J. Appl. Poult. Res.
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J APPL POULT RES 2007. 16:555-562. doi:10.3382/japr.2006-00116
© 2007 Poultry Science Association
This Article
Right arrow Summary Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (2)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by García, V.
Right arrow Articles by Madrid, J.
Right arrow Search for Related Content
PubMed
Right arrow Articles by García, V.
Right arrow Articles by Madrid, J.

Research Reports

Effect of Formic Acid and Plant Extracts on Growth, Nutrient Digestibility, Intestine Mucosa Morphology, and Meat Yield of Broilers

V. García1, P. Catalá-Gregori, F. Hernández, M. D. Megías and J. Madrid

Department of Animal Production, University of Murcia, Campus de Espinardo 30071, Murcia, Spain

Correspondence: 1 Corresponding author: vgarcia{at}um.es


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The effect of formic acid and 2 plant extracts on performance traits, apparent ileal digestibility (AID), intestine mucosa morphology, and meat yield of broilers was studied in a 49-d experiment. There were 6 treatments: a negative control diet without additives (control); 10 ppm of avilamycin; 5,000 of formic acid; 10,000 ppm of formic acid; 200 ppm of plant extract based on a blend of oregano, cinnamon, and pepper essential oil; and 5,000 ppm of hydroalcoholic plant extract from sage, thyme, and rosemary leaves. A total of 312 Ross chicks were distributed into 24 groups of 13 in each, comprising 4 replicates per treatment. The performance data revealed significantly better FCR in all the supplemented diets except for the 5,000 ppm of hydroalcoholic plant extract diet. All additives improved AID of nutrients. Both acidifier inclusion levels improved villus height, and the group fed the 10,000 ppm of formic acid diet also had the greatest crypt depth; however, villus surface area was not influenced. Meat yield was not affected. It was concluded that the diets with 5,000 and 10,000 ppm of formic acid, and with 200 ppm of plant extract based on a blend of oregano, cinnamon, and pepper essential oils were similar to avilamycin and were beneficial for improving growth traits and nutrient AID. Furthermore, a positive effect of formic acid on intestine mucosa was observed. This experiment involved a small sample, so the additives that showed beneficial effects should be further studied in commercial farms.

Key Words: formic acid • plant extract • performance • nutrient digestibility • intestinal morphology • meat yield


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The use of antibiotic growth promoters (AGP) to improve animal performance and health has been practiced during the last 50 yr. Nevertheless, a full ban on the feed use of AGP came into effect in the European Union in 2006, based on the potential for a reservoir in food animals of an antibiotic-resistant bacterial population that could be transferred to humans [1]. This reality has led to a new urgency in the search for AGP replacements. Most supplements claimed to be alternatives to antibiotics have effects on the microflora, either directly or indirectly [2]. Organic acids and plant extracts are among the candidates for AGP replacement.

In poultry production, organic acids have been studied as a tool to reduce unwanted bacteria [3], and formic acid in particular has been shown to be particularly effective against Escherichia coli [4]. The beneficial effects of organic acids on the productive traits of pigs have been demonstrated in many studies, but consistent data have not been obtained for poultry [5].

On the other hand, various plant extracts, especially essential oils, have been investigated on the basis of their demonstrated in vitro antimicrobial activity [6, 7, 8, 9]. The results of inclusion of plant extracts on the growth performance of broilers [10] or pigs [11] are controversial. This study was conducted to assess the potential of formic acid and 2 plant extracts as possible alternatives to AGP. The parameters evaluated were growth performance, apparent ileal digestibility (AID) of nutrients, intestine mucosa morphology, and meat yield of broilers.


   MATERIALS AND METHODS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Dietary Treatments
Six experimental diets, with 4 replicates, were fed to broiler chicks for 49 d: a negative control diet, without additive supplementation (control); 10 ppm of avilamycin (AV) [12]; 5,000 ppm of formic acid (FA1); 10,000 ppm of formic acid (FA2) [13]; 200 ppm of plant extract (PE1) [14], based on a blend of oregano, cinnamon, and pepper essential oils (rich in cinnamaldehyde, carvacrol, and capsaicin); and 5,000 ppm of hydroalcoholic plant extract (PE2) [15], obtained from sage, thyme, and rosemary leaves (rich in rosmarinic acid, apigenin-7-glucoside, and isocutellarein-7-glucoside). All birds received a starter diet in crumble form from 1 to 21 d and a finisher diet from 22 to 49 d in pelleted form (4-mm die). The diets were consecutively prepared using the same batch of ingredients, and the different additives used were added together with the microingredients. Celite [16] was included as an acid-insoluble ash digestibility marker [17]. All diets were formulated to meet or exceed the nutrient requirements of broiler chickens [18]. These diets are usually used by local producers, who also add phytase, and xylanase is included when the diets are wheat-based. Both enzymes were added post pelleting in liquid form. The ingredient composition, estimated nutrient content [19], and analyzed chemical values of diets are shown in Table 1Go.


View this table:
[in this window]
[in a new window]

  		Table 1. Composition of the experimental diets
 
Birds and Experimental Facilities
A total of 312 male Ross 308 chicks [20], vaccinated against coccidia at 1 d of age [21], were used in this experiment. Chicks were randomly allotted to groups of 13 birds to each of 24 floor pens (1 x 1 m), with 4 pens per treatment. Each pen was equipped with a feeding trough and 4 nipple drinkers, and the floor was covered with clean litter. Pens were placed inside a commercial farm so that experimental animals were reared with their contemporaries at the farm. The initial temperature of 32°C was gradually reduced according to the age of the birds until reaching 20°C at the end of the experiment. The lighting cycle was 24 h from 1 to 3 d of age, 18 h from 4 to 20 d of age, 21 h from 21 to 35 d of age, and 23 h from 35 to 49 d of age. Experimental procedures followed the principles for care of animals in experimentation [22].

Measurements
Birds and feeds were weighed weekly on a pen basis. The BW gain (BWG), feed intake, and the FCR were determined. At 42 d of age, 5 chicks per replicate (20 per treatment) were randomly selected and killed by intravenous injection of sodium pentobarbital. The ileum, defined as the region from Meckel’s diverticulum to a point 40 mm proximal to the ileocecal junction, was dissected, and the contents were collected by gently flushing with distilled water into plastic containers. Ileal digesta were pooled within a pen, lyophilized, ground to pass through a 0.5-mm sieve, and stored at –18°C in airtight containers for nutrient AID determination. Within the above-mentioned birds, the jejunum was removed from 4 chicks per treatment and a morphological examination was done. The jejunum was defined as the portion of intestine extending from the bile duct entrance to Meckel’s diverticulum. Samples of jejunum (3-cm segments) were obtained at its midpoint and immersed in a phosphate-buffered formalin solution. Two portions per sample were cut perpendicular to the longitudinal axis of the intestine and embedded in paraffin wax. Transverse sections were cut (3 µm), stained by hematoxylineosin, and analyzed under a light microscope to determine morphometric indices by using image-analysis software [23]. The morphometric variables measured included villus height, crypt depth, and villus width at the top and the base. The villus surface area was calculated from the villus height and the villus width at half height. The mean from 10 villi per sample was used as the average value for further analysis.

At 49 d of age, the birds left in each pen or replicate were weighed, and the 5 chicks that were closest to the mean weight of the pen were selected and transported to a commercial slaughterhouse (20 birds per treatment). Feed was removed 12 h before processing. Birds were electrically stunned and slaughtered, and after blood removal were defeathered, processed, and eviscerated. Determinations of the carcass (without abdominal fat), right breast (skinless and boneless), and right thigh (with skin and bone) yield (g/kg of BW) were performed.

Chemical Analysis
Diet and ileal digesta were analyzed for nitrogen by the Kjeldahl method (AOAC) [24] and CP (N x 6.25). Dry matter was determined by drying in an oven at 103°C for 8 h. Acid-insoluble ash [25] and starch contents [26] were also analyzed. All values were expressed on a DM basis.

Statistical Analysis
The effects of additives on growth, AID of nutrients, intestine mucosa morphology, and meat yield were statistically analyzed by the GLM procedure with SPSS software [27]. When significant differences were found, the LSD test was conducted. All statements of significance are based on a probability of less than 0.05. The experimental unit was the pen.


   RESULTS AND DISCUSSION
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Measurements
Body weight gain, FCR, and AID of nutrients at 42 d of age are presented in Table 2Go. Type of diet influenced BWG (P < 0.05). Birds fed the PE2 diet had the lowest BWG but were not statistically different from the birds fed the AV, FA1, or FA2 diets. All additives tested except PE2 improved FCR compared with the negative control group (P < 0.001). The beneficial effect of growth promoter substances, such as antibiotics, on performance is related to a more efficient use of nutrients, which in turn results in an improved FCR [28]. This effect was also observed in birds fed the FA1, FA2 and PE1 diets. The AGP also improves the growth rate [28], which was not found in this study. Similar to our results, Runho et al. [29] indicated that the dietary addition of fumaric acid did not affect BWG of broilers but did improve FCR. Moreover, Hernández et al. [30] failed to observe any effect on the performance of chickens when formic acid (5,000 or 10,000 ppm) was added to the feeds. Nevertheless, the experiment was performed under ideal conditions of experimentation, which could explain the lack of effects observed, because the growth-enhancing effects of antimicrobial additives become apparent when chickens are subjected to suboptimal conditions, such as a less digestible diet or a less clean environment. In addition, AGP exert no benefits on the performance of germ-free animals, an aspect that clearly points to their effect as being one of antimicrobial activity rather than being caused by direct interaction with the physiology of the animal [31]. In the current trial, broilers were housed in floor pens placed inside a commercial farm, where they were reared with their commercial contemporaries. A knowledge of the animal housing environment is essential for accurate interpretation of results from academic cage trials, for example, where the micro-biological stresses on the animal would presumably be unrepresentative of those encountered under normal commercial conditions [31]. On the other hand, additional effects of AGP on parameters other than performance that also occur in germ-free animals include a reduction in gut size, including thinner intestinal villi and total gut wall, which result in a sparing use of the nutrients and an improvement in performance [32]. Chicks fed the PE1 diet also had a lower FCR than the negative control group, but a beneficial response to the PE2 diet was not observed. It has previously been reported that the effects of essential oils on growth performance in chickens are either positive or not significant. Lee et al. [33] found that dietary carvacrol and thymol at a concentration of 200 ppm lowered BWG and feed intake but improved FCR when female broilers were fed the respective diet for 4 wk. In contrast, Botsoglou et al. [10] reported that when dietary oregano essential oils, at concentrations of 50 and 100 ppm, were fed to broiler chickens for a period of 38 d, hardly any effects on BW and FCR could be demonstrated.


View this table:
[in this window]
[in a new window]

  		Table 2. The effect of formic acid and plant extracts on growth performance and apparent ileal digestibility of nutrients in broilers at 42 d of age1
 
Our data indicated a positive effect of all the additives tested on DM and CP AID in finisher diets (P < 0.001; Table 2Go). The digestibility results obtained in control birds were unusually low, either because of the method used or the health of the chicks. Even though the recommended procedure [34] and the most accurate marker [35] for AID determination were used, abnormally low values were found only in the control treatment. Second, all birds were apparently healthy (similar BWG in all groups), and litter analysis for moisture content and coccidia showed normal levels for both parameters. Therefore, these results do not explain the poor FCR found in the control diet. On the other hand, a high FCR is associated with low digestibility of the diet, as shown in the unsupplemented group.

Antibiotics are well known to alter the normal pathogenic and nonpathogenic flora of the gut, and these changes have a beneficial effect on the utilization of nutrients [36]. In this sense, Huang et al. [37] found that the supplementation of broiler diets with flavomycin increased the AID of DM and CP by 4 and 18 units, respectively, as compared with the negative control. In addition, Jamroz et al. [38] reported a 7.8% increase in N retention and improved AID of amino acids by 1 to 3 units when avilamycin was included in chickens diets. On the other hand, numerous authors [39] have observed an improved digestibility of DM, organic matter, ash, and nitrogen in diets with organic acids (including formic acid) in swine, but complete studies of the effect of organic acids on the nutrient digestibility of poultry are not as numerous. Hernández et al. [30] showed a positive effect of 10,000 ppm of formic acid on the AID of DM in chickens. Moreover, Runho et al. [29] found that fumaric acid at 0.5 to 10% increased the metabolizable energy of broiler diets. There is also evidence to suggest that dietary essential oils can improve digestion [40, 41]. In a previous study, Hernández et al. [42] reported an improvement in AID of DM of broiler diets also supplemented with PE1 and PE2, but the AID of CP was not affected.

The villus height, crypt depth, and villus surface area of broiler jejunum at 42 d of age are shown in Table 3Go. Chickens fed diets containing formic acid had the longest villi compared with the other treatment groups (1,273 and 1,250 vs. 1,088, 1,122, 1,056, and 1,207 µm for FA1 and FA2 vs. the control, AV, PE1, and PE2 diets, respectively). Good intestinal health in the poultry industry is of great importance to achieve target growth rates and feed efficiency [43]. Antimicrobial agents are known to reduce the intestinal microbial load, which in turn reduces the presence of toxins at this level that are associated with changes in intestinal morphology, such as shorter villi and deeper crypts [44]. Crypts of jejunum were deeper for birds fed the FA2 diet than birds fed the AV or PE1 diets (266 vs. 186 and 189 µm, for the FA2 vs. AV and PE1 diets, respectively; P < 0.05). Thus, FA2 supplementation increased both the villus height and crypt depth. Short-chain fatty acids have been demonstrated to stimulate the proliferation of normal crypt cells, enhancing healthy tissue turnover and maintenance [45]. This trophic effect was demonstrated by Frankel et al. [46], who found an increase in villus height, crypt depth, and surface area in the colon and jejunum of rats fed diets supplemented with butyric acid. In the current study, formic acid at 10,000 ppm seemed to exert such an effect, but to confirm the possible trophic effect of formic acid on the intestinal epithelium of broilers, further research is required. The villus surface area did not differ among treatments.


View this table:
[in this window]
[in a new window]

  		Table 3. Effect of formic acid and plant extracts on intestine mucosa morphology of broilers at 42 d of age1
 
The carcass, right breast, and right thigh yields of birds at 49 d of age were unaffected by supplements (Table 4Go). Leeson et al. [47] observed no effect on carcass weight when broilers were fed virginiamycin or 0.2 or 0.4% butyric acid, whereas carcass weight and breast meat yield increased in birds fed 0.2% butyric acid when bacitracin methylene disalicylate or 0.1 or 0.2% butyric acid were compared in another trial. In addition, Visek [48] demonstrated that the inclusion of antibiotics reduces the weight and length of the intestines in poultry, which has direct implications on carcass yield.


View this table:
[in this window]
[in a new window]

  		Table 4. The effect of formic acid and plant extracts on carcass, breast, and thigh yield of broilers at 49 d of age1
 
Finally, the FCR could be worsened for 2 reasons: first, because of a less efficient digestibility of feed, and second, because of a fattening of the BWG, as has been previously described by other authors [49]. In our case, the poor FCR found in the control diet was probably due to a lower digestibility of feed, because no differences on carcass yield were shown.


   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 

  1. Improved FCR were observed in the supplemented groups compared with the negative control group, except for the group fed the PE2 diet.
  2. The AID of all the nutrients measured was significantly improved by additives.
  3. A beneficial effect of formic acid on the villus height of chickens was observed. Moreover, formic acid at 10,000 ppm may exert a trophic effect on the intestinal epithelium, but further investigation to confirm such an effect is required.
  4. Between the 2 plant extracts assayed, the one based on a blend of oregano, cinnamon, and pepper essential oils (PE1) significantly improved the FCR and AID of nutrients.
  5. It is likely that the replacement for AGP will involve the use of multiple products in the diet. Thus, the combination of both alternatives (organic acids and essential oils) in the diet could be of great interest in future studies.
  6. Because the experiment conducted involved a small sample, the additives that showed beneficial effects should be studied further in commercial farms to obtain results that can be incorporated into practice.


   ACKNOWLEDGMENTS
 
The authors would like to thank Avícola Levantina S. A. (Murcia, Spain), government of the region of Murcia (Spain), and Fondo Europeo de Desarrollo Regional (European Union) for their technical and economic assistance (project AGR/15/FS/02). P. Catalá-Gregori is recipient of a research fellowship (AP2002-3340) from the Ministry of Education and Science of Spain.


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

  1. Dibner, J. J., and P. Buttin. 2002. Use of organic acid as a model to study the impact of gut microflora on nutrition and metabolism. J. Appl. Poult. Res. 11:453–463.[Abstract/Free Full Text]
  2. Taylor, D. J. 2001. Effects of antimicrobials and their alternatives. Br. Poult. Sci. 42(Suppl.):67–68.
  3. Griggs, J. P., and J. P. Jacob. 2005. Alternatives to antibiotics for organic poultry production. J. Appl. Poult. Res. 14:750–756.[Abstract/Free Full Text]
  4. Ratcliff, J. 2000. Antibiotic bans—A European perspective. Pages 135–152 in Proc. 47th Maryland Nutr. Conf. for Feed Manufacturers, Baltimore, MD. J. A. Doerr, ed. Univ. Maryland, College Park.
  5. Langhout, P. 2000. New additives for broiler chickens. World Poult. 16:22–27.
  6. Deans, S. G., and G. Ritchie. 1987. Antibacterial properties of plant essential oils. Int. J. Food Microbiol. 5:165–180.[CrossRef][Web of Science]
  7. Reddy, G. B. S., A. B. Melkhani, G. A. Kalyani, J. V. Rao, A. Shirwaikar, M. Kotian, R. Ramani, K. S. Aithal, A. L. Udupa, G. Bhat, and K. K. Srinivasan. 1991. Chemical and pharmacological investigations of Limnophila conferta and Limnophila heterophylla. Int. J. Pharmacognosy 29:145–153.
  8. Cowan, M. M. 1999. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12:564–582.[Abstract/Free Full Text]
  9. Hammer, K. A., C. F. Carson, and T. V. Riley. 1999. Antimicrobial activity of essential oils and other plants extracts. J. Appl. Microbiol. 86:985–990.[CrossRef][Medline]
  10. Botsoglou, N. A., P. Florou-Paneri, E. Christaki, D. J. Fletouris, and A. B. Spais. 2002. Effects of dietary oregano essential oil on performance of chickens and on iron-induced lipid oxidation of breast, thigh and abdominal fat tissues. Br. Poult. Sci. 43:223–230.[CrossRef][Web of Science][Medline]
  11. Turner, J. L., P. S. S. Dritz, and J. E. Minton. 2001. Review: Alternatives to conventional antimicrobials in swine diets. Prof. Anim. Sci. 17:217–226.[Abstract/Free Full Text]
  12. Maxus, Elanco Animal Health Ltd., Madrid, Spain.
  13. Amasil 85%, BASF Aktiengesellschaft, Ludwigshafen, Germany.
  14. Xtract, Axiss, Archamps, France.
  15. Labiatae extract, Furfural Español, Murcia, Spain.
  16. Food Chemicals Codex grade, Celite Corp., Lompar, CA.
  17. Scott, T. A., and F. Boldaji. 1997. Comparison of inert markers (chromic oxide or insoluble ash (Celite®) for determining apparent metabolizable energy of wheat or barley-based broiler diets with or without enzymes. Poult. Sci. 76:594–598.[Abstract/Free Full Text]
  18. NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. Natl. Acad. Press, Washington, DC.
  19. de Blas, C., G. G. Mateos, and P. G. Rebollar. 2003. Tablas FEDNA de composición y valor nutritivo de alimentos para la fabricación de piensos compuestos. 2nd ed. Fundación Española para el Desarrollo de la Nutrición Animal, Madrid, Spain.
  20. Ross 308, Ross Breeders Peninsular S. A., Riells del Fai, Spain.
  21. Paracox-5, Schering-Plough S.A., Madrid, Spain.
  22. BOE. 2005. Real Decreto Español 1201/2005, de 10 de octubre, sobre protección de los animales utilizados para experimentación y otros fines científicos. Bol. Ofic. Estado 252:34367–34391.
  23. MIP 4 Advanced Version 4.55, Microm Spain, S.A., Barcelona, Spain.
  24. AOAC. 1990. Method 984.13 in Official Methods of Analysis. 15th ed. Assoc. Offic. Anal. Chem., Washington, DC.
  25. Vogtmann, H., H. P. Pfirter, and A. L. Prabucki. 1975. A new method of determining metabolizability of energy and digestibility of fatty acids in broiler diets. Br. Poult. Sci. 16:531–534.[Web of Science][Medline]
  26. Association Française de Normalisation. 1997. Enzymatic Method NF V18-121 (Status: Certified Standard) in Animal Feedingstuffs. Determination of Starch Content. Assoc. Française de Normalisation, Paris, France.
  27. SPSS. 1997. SPSS Base 7.5 for Windows. SPSS, Chicago, IL.
  28. Elwinger, K., G. Daube, J. Hommez, and F. Haesebrouck. 1993. In vitro susceptibility of Clostridium perfringens isolated from farm animals to growth-enhancing antibiotics. J. Appl. Bacteriol. 75:55–57.[Medline]
  29. Runho, R. C., N. K. Sakomura, S. Kuana, D. Banzatto, and O. M. Junqueira. 1997. Uso do ácido orgânico (ácido fumárico) nas raçoes de frangos de corte. R. Bras. Zootec. 26:1183–1191.
  30. Hernández, F., V. García, J. Madrid, J. Orengo, and P. Catalá. 2006. Effect of formic acid on performance, digestibility, intestinal histomorphology and plasma metabolite levels of broiler chickens. Br. Poult. Sci. 47:50–56.[CrossRef][Web of Science][Medline]
  31. Bedford, M. 2000. Removal of antibiotic growth promoters from poultry diets: Implications and strategies to minimise subsequent problems. World’s Poult. Sci. J. 56:347–365.[CrossRef][Web of Science]
  32. Dibner, J. J., and J. D. Richards. 2005. Antibiotic growth promoters in agriculture: History and mode of action. Poult. Sci. 84:634–643.[Abstract/Free Full Text]
  33. Lee, K.-W., H. Everts, H. J. Kappert, K.-H. Yeom, and A. C. Beynen. 2003. Dietary carvacrol lowers body weight gain but improves feed conversion in female broiler chickens. J. Appl. Poult. Res. 12:394–399.[Abstract/Free Full Text]
  34. García, A. R., A. B. Batal, and N. M. Dale. 2007. A comparison of methods to determine amino acid digestibility of feed ingredients for chickens. Poult. Sci. 86:94–101.[Abstract/Free Full Text]
  35. Scott, T. A., and F. Boldaji. 1997. Comparison of inert markers [chromic oxide or insoluble ash (CeliteTM)] for determining apparent metabolizable energy of wheat- or barley-based broiler diets with or without enzymes. Poult. Sci. 76:594–598.[Abstract/Free Full Text]
  36. Jukes, T. H. 1977. The history of the "antibiotic growth effect". Fed. Proc. 37:2514–2518.
  37. Huang, R. L., Y. L. Yin, G. Y. Wu, Y. G. Zhang, T. J. Li, L. L. Li, M. X. Li, Z. R. Tang, J. Zhang, B. Wang, J. H. He, and X. Z. Nie. 2005. Effect of dietary oligochitosan supplementation on ileal digestibility of nutrients and performance of broilers. Poult. Sci. 84:1383–1388.[Abstract/Free Full Text]
  38. Jamroz, D., M. Kirchgessner, A. Wiliczkiewicz, J. Orda, and J. Skorupinska. 1995. Effect of application avilamycin (Maxus) and different levels of crude protein in concentrate mixtures on the nitrogen excretion and retention and on the apparent digestibility of amino acids in broiler chickens. Arch. Geflügelkd. 59:152–157.
  39. Doyle, M. E. 2001. Alternatives to antibiotic use for growth promotion in animal husbandry. Food Res. Inst. Briefings. Univ. Wisconsin, Madison.
  40. Mellor, S. 2000. Antibiotics are not the only growth promoters. World Poult. 16:14–15.
  41. Mellor, S. 2000. Nutraceuticals—Alternatives to antibiotics. World Poult. 16:30–33.
  42. Hernández, F., J. Madrid, V. García, J. Orengo, and M. D. Megías. 2004. Influence of two plant extracts on broilers performance, digestibility and digestive organ size. Poult. Sci. 83:169–174.[Abstract/Free Full Text]
  43. Montagne, L., J. R. Pluske, and D. J. Hampson. 2003. A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Anim. Feed Sci. Technol. 108:95–117.[CrossRef]
  44. Xu, Z. R., C. H. Hu, M. S. Xia, X. A. Zhan, and M. Q. Wang. 2003. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult. Sci. 82:648–654.[Abstract/Free Full Text]
  45. Scheppach, W., H. P. Bartram, and F. Richter. 1995. Role of short-chain fatty acids in the prevention of colorectal cancer. Eur. J. Cancer 31A:1077–1080.[CrossRef]
  46. Frankel, W. L., W. Zhang, A. Singh, D. M. Klurfeld, S. Don, T. Sakata, and J. L. Rombeau. 1994. Mediation of the trophic effects of short chain fatty acids on the rat jejunum and colon. Gastroenterology 106:385–390.
  47. Leeson, S., H. Namkung, M. Antongiovanni, and E. H. Lee. 2005. Effect of butyric acid on the performance and carcass yield of broiler chickens. Poult. Sci. 84:1418–1422.[Abstract/Free Full Text]
  48. Visek, W. J. 1978. The mode of growth promotion by antibiotics. J. Anim. Sci. 46:1447–1469.[Abstract/Free Full Text]
  49. Skrede, G., O. Herstad, S. Sahistrom, A. Holck, E. Slinde, and A. Skrede. 2003. Effects of lactic acid fermentation on wheat and barley carbohydrate composition and production performance in the chicken. Anim. Feed Sci. Technol. 105:135–148.[CrossRef]



This article has been cited by other articles:


Home page
 J. Appl. Poult. Res.Home page
J. P. Wang, J. S. Yoo, J. H. Lee, T. X. Zhou, H. D. Jang, H. J. Kim, and I. H. Kim
Effects of phenyllactic acid on production performance, egg quality parameters, and blood characteristics in laying hens
J. Appl. Poult. Res., January 1, 2009; 18(2): 203 - 209.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Summary Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (2)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by García, V.
Right arrow Articles by Madrid, J.
Right arrow Search for Related Content
PubMed
Right arrow Articles by García, V.
Right arrow Articles by Madrid, J.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS