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Assessing the effect of administering probiotics in water or as a feed supplement on broiler performance and immune response
Dr M.A. Karimi Torshizi , A.R. Moghaddam , Sh. Rahimi & N. Mojgani
a a a a b

Department of Poultry Science, Faculty of Agriculture, Tarbiat Modares University, P.B. 14115-336, Tehran

Department of Biotechnology, Razi Vaccine and Serum Research Institute, Karaj, Iran

Version of record first published: 10 May 2010

To cite this article: Dr M.A. Karimi Torshizi, A.R. Moghaddam, Sh. Rahimi & N. Mojgani (2010): Assessing the effect of administering probiotics in water or as a feed supplement on broiler performance and immune response, British Poultry Science, 51:2, 178-184 To link to this article:

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MOGHADDAM. 14115-336. Two routes of probiotic administration in broiler farms.B. 2006).British Poultry Science Volume 51. perfect environmental and nutritional conditions (no stresses present). compared to the control and feed groups.A.R. which also improved T-cell dependent skin thickness response to phytohaemagglutinin (PHA) injection. Blankenship. 2008). A large number of reports of research using probiotics on poultry have shown very variable results.. and poor animal welfare. frequency of administration. 1992.B.. Tarbiat Modares University. 2002) and more recently the vent lip method (Higgins et al. Karimi Torshizi. Spleen (28 and 42 d) and bursa (42 d) relative weights were influenced by method of probiotic administration. A. feed intake (FI) and feed conversion ratio (FCR) improved when probiotic was provided via drinking water. MOJGANI1 Department of Poultry Science. poor storage conditions.. RAHIMI AND N. They reported that administration of probiotics via drinking water significantly affected live weight gain and feed conversion efficiency at the end of the day Accepted for publication 28th October 2009. The method of probiotic administration can influence the performance and immune competence of birds. KARIMI TORSHIZI. Watkins and Kratzer. 3.. Faculty of Agriculture. oral dosing (Ghadban. were compared using 360 one-day-old male broiler chickens. Tehran and 1Department of Biotechnology. Probiotic administration reduced plasma cholesterol and triglyceride concentrations. the use of spray (Pivnick and Controls received no probiotics or antimicrobials. INTRODUCTION Probiotics are possible alternative to antibiotics as growth promoters. The most common routes of administrating probiotic preparations are in feed and drinking water (Tortuero. improper source of microorganisms. Mastbaum et al. Tarbiat Modares University. 2007b). (1997) used probiotic either via the feed or drinking water in broilers. 1993). 4. The water group received a probiotic preparation at a rate of 0Á5 g/l. Iran Downloaded by [Universidad Autonoma Metropolitana] at 11:33 09 July 2012 Abstract 1. P. Faculty of Agriculture. in water and in feed. 1997). 1989). Department of Poultry Science. dosage levels. Edens et al. Several factors could account for these discrepancies including. Performance of broilers in terms body weight gain (BWG). 178—184 Assessing the effect of administering probiotics in water or as a feed supplement on broiler performance and immune response M. Tehran. Karaj. Generally probiotic preparations are used on farms as soon as chicks arrive. contamination of antimicrobial chemicals.1080/00071661003753756 . E-mail: karimitm@modares. Schneitz et al. 1982. and the feed group received it at an inclusion rate of 1 g/kg. P. pp. Oral administration of lactobacilli to broiler chickens caused increased phagocytosis of enterocytes and an increase in serum IgG and IgM (Koenen et al. They also emphasised that this Correspondence to: Dr M. they are live microorganisms that contribute to the health and balance of host intestinal tract (Fuller.A. Number 2 (April 2010). and administration via drinking water appears to be superior to the more conventional in-feed supplementation method. 1990. Sh. One of the proposed mechanisms responsible for benefits of probiotic is an immunomodulatory effect (Higgins et al. 1973. 2.. The effect of challenge by dinitrochlorobenzene (DNCB) depended on the method of probiotic administration . Razi Vaccine and Serum Research Institute. 1992. 14115-336. 1983) less common are in ovo injection (Cox et al.. from almost negative and absent effects to dramatic positive effects. as well as method of probiotic administration. ISSN 0007–1668(print)/ISSN 1466–1799 (online)/10/020178—7 ß 2010 British Poultry Science Ltd DOI: 10.

Blood biochemistry Blood specimens (1Á5 ml) were taken from the brachial vein of 6 birds per experimental group at 40 d to determine haemoglobin. 1999). electrical conductivity 620 mmohs/cm and free residual chlorine 0 mg/l. 51Á74 mg. plantarum. B12. 0Á1 ml of 5% (v/v. Folic acid.8 IU. 1Á97 mg. Immune system competence Lymphoid organ weights Table 1. Zn. SRBC was injected into the breast muscle. 60 mg. 0Á38 mg. The counts for lactic acid bacteria in feed and water were not assessed. Niacin. Regardless of route. Serum specimens were taken at 40 d to determine antibody produced . Performance Data on performance (average daily feed and water intake. 8. 22—42 and 1—42 d). so in order to maintain the same amount of probiotic microorganisms received. 7. 320 mg. Biotin. suspension in sterile PBS) of 9 chicks per treatment at 35 d. 60 mg. Mn. L. The actual total count of lactic acid bacteria in the preparation was verified by a count on MRS agar under microaerophilic conditions (Singleton. The purpose of the present study was to compare the effects on broiler performance and immune competence of administrating probiotic in drinking water or in feed. administered probiotic to Japanese quail via feed and drinking water (1Á5 g/kg or l). Spleens and bursae were weighed and expressed as: (organ weight/body weight) Â 100. Fe. L. The drinking water group had probiotic (Protexin. Vit. I. 28 mg. 1994). UK. MATERIALS AND METHODS Animals. Streptococcus thermophilus and Candida pintolopesii) at a concentration of 0Á5 g/l of drinking water. Pyridoxine. Enterococcus faecium. Riboflavin. body weight gain and feed conversion ratio) were recorded weekly and are presented here on a periodic basis (1—21.PROBIOTIC ADMINISTRATION VIA WATER OR FEED 179 Downloaded by [Universidad Autonoma Metropolitana] at 11:33 09 July 2012 beneficial effect was clearer at the end of the day 31. Protexin probiotic was used because it was readily dipersable in water. 6Á4 mg. then maintained there to the end of experiment. 4Á8 mg. 1Á2 mg. Humoral immune response to sheep red blood cell (SRBC) Supplied per kg diet: Vit. Lactobacillus acidophilus. Chicks had free access to non-medicated water and starter (1—21 d). Bifidobacterium bifidum. 3Á2 mg. The temperature was set at 32 C on the first day. Arslan and Saatci (2004). 0Á69 mg. consisting of 9 different microorganisms — each with similar counts. L. Providing probiotic in feed is simpler as a part of diet preparation in feed mill plants. cholesterol and triglyceride concentrations using commercial diagnostic kits (Pars Azmun. thiamine. D3. the concentration of protexin in the-water was half of that in the feed. Broiler chickens maintained at moderate temperature usually consume twice as much water by weight as of feed (NRC. Cu. Iran). 0Á16 mg. gradually reduced to 24 C by the third week. 0Á008 mg. Choline. Birds in the feed group received diets supplemented with the same probiotic preparation at a concentration of 1 g/kg of diet. Pantothenic acid. Composition of the experimental diets (g/kg) Ingredients Yellow maize Soybean meal Fish meal Vegetable oil Dicalcium phosphate Calcium carbonate Sodium chloride Premix1 DL-Methionine Calculated values Metabolisable energy MJ/kg Crude protein 1 Starter 562Á0 330Á0 40Á0 37Á8 12Á0 10Á0 2Á0 5Á0 1Á2 12Á97 220 Grower 625Á7 295Á0 25Á0 26Á0 10Á0 10Á0 2Á3 5Á0 1Á0 12Á55 200 At 28 and 42 d. Se. The lighting pattern was 23 h L : 1 h D. K3. Vit. Of the two most practical methods of probiotic administration. rhamnosus. total dissolved solid 404 mg/l. Birds in the control group received no probiotic in either water or in feed. A. to approximately compensate for differences in water and feed consumption. 1Á76 mg. feed conversion and feed conversion efficiency of these birds.040 IU. and grower (22—42 d) diets based on maize—soybean meal (Table 1). Vit. bulgaricus. pH 7Á98. 0Á12 mg. The drinking water was untreated well water with following specification. feed supplementation is more conventional while provision via drinking water is used to a limited extent. totaling up to 9 log cfu/g. 2. 6 birds per experimental group were weighed and killed humanely. E. the species were Aspergillus oryzae. Vit. Three hundred and sixty 1-day-old male broiler chicks (Ross 308) were assigned at random to three experimental groups. Each consisted of 6 replications of deep litter pens (2 Â 1 m) of 20 birds. probiotic administration improved live weight.000 IU. diets and probiotic administration University approved methods were applied in all animal care.

Cellular immune response DNCB challenge Downloaded by [Universidad Autonoma Metropolitana] at 11:33 09 July 2012 On day 28. Generally the probiotic via drinking water increased body weight gain of broilers throughout production periods compared to the control group (P50Á05). PHA-M induced lymphoproliferation Phytohemagglutinin-M (Gibco. 1990). Feed conversion ratios were affected by treatment.. This ratio was not affected by probiotic administration (P40Á05). when an inoculum of bacteria is first introduced into a growth medium. Statistical analysis Mean values between treatments were compared using analysis of variance followed by least significant difference test. grower and whole period of production are presented in Table 2. while improvement in efficiency of feed utilisation might also be involved. were sensitised (Verma et al. whilst a similar area on the left side received the solvent without DNCB as a control. the water group received slightly less of the probiotic preparation than the feed group. The-water group had the highest feed intake in the starter period. Water intake was not influenced by probiotic provision during the first 21 d (P40Á05).and 1—42-d periods (P50Á01). It seems that probiotic in water survives the demanding conditions of the upper gut. Improvement of feed conversion ratio was evident in the water group over control and feed groups during both grower and overall phases (P50Á05). In this study the actual water/feed ratio was less than two. Increase in total digestive enzyme activity in the treated groups (originating both from the bird (endogenous activity) and from microorganisms) could to some extent account for the improved probiotic performance in our trial. Regardless of culture system (batch or continuous). in part.  is the population mean. Jin et al. rather than a direct effect of probiotic administration per se.. 1996a. 2004) by a single percutaneous application of 1-chloro-2. it probably requires a period to adapt to its new . The diluting ability of water might confer further benefit by reducing the negative impact of gastric acid and digestive secretions like bile and enzymes on the survivability of probiotic microorganisms in an aqueous milieu. including increased lipid. 12 birds per treatment. USA). it may be that this trend is a consequences of a link between water and feed intake. Feed conversion data show that the increase in body weight gain is not a simple consequence of increased feed intake. Statistical model of ANOVA procedure of SAS (1990) used was: Yij ¼  þ Ai þ "ij where Yij is the observation. protein. A total of 250 ml of DNCB (10 mg/ml of acetone and olive oil 4 : 1). While water intake was influenced by probiotic supplementation in a manner similar to the feed intake over 22—42. were applied on a featherless area of the right side. 1990.A.. Ai is the administration method effect (i ¼ 1À3) and "ij is the residual error. Changes in mean skin thickness before and 24 h postchallenge were assessed using digital calipers (Mitutoyo. Table 2 shows water/feed ratio values. KARIMI TORSHIZI ET AL. Provision of probiotic in water increased body weight gain compared to probiotic in the feed (P50Á05). in spite of our initial assumption that water intake would be double food intake. Neutralisation of enterotoxin by probiotic microorganisms and consequently better functionality of absorptive mucosal surfaces could explain. its better performance could thus not be attributed to a higher consumption than the feed group. Appetite stimulation due to probiotics has been reported in laying birds by Nahanshon et al. feed intake. T-cell mitogen was injected (100 mg dissolved in 100 ml of sterile PBS) to the right toe web of 9 birds per experimental group at 40 d.4-dinitrobenzene (DNCB-Merck). 1996). Significant differences were accepted if P 0Á05.b). The probiotic increased feed intake of birds during the grower phase and over the whole period compared to control (P50Á01). the beneficial results. while the feed supplemented group had higher feed intake than the water group during the grower and whole periods. The increase in toe web thickness was measured 24 h after injection (Corrier. Accordingly. and mineral retention. the lowest values were obtained in the water group (P50Á05). Probiotic increased daily body weight gain and feed intake of birds (Table 2).180 M. (1993. Several trials have described the digestive enzyme activity of lactic acid bacteria both in vitro and in vivo (Collington et al. water consumption and feed conversion ratio over the starter. against SRBC by micro-haemagglutination test as described by Wegmann and Smithies (1966). possibly due to a shorter transit time compared to solid particulate feed. Japan). RESULTS AND DISCUSSION Performance Body weight gain.

181 .Downloaded by [Universidad Autonoma Metropolitana] at 11:33 09 July 2012 Table 2. non-significant. abc Means with different superscripts in each column are significantly different. (*P50Á05. **P50Á01). Effect of probiotic administration in drinking water or feed on growth performance of broilers Feed intake (g/bird/d) 1—21** 45Á34b 47Á14a 45Á36b 87Á54 90Á77 87Á67 0Á66 1Á46 0Á30 1Á50 0Á79 152Á37b 158Á88a 162Á35a 99Á19b 103Á41a 104Á02a 266Á89b 279Á57ab 286Á37a 177Á21b 185Á17a 187Á01a 2Á79 22—42** 1—42** 1—21NS 22—42** 1—42** Water intake (ml/bird/d) Water/feed (ml/g) 1—21NS 22—42NS 1—42NS Feed conversion ratio 1—21NS 22—42* 1—42* Periods (d) 1—42** 52Á15c 55Á46a 53Á39b 0Á51 Body weight gain (g/bird/d) 1—21* 22—42* Probiotic supplementation Control Drinking water Feed 33Á59b 35Á18a 33Á77b 70Á71b 75Á71a 72Á99b 1Á932 1Á927 1Á933 0Á014 1Á750 1Á650 1Á762 0Á012 1Á788 1Á790 1Á798 0Á010 1Á26 1Á25 1Á26 0Á005 2Á15ab 2Á08b 2Á24a 0Á28 1Á71ab 1Á67b 1Á75a 0Á20 SEM 0Á31 0Á82 PROBIOTIC ADMINISTRATION VIA WATER OR FEED NS.

with heavier weights indicating higher immune competence. with the lowest values in the control group. surroundings — the less optimal these are. there is no net increase in bacterial numbers. (*P50Á01). The length of the lag phase will also depend on the age and general health of the cells in the inoculum. Immune system competence Lymphoid organ weights Spleen (28 and 42 d) and bursa (42 d) relative weights were influenced by probiotic administration. 1998b. However administration of probiotic through drinking water is not as easy as feed supplementation. which suggests any competitive interaction was absent. 2005). Some drawbacks of this route are listed below: (1) Uneven distribution of probiotic. Humoral and cellular immune response Antibody titre against SRBC was not affected by administration route (P40Á05). Gore and Qureshi (1997) used relative lymphoid organ weight (bursa of Fabricius and spleen) as criteria for immune response competence.A. KARIMI TORSHIZI ET AL. Our findings showed lymphoid organ weights were generally heavier when probiotic was administered (Table 4) and were greater in the water than in the feed group.. Spleen (P50Á01 at 28 d. Downloaded by [Universidad Autonoma Metropolitana] at 11:33 09 July 2012 cholesterol by some microorganisms. 2007a). by accelerating the revival process of probiotic microorganisms and consequently shorten the lag phase. Cholesterol and triglyceride concentrations in plasma were significantly reduced by probiotic application (Table 3). especially folic acid. (4) Interference with water administered medications. and could not be administered in the drinking water. During this period. containing no free water. while blood haemoglobin was not influenced by probiotic and its different administration routes (P40Á05). though the mechanism remains to be clarified (Klaver and van der Meer. It seems that reconstitution of probiotic preparations in water could facilitate the subsequent adaptation process to a gastrointestinal milieu. Continuous supply of a probiotic may require pure water and might interfere with some medications and in addition may need a special device for appropriate dosing. (1998a). Treatment had a clear effect at 28 d but at 42 d there was no difference between water and feed groups. which might imply more susceptibility to environmental conditions. triglyceride and blood haemoglobin concentrations are shown in Table 3. Microorganisms are more active in hydrated conditions (in water) in comparison to the limited water content of dry feed (about 90% dry matter). In contrast. Table 3 shows that in this study the probiotic did not influence haemoglobin concentrations. (2) When feed is withheld from hatched chicks. P50Á05 at 42 d) and bursa (P50Á01 at 42 d) relative weights were highest in the water group. however the cells are metabolically active (Hogg.182 M. Mohan et al. within the host animal. These scenarios might result in a faster colonisation of probiotic microorganisms. the longer the period of adaptation. non-significant. which is an indispensable factor required for microbial revival and proliferation. 1993. Effect of probiotic administration in drinking water or feed on plasma cholesterol and blood haemoglobin Probiotic supplementation Plasma Plasma HaemoglobinNS cholesterol* triglyceride* mg/dl 155Á95a 130Á25b 138Á91ab 4Á22 125Á89a 90Á86b 90Á48b 6Á35 7Á52 7Á27 7Á34 0Á08 Control Drinking_water Feed SEM NS. It should be noted that some probiotic preparations are not dispersible in water. who administered probiotics in the feed.. (3) Water sanitation practices. Probiotic administration lowered plasma cholesterol and triglyceride concentrations compared to control group (P50Á01). . found no significant effect of single strain or mix culture of 12 lactobacilli on relative weights of spleen and bursa of broilers.. (5) Requirement for specialised dosing devices to provide constant doses of fresh probiotic in water pipe lines. The greatest skin response to DNCB (P50Á05) and PHA (P50Á01) was in the water group. The route of administration was not significant. 2002). Commercial probiotic preparations are generally manufactured and marketed in lyophilised form. although the water group showed lower plasma cholesterol in comparison to the feed group. is well documented. as sometimes chicks refuse to drink. There is uncertainty regarding probiotics competiting for some nutrients. application of probiotics via water is not always optimal (Ghadban. The lowering of Table 3. Jin et al. Blood biochemistry Plasma cholesterol. ab Means with different superscripts in each column are significantly different. whereas skin response to DNCB challenge or PHA injection was influenced by it. 1996). Jin et al. which in turn is a pre-requisite for most of the beneficial properties of probiotics (Higgins et al.

34: 369–373. M. D. J..A. H. cell mediated immunity as assessed by contact sensitivity to DNCB and PHA-M injection Sampling time Relative weight (g/100 g body weight) Spleen 28 d** Probiotic supplementation Control Drinking water Feed SEM 42 d* 28 dNS Bursa 42 d** HA titre (Log 2) 40 dNS Increase in skin thickness (%) to DNCB 28 d* PHA 24 h** 0Á095b 0Á138a 0Á088b 0Á008 0Á081b 0Á119a 0Á119a 0Á007 0Á185 0Á188 0Á172 0Á004 0Á130b 0Á204a 0Á191a 0Á012 2Á33 2Á50 2Á33 0Á11 1Á60b 2Á26a 1Á82b 0Á11 0Á64c 1Á16a 0Á89b 0Á08 NS. Archive fur Geflugelkunde. J. 13: 975–980. Archive fur Geflugelkunde. G. COX..PROBIOTIC ADMINISTRATION VIA WATER OR FEED 183 Table 4. BREWER. S. abc Means with different superscripts in each column are significantly different... B..A.. FULLER. Haghighi et al. ERF. B. Probiotic administration via drinking water significantly improved cellular immune response to DNCB and PHA. Poultry Science.M. & SAATCI.. ACKNOWLEDGEMENTS Funding provided by the Research Affairs of Tarbiat Modares University. Clinical Diagnostic Laboratory Immunology. J. VICENTE. (2006) Probiotics stimulate production on natural antibody in chickens. L... & ARMSTRONG. Downloaded by [Universidad Autonoma Metropolitana] at 11:33 09 July 2012 The immune modulation property of probiotics has been well addressed (Koenen et al. **P50Á01).. The method of administration affected probiotic efficiency. (1997) Enhancement of humoral and cellular mmunity by vitamin E after embryonic exposure. However. haemagglutinin titres against SRBC (HA titre). DNCB challenge has been successfully applied (Swamy et al... & HARGIS. EDENS. The authors thank Afshin Khakpour for improving the manuscript. HAGHIGHI. B.L. 68: 160–163. (1990) Comparison of phytohemagglutinin induced cutaneous hypersensivity reactions in the interdigital skin of broiler and layer chickens. Poultry Science.. while probiotic provision in the feed improved cellular immune response to PHA injection compared to control (P50Á01). A. J. R.P. Poultry Science.A.N. G.R. To our knowledge.R.. 5: 593–597.W.. D.A.A. 64: 59–70. 2004) to test cellular immune response in broilers fed mycotoxincontaminated feed. J. J. 2004. & DOBROGOSZ. N. I.. TELLEZ. N. (1992) In ovo application of competitive exclusion bacteria. HAYES.. (1990) The influence of inclusion of either an antibiotic or a probiotic in the diet on the development of digestive enzyme activity in the pig. Effect of probiotic administration in drinking water or feed on the relative weights of lymphoid organs. A. (2002) Probiotics in broiler production — a review.R. 12: 1387–1392. 2007b). Haghighi et al. 2006). (*P50Á05. Probiotic administration through drinking water slightly improved antibody production against SRBC in comparison to control and probiotic fed groups (P40Á05).. GORE.R. 76: 984–991.L. I.. REFERENCES AHMAD. P. Journal of Applied Bacteriology. reported enhancement of serum and intestinal natural antibodies to several foreign antigens. BAILEY. GONG. F. J. 86: 1662–1666.M. COX. In conclusion. & HARGIS. GYLES.E. R.S. L. SANEI. Probiotic enhances the immune competence of broilers by macrophage activation.E.. BLANKENSHIP. the current study is the first report of DNCB test used in probiotic immune-stimulating assays. HIGGINS.D. CHAMBERS.S. PARKER.J. 66: 365–378. Iran is acknowledged. H. Poultry Science. N.. CORRIER. HIGGINS.. with drinking water as the method of choice because of its greater efficiency. H. our results showed that probiotic administration benefited broiler performance. (2004) Effects of probiotic administration either as feed additive or by drinking water on performance and blood parameters of Japanese quail. S. . S. M. ZHOU.D. B..S.J. PARVIZI. H.C... & WILLIAMS. O.. COLLINGTON. British Journal of Nutrition. 69(Suppl 1): 162–166. HIGGINS. M. 72: 1667–1672...E.R. A. STERN. HIGGINS.. increase of systemic and local antibody production (Ahmad... CHAMBERS. PARKHURST. 2004.C. HAYES. C. C. W. C.G. (2005) Modulation of antibody-mediated immune response by probiotics in chickens. Avian Disease. (2007a) Temporal effects of lactic acid bacteria probiotic culture on neonatal broilers. G. & QURESHI.. BAILEY. A. Higgins et al. WOLFENDEN. J. enhanced immune response to DNCB challenge was not significant in probiotic fed group in comparison to control (P40Á05)..P. D. 76: 179–196. non-significant. SANEI. S. (1997) Principles of ex ovo competitive exclusion and administration of Lactobacillus reuteri. G. Verma et al. 2005.F. GONG. GYLES. GISAVI. S. GHADBAN. C.B.K. & SHARIF. ARSLAN. (1993) Two-step mucosal competitive exclusion flora treatment to diminish Salmonellae in commercial broiler chickens. J. HAGHIGHI. G.L. & BLANKENSHIP. 22: 49–58. International Journal of Poultry Science..S. (2006). GAONA-RAMIREZ. some blood biochemical values and immune modulation. (1989) A review: probiotics in man and animals. M. (2006) Effect of probiotics on broilers performance. & SHARIF. CASAS. WOLFENDEN. HENDERSON. Poultry Science. Clinical Vaccine Immunology..

J. 83: 533–543.V.. MOHAN. 52: 197–203. SAS INSTITUTE (1990) SAS/STATÕ User’s Guide. British Poultry Science.M. NURMI. O. H.) Developments in Food Microbiology.. KRAMER. (1984) Drinking water treatment with commercial preparation of a concentrated Lactobacillus culture for broiler chickens.. Applied Environmental Microbiology. G. 11th European Symposium on Poultry Nutrition. & AMEENA. HO. WEGMANN.D. JIN.. F. L. S. Animal Feed Science and Technology.A. M. RAND. M. (1996) Performance of Single Comb White Leghorn layers with a live microbial during the growth and egg laying phases. 224—225. 511—513. G. GRIMBERG.. HIGGINS.. British Poultry Science. Y. National Academic Science). . HENDERSON. (1998b) Growth performance. VIOLA. (1973) Influence of the implantation of Lactobacillus acidophilus in chicks on the growth. S. & JALALUDIN.A. UK. M.). J. KARROW. NOY. L. Y. & JALALUDIN. ABDULLAH. 86: 2315–2321. L. (2004) Effect of graded levels of aflatoxin. K. Animal Feed Science and Technology. (1992) Competitive exclusion in the young bird: challenge models. H. & NURMI. 9: 397–403. (1996b) Effect of Lactobacillus cultures on digestive enzymes in chicken intestine. (1993) The assumed assimilation of cholesterol by lactobacilli and Bifidobacterium bifidum is due to their bile-salt deconjugating activity.. S. S. G. SAS Institute Inc. 37: 395–401. W. KOENEN. SWAMY. TORRES-RODRINGUEZ. (1993) Effect of direct-fed microbials on nutrient retention and parameters of Single Comb White Leghorn pullets.. (1982) The Nurmi concept and its role in the control of Salmonella in poultry. E..Z. NATARAJAN. H.N. pp.N. 6: 67–75. & LITMAN. SMITH. S.E. & JALALUDIN.J. feed conversion. L. WOLFENDEN. NAKAUE. NURMI. 72: 87. A.S. pp. & BHASKARAN. R. NC.A... R. Biotechnology and Medicine. MARKS.and meat-type chickens. G.. 45: 355–366. S.A. NUOTIO. Y. World’s Poultry Science Association Proceedings. B. B.W. 376—377 (London. pp. & MIROSH. (2004) JEURISSEN. & JALALUDIN. HERES.A. MEAD. (Ed. (1990) Droplet application for protecting chicks against Salmonella colonization by competitive exclusion.H.. & VAN DER MEER. (1966) A simple haemagglutination system requiring small amounts of red cells and antibodies. Animal Feed Science and Technology. & PESTI.03 edition (Cary.P.W. KADIRVEL. (1997) Effects of the probiotic ‘‘PRIMALAC’’ on broilers administered either as a feed additive or in the drinking water. NAHANSHON.. ABDULLAH. Y. (1998a) Effects of adherent Lactobacillus cultures on growth. T. Veterinary Record.W. NAKAUE.. A. C. E. B. S. HIGGINS. HO.S. Poultry Science. & BOERMANS.A... & HARGIS. J..L. J. (1999) Bacteria in Biology. L.K. 59: 1120–1124. NATIONAL RESEARCH COUNCIL (1994) Nutrient Requirements of Poultry.A. M. T. YOSSILEWITSCH. (2004) Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on growth and immunological parameters of broiler chickens... SWAIN. S. ABDULLAH.Z. Poultry Science.. 5th edn.A. (1984) The roles of protein level and diet form in water consumption and abdominal fat pad deposition of broilers. R. Downloaded by [Universidad Autonoma Metropolitana] at 11:33 09 July 2012 (2007b) Effects of probiotic treatment in broiler chicks on intestinal macrophage numbers and phagocytosis of Salmonella Enteritidis by abdominal exudates cells. KEDEM. F.W. Poultry Science.. S. NUOTIO. MASTBAUM. (1996a) Influence of dried Bacillus subtilis and Lactobacillus cultures on intestinal microflora and performance in broilers. M.. B. Poultry Science.. & NURMI. (1996) Effect of probiotic supplementation on growth.. Poultry Science. in: DAVIS. HOGG. F.. intestinal microbial populations. malabsorption of fats syndrome and intestinal flora. 63: 1617–1625. WATKINS. ABDULLAH. SCHNEITZ. N. & MEAD. M. JIN. L. KARIMI TORSHIZI ET AL. British Poultry Science. A. 77: 1259–1265. S. SINGLETON. C.. John Wiley).N. release 6. E. (2008) Evaluation of a Lactobacillus-based probiotic culture for the reduction of Salmonella Enteritidis in neonatal broiler chicks. Transfusion.. Tokyo. DVORIN. nitrogen utilization and serum cholesterol in broilers. & BOERSMA..W. N. T. (2005) Essential Microbiology (West Sussex. pp. Japan. ochratoxin and their combinations on the performance and immune response of broilers. L. S.Z. 63: 1671–1673. HO. England. M. VERMA. SCHNEITZ. Poultry Science. & KRATZER. M. JIN. R. weight of organs and intestinal microflora and volatile fatty acids in broilers. DC.. P. M. HAKKIEN. TORTUERO. L..M.A. A. H. PIVNICK..H.E. E. 57: 25–38. VAN DER HULST.W..A.S. (Washington. Applied Science Publishers). & SMITHIES.. & MIROSH. Immunomodulation by probiotic lactobacilli in layer.. Poultry Science.N.. administration and reciprocal protection. International Journal of Food Microbiology. M. JOHRI.L.M.184 M.Z. JIN. S. L. L. H. H. 70: 197–209.. KLAVER. Y. 9th edn. 15: 241–255. NAHANSHON.. L. Proceedings of the 8th Animal Science Congress. TELLEZ. HO. 87: 27–31. Chiba. 126: 510.. John Wiley & Sons Ltd). M. ALI. 41—70 (London. Poultry Science.M.. and serum cholesterol of broilers fed diets containing lactobacillus cultures. 45: 512–518.