 2231–2235.
|
CAS |
PubMed |
Maisonnier S,
Gomez J,
Bree A,
Berri C,
Baeza E, Carre B
(2003) Effects of microflora status, dietary bile salts and guar gum on lipid digestibility, intestinal bile salts, and histomorphology in broiler chickens. Poultry Science 82, 805–814.
|
CAS |
PubMed |
Mikkelsen LL,
Bendixen C,
Jakobsen K, Jensen BB
(2003) Enumeration of bifidobacteria in gastrointestinal samples from piglets. Applied and Environmental Microbiology 69, 654–658.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Miller TL, Wolin MJ
(1974) A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Applied Microbiology 27, 985–987.
|
CAS |
PubMed |
Montagne L,
Pluske JR, Hampson DJ
(2003) A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Animal Feed Science and Technology 108, 95–117.
| Crossref | GoogleScholarGoogle Scholar |
Niba AT,
Beal JD,
Kudi AC, Brooks PH
(2009) Bacterial fermentation in the gastrointestinal tract of non-ruminants: Influence of fermented feeds and fermentable carbohydrates. Tropical Animal Health and Production 41, 1393–1407.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Nousiainen J
(1991) Comparative observations on selected probiotics and olaquindox used as feed additives for piglets around weaning. 2. Effect on villus length and crypt depth in the jejunum, ileum, caecum and colon. Journal of Animal Physiology and Animal Nutrition 66, 224–230.
| Crossref | GoogleScholarGoogle Scholar |
Orban JI, Patterson JA
(2000) Modification of the phosphoketolase assay for rapid identification of bifidobacteria. Journal of Microbiological Methods 40, 221–224.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Owens B,
Ellis SM, McCracken KJ
(2003) Effects of yeast extracts, with and without oxygenised water, on the performance and gut histology of broiler chickens. British Poultry Science 44(Suppl. 1), S21–S22.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Patterson JA,
Orban JI,
Sutton AL, Richards GN
(1997) Selective enrichment of bifidobacteria in the intestinal tract of broilers by thermally produced ketoses and effect on broiler performance. Poultry Science 76, 497–500.
|
CAS |
PubMed |
Pedroso AA,
Menten JFM,
Lambais MR,
Racanicci AMC,
Longo FA, Sorbara JOB
(2006) Intestinal bacterial community and growth performance of chickens fed diets containing antibiotics. Poultry Science 85, 747–752.
|
CAS |
PubMed |
Petr J, Rada V
(2001) Bifidobacteria are obligate inhabitants of the crop of adult laying hens. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 48, 227–233.
|
CAS |
PubMed |
Rada V,
Sirotek K, Petr J
(1999) Evaluation of selective media for bifidobacteria in poultry and rabbit caecal samples. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 46, 369–373.
|
CAS |
Santos FSDL,
Farnell MB,
Tellez G,
Balog JM,
Anthony NB,
Torres-Rodriguez A,
Higgins D,
Hargis BM, Donoghue AM
(2005) Effect of prebiotic on gut development and ascites incidence of broilers reared in hypoxic environment. Poultry Science 84, 1092–1100.
| PubMed |
Smits CHM,
Veldman A,
Verkade HJ, Beynen AC
(1998) The inhibitory effect of carboxymethylcellulose with high viscosity on lipid absorption in broiler chickens coincides with reduced bile salt concentration and raised microbial numbers in the small intestine. Poultry Science 77, 1534–1539.
|
CAS |
PubMed |
Verdonk JMAJ,
Shim SB,
Van leeuwen P, Verstegen MWA
(2005) Application of inulin-type fructans in animal feed and pet food. The British Journal of Nutrition 93, S125–S138.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Vidanarachchi JK,
Iji PA,
Mikkelsen LL,
Sims I, Choct M
(2009) Isolation and characterisation of water-soluble prebiotic compounds from Australian and New Zealand plants. Carbohydrate Polymers 77, 670–676.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Vidanarachchi JK,
Iji PA,
Mikkelsen LL, Choct M
(2010) Fructans from Rengarenga lily (Arthropodium cirratum) extract and Frutafit as prebiotics for broilers: their effects on growth performance, digestive organ size, gut morphology and nutrient digestibility. Asian-Australasian Journal of Animal Sciences 23, 580–587.
|
CAS |
Xu ZR,
Hu CH,
Xia MS,
Zhan XA, Wang MQ
(2003) Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poultry Science 82, 1030–1036.
|
CAS |
PubMed |
Zdunczyk Z,
Jankowski J, Juskiewicz J
(2005) Performance and intestinal parameters of turkeys fed a diet with inulin and oligofructose. Journal of Animal and Feed Sciences 14, 511–514.
Zhu XY,
Zhong T,
Pandya Y, Joerger RD
(2002) 16S rRNA-based analysis of microbiota from the cecum of broiler chicken. Applied and Environmental Microbiology 68, 124–137.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |