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The Journal of Poultry Science logoLink to The Journal of Poultry Science
. 2016 Apr 25;53(2):128–135. doi: 10.2141/jpsa.0150077

Effects of Flavomycin, Bacillus licheniformis and Enramycin on Performance, Nutrient Digestibility, Gut Morphology and the Intestinal Microflora of Broilers

Hong L Wang 1, Meng Shi 1, Xiao Xu 1, Long Pan 1, Pan F Zhao 1, Xiao K Ma 1, Qi Y Tian 1, Xiang S Piao 1,✉
PMCID: PMC7477275  PMID: 32908375

Abstract

The effects of Flavomycin, Bacillus licheniformis and Enramycin on broiler performance, nutrient digestibility, gut morphology and the intestinal microflora were studied in a 42-d experiment. A total of 288, one-day-old, male, Arbor Acres broilers were randomly assigned to 1 of 4 dietary treatments with 12 pens per treatment and 6 birds per pen. The treatments were comprised of a control diet without supplementation, a diet supplemented with 5 ppm Flavomycin, a diet supplemented with the combination of 5 ppm Flavomycin and 1.35 × 109 CFU/kg Bacillus licheniformis, as well as a diet supplemented with 5 ppm Enramycin. The average daily gain (ADG) and feed conversion ratio (FCR) of birds fed the diet with Flavomycin combined with Bacillus licheniformis and the Enramycin diet were improved (P<0.05) compared with the control diet. The digestibility of dry matter, energy, and calcium for birds fed the combination of Flavomycin and Bacillus licheniformis and the Enramycin diet were also enhanced compared with the control diet. All additives improved the villus height and crypt depth in the duodenum, jejunum and ileum on d 21. In addition, reduced numbers of cecal E. coli (P<0.01) were found in birds fed all three supplemented diets on d 42. In conclusion, supplementation with Flavomycin and Bacillus licheniformis in combination or Enramycin would appear to be superior to supplementation with Flavomycin alone. All three supplemented diets were superior to the control.

Keywords: broilers, gut morphology, intestinal microbes, nutrient digestibility, performance

Introduction

Antibiotics are commonly used as feed additives to improve the health and performance of livestock as well as for therapeutic and prophylactic purposes (Jones and Ricket, 2003). The introduction of these agents coincided with the introduction of intensive animal rearing (Butaye et al., 2003). Antibiotics stabilize the bacterial population present in the digestive tract resulting in improved performance and reduced morbidity and mortality due to clinical and subclinical diseases (Miles et al., 2006).

Flavomycin, also known as moenomycin or bambermycin, is a fermentation product of Streptomyces ghaenaensis (Kling et al., 1976; Moeller et al., 1976; Ni et al., 2012). It is a phosphorus-containing glycolipid and is non-absorbable (Wasiliewski et al., 1965). It inhibits peptidoglycan synthesis by inhibiting peptidoglycan polymerases through impairment of the trans-glycolase activities of penicillin-binding proteins (Van et al., 1987). Flavomycin enhances the normal avian gut flora instead of disrupting it (Humbert et al., 1991; Manning et al., 1994). Its supplementation in broiler diets has been shown to improve weight gain and feed conversion without altering the predominant species of microorganisms present in the gastrointestinal tract (Evangelisti et al., 1975). Flavomycin also increases the villus height and decreases the crypt depth to enhance the efficiency of nutrient absorption (Markovic et al., 2009; Ni et al., 2012).

Bacillus licheniformis, a gram-positive bacterium, is classified as a ‘Generally Recognized as Safe” (GRAS) microorganism by the United States Food and Drug Administration (Wang et al., 2004). Bacillus have been suggested to have probiotic effects (Sanders et al., 2003). The microbial populations in the gastrointestinal tract of poultry play a key role in the normal digestive processes and in maintaining animal health. In piglets, ingestion of Bacillus licheniformis spores has been shown to increase growth, feed conversion, and meat quality (Kyriakis et al., 1999; Alexopoulos et al., 2004).

Enramycin is a linear-ring, peptide antibiotic produced by Streptomyces fungicidicus and was first isolated in 1967 (Higashiide et al., 1968). It consists of two major components namely Enramycin-A (C107 H138 N26 O31 Cl2) and Enramycin-B (C106 H140 N26 O31 C12). It inhibits gram-positive bacteria such as Clostridiumand Streptoccocus by destroying bacterial cell walls (EI-Husseiny et al., 2008). It is highly stable, both in dry formand in aqueous solution, over a pH range of 3.5 to 7.5 (Inoue et al., 2010).

Enramycin is regularly used in the animal feed industry as an antibiotic. Both Kamran et al. (2013) and EI-Husseiny et al. (2008) have shown that diets supplemented with Enramycin (120 g/ton feed) significantly increased weight gain, feed intake and feed conversion of broilers. Emramycin inclusion in feed also decreased the numbers of E. coli in the intestinal tract (Amaechi and Iheanetu, 2014).

Flavo combi® (Huvepharma N. V. Antwerp, Belgium) is a commercial product which contains both Flavomycin and Bacillus licheniformis. Athough Flavomycin and Bacillus licheniformis have been fed separately to broilers, there are no reports in the literature of these additives being fed in combination. It is not known if they provide any synergistic effects. The objective of the present study was to determine whether the effects of this combination are superior to Flavomycin fed alone. In addition, an attempt was made to compare the effects of these products on the performance, nutrient digestibility, gut morphometric indices and the intestinal microflora of broilers fed diets containing Enramycin.

Materials and Methods

Bird Husbandry

One-day-old, male, Arbor Acres broiler chicks were obtained from the Beijing Arbor Acres Poultry Breeding Company (Beijing, China). The broiler chicks were housed in wire-floored cages (90 × 60 × 40 cm3) and raised under environmentally controlled conditions in which the temperature was gradually decreased from 33 to 24°C by reducing the temperature 3°C a week for the first 3 weeks. The temperature was then maintained at 24°C until the end of the experiment. The mean relative humidity was set at 45 to 55% and was kept within this range. Supplemental lighting was provided on a continuous basis. All birds were provided feed and water ad libitum. All procedures were approved by the Animal Care and Use Committee of China Agricultural University (Beijing, China).

Experimental Products

The Flavo Combi® used in this experiment is a complex product with a content of 40 g Flavomycin and 1.08 × 1013 CFU Bacillus licheniformis per kg. The concentrations of Flavomycin and Enramycin in the other products were both 80 g/kg. All three products were provided by Huvepharma N. V. (Antwerp, Belgium).

Diets and Experimental Design

A total of 288, one-day-old, male, Arbor Acres broilers were randomly assigned to 1 of 4 dietary treatments with 12 pens per treatment and 6 birds per pen. The treatments comprised of a control diet without supplementation, a diet supplemented with 5 ppm Flavomycin, a diet supplemented with the combination of 5 ppm Flavomycin and 1.35 × 109 CFU/kg Bacillus licheniformis as well as a diet supplemented with 5 ppm Enramycin. All diets were formulated to meet the nutritional levels for broiler chickens recommended by the National Research Council (1994). The birds were fed starter diets from d 0 to 21 and grower diets from d 22 to 42. The composition of the experimental diets is listed in Table 1.

Table 1. Composition of basal diets and nutrient levels.

Starter phase (d 0–21) Grower phase (d 22–42)
Ingredient (% as-fed)
  Corn 56.60 60.40
  Soybean meal 33.12 29.30
  Soybean oil 1.95 3.07
  Fish meal 4.50 3.56
  Dicalciumphosphate 1.00 1.05
  Limestone 1.48 1.32
  Salt 0.25 0.25
  DL-methionine (98%) 0.10 0.05
  Premix1 1.00 1.00
Nutritional content2 (% as fed)
  Crude protein 23.32 20.40
  Calcium 1.02 0.92
  Total phosphorus 0.69 0.64
  Lysine 1.36 1.14
  Threonine 0.90 0.80
  Tryptophan 0.26 0.22
  Methionine + cysteine 0.82 0.74
  ME, (MJ/kg) 13.02 12.96
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1

Premix supplied per kg diet: vitamin A, 11,000 IU; vitamin D, 3,025 IU; vitamin E, 22 mg; vitamin K3, 2.2 mg; thiamine, 1.65 mg; riboflavin, 6.6 mg; pyridoxine, 3.3 mg; cobalamin, 17.6 µg; nicotinic acid, 22 mg; pantothenic acid, 13.2 mg; folic acid, 0.33 mg; biotin, 88 µg; choline chloride, 500 mg; iron, 48 mg; zinc, 96.6 mg; manganese, 101.76 mg; copper, 10 mg; selenium, 0.05 mg; iodine, 0.96 mg; cobalt, 0.3 mg.

2

Analyzed values except for ME.

Sample Collection and Laboratory Analysis

All birds were weighed individually after their arrival from the hatchery. The birds were also weighed on d 21 and 42 after a 12 h fast. Feed bags were weighed at the same time and these values were used to calculate average daily gain (ADG), average daily feed intake (ADFI) and feed conversion ratio (FCR).

On d 19 and 40, all feed and excreta were removed from the feeders and collection trays. A weighed amount of feed was then added to the feeders in sufficient quantity that the feeders would not run out of feed during the 3 d collection period. The amount of feed consumed by birds in each pen during these three days was measured, and all excreta from each pen was collected and then feathers and spilled feed were removed and the excreta weighed. A 500 gram sample of excreta was removed and dried at 60°C for 72 h. Feed and dried excreta samples were subsequently ground to pass through a 40-mesh screen and thoroughly mixed before analyses.

The dry matter, crude protein, calcium, and phosphorus content of the diets were determined according to the methods of the Association of Official Analytical Chemists (AOAC, 1990) whereas the gross energy content was measured with an Isoperibol Bomb Calorimeter (Model 1281, Parr, Moline, IL, USA). Feed samples were hydrolyzed with 6 N HCl for 24 h at 110°C (AOAC Method 999. 13) and subsequently analyzed for their amino acid (AA) content using an AA Analyzer (Hitachi L-8900, Tokyo, Japan). Methionine and cystine were determined as methionine sulfone and cysteic acid after cold performic acid oxidation overnight and hydrolyzed with 7.5 N HCl for 24 h at 110°C (AOAC Method 994.12). Tryptophan was determined after LiOH hydrolysis for 22 h at 110°C (AOAC Method 998.15) using High Performance Liquid Chromatography (Agilent 1200 Series, Santa Clara, CA, USA).

One bird per cage was randomly selected and slaughtered on d 21 and 42. Immediately after euthanasia, a 2-cm sample of the duodenum (taken at the midpoint of the duodenum), the jejunum (midway between the entrance to the bile duct and Meckel's diverticulum) and the ileum (at the distal end of the lower ileum) were aseptically isolated, flushed with 0.9% salt solution, fixed with 10% formaldehyde-phosphate buffer and kept at 4°C for microscopic assessment of mucosa morphology. A portion of the cecum containing digesta was cut away and both ends were tied with a cotton thread. The tied off ceca were packed and then frozen by immersion in liquid nitrogen and stored at −80°C until analysis.

Villus height and crypt depth were measured according to Li et al. (1990) with some modifications. In brief, fixed intestinal samples were prepared using conventional paraffin embedding techniques. Samples were sectioned at a thickness of 5 µm and then placed on a glass slide and stained with hematoxylin and eosin. Villus height and crypt depth were measured under 10 times magnification using an Olympus CK 40 microscope (Olympus Optical Company, Shenzhen, China). The villus height and crypt depth was measured in triplicate for each bird.

Cecal numbers of Lactobacillus and E. coli were determined according to the method of Mikkelsen et al. (2003) with some modifications. In brief, the frozen cecal samples were transferred to an incubator at 4°C for 10 h of incubation. Thereafter, 1 g of digesta was serially diluted 10 fold with sterile physiological saline resulting in dilutions ranging from 10−1 to 10−7. E. coli were cultivated on MacConkey agar (Beijing Haidian Microbiological Culture Factory, Beijing, China), while Lactobacillus were cultured on DeMan Rogosa-Sharpe media (Beijing Haidian Microbiological Culture Factory, Beijing, China). Each dilution was determined in triplicate and the average of 3 replicates was recorded. Lactobacillus and E. coli were cultured in disposable culture dishes. All dishes were incubated at 37°C for 24 h. The microbial enumerations in the digesta are expressed as log10 CFU per gram. Bacteria were enumerated by a visual count of colonies using the best replicated set from dilutions that resulted in 30 to 300 colonies per dish.

Statistical Analysis

Analysis of variance was conducted for a randomized block design using the General Lineal Model (GLM) procedures of the Statistical Analysis System Institute (Cary, NC). Statistical significance was declared at P<0.05. If significant effects were found, individual means were compared using Tukey's Multiple Range Test. Values in the tables are means and pooled S.E.M.

Results

Broiler Performance

From d 0 to 21, there were no differences in the performance of birds fed the diets supplemented with any of the growth promoters compared with the control diet. From d 22 to 42, the FCR for birds fed the diets supplemented with Flavomycin and Bacillus licheniformis or Enramycin were improved in comparison with the control and Flavomycin diets. From d 0 to 42, the ADG of birds fed all three supplemented diets was improved compared with the control while the FCR of birds fed the combination of Flavomycin and Bacillus licheniformis or the Enramycin diet was improved compared with that of birds fed Flavomycin alone or the control.

Nutrient Digestibility

The effect of the dietary additives on the apparent digestibility of dry matter, energy, crude protein, calcium and phosphorous are shown in Table 3. From d 19 to 21, the digestibility of dry matter, energy and calcium in broilers fed the combination of Flavomycin and Bacillus licheniformis diet or the Enramycin diet were greater (P<0.05) than for birds fed the control diet. The digestibility of phosphorous for birds fed the Enramycin treatment was significantly higher (P<0.05) than for birds fed the other three diets. Values for birds fed Flavomycin alone were intermediate to those of birds fed the combination of Flavomycin and Bacillus licheniformis or Enramycin and the control diet.

Table 2. Effects of dietary Flavomycin, Bacillus licheniformis and Enramycin supplementation on broiler performance.

Control FLV FLC ENR SEM P-value
0–21 days
  ADG, g 34.4 35.5 35.4 35.6 0.50 0.23
  ADFI, g 41.5 42.0 41.9 42.2 0.73 0.92
  FCR 1.21 1.18 1.18 1.18 0.01 0.47
22–42 days
  ADG, g 79.6 82.3 82.0 81.9 1.46 0.52
  ADFI, g 145.8 146.0 138.8 140.0 2.49 0.09
FCR 1.83a 1.78a 1.70b 1.71b 0.03 0.03
0–42 days
  ADG, g 56.6b 59.0a 59.3a 59.2a 0.79 0.04
  ADFI, g 93.4 94.2 90.8 90.7 1.27 0.22
  FCR 1.65a 1.60a 1.53b 1.54b 0.02 <0.01
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Control: basal diet; FLV: basal diet+5 ppm Flavomycin; FLC: basal diet+5 ppm Flavomycin+1.35×109 CFU/kg Bacillus licheniformis; ENR: basal diet+5 ppm Enramycin.

a, b

Means in the same row with different superscripts differ (P<0.05).

Table 3. Effect of dietary Flavomycin, Bacillus licheniformis and Enramycin supplementation on nutrient digestibility of broilers.

Control FLV FLC ENR SEM P-value
Day 19 to 21
  Dry matter 0.68c 0.70bc 0.71b 0.73a 0.01 <0.01
  Energy 0.74c 0.75bc 0.76ab 0.77a 0.01 <0.01
  Crude protein 0.73 0.74 0.74 0.75 0.01 0.19
  Calcium 0.38c 0.40bc 0.43ab 0.45a 0.01 <0.01
  Phosphorous 0.50b 0.52b 0.53b 0.56a 0.01 <0.01
Day 40 to 42
  Dry matter 0.70c 0.73b 0.77a 0.74b 0.01 <0.01
  Energy 0.76b 0.79a 0.81a 0.79a 0.01 <0.01
  Crude protein 0.50c 0.56b 0.66a 0.57b 0.02 <0.01
  Calcium 0.36b 0.37b 0.49a 0.44a 0.02 <0.01
  Phosphorous 0.74b 0.77b 0.83a 0.81a 0.01 <0.01
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Control: basal diet; FLV: basal diet+5 ppm Flavomycin; FLC: basal diet+5 ppm Flavomycin+1.35×109 CFU/kg Bacillus licheniformis; ENR: basal diet+5 ppm Enramycin.

a–c

Means in the same row with different superscripts differ (P<0.05).

From d 40 to 42, the digestibility of dry matter, energy and crude protein in birds fed the Flavomycin, Flavomycin and Bacillus licheniformis or Enramycin diets were significantly improved (P<0.05) compared with the control diet. The digestibility of calcium and phosphorous for birds fed the Flavomycin and Bacillus licheniformis or Enramycin diets were significantly (P<0.05) higher than for birds fed the control diet. The digestibility of all nutrients for birds the Flavomycin and Bacillus licheniformis treatment were significantly higher (P<0.05) than for birds fed Flavomycin alone with the exception of energy.

Small Intestinal Morphology

The data displayed in Table 4 shows the effects of the dietary additives on the small intestinal morphology of broiler chickens on d 21. All diets supplemented with growth promoters significantly (P<0.05) increased the villus height, and the villus:crypt ratio while decreasing the crypt depth in the duodenum, jejunum and ileumin comparison with birds fed the control diet.

Table 4. Effect of dietary Flavomycin, Bacillus licheniformis and Enramycin supplementation on the small intestinal morphology of broilers (d 21).

Control FLV FLC ENR SEM P-value
Duodenum (µm)
  Villus height 1626b 1752a 1764a 1765a 12.16 <0.01
  Crypt depth 225a 210b 208b 207b 3.13 <0.01
  Villus: Crypt ratio 7b 8a 8a 8a 0.09 <0.01
Jejunum (µm)
  Villus height 987b 1042a 1045a 1045a 9.46 <0.01
  Crypt depth 188a 173b 165b 163b 4.34 <0.01
  Villus: Crypt ratio 5b 6a 6a 6a 0.15 <0.01
Ileum (µm)
  Villus height 786b 820a 829a 834a 8.50 <0.01
  Crypt depth 166a 151b 145b 144b 3.59 <0.01
  Villus: Crypt ratio 4b 5a 5a 6a 0.14 <0.01
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Control: basal diet; FLV: basal diet+5 ppm Flavomycin; FLC: basal diet+5 ppm Flavomycin+1.35×109 CFU/kg Bacillus licheniformis; ENR: basal diet+5 ppm Enramycin.

a, b

Means in the same row with different superscripts differ (P<0.05).

Table 5 shows the effects of the dietary additives on the small intestinal morphology of the broilers on d 42. There was no significant difference in the gut morphology in the duodenum (P>0.05) for any treatment. However, the villus height in the jejunum and ileumin birds fed the combination of Flavomycin and Bacillus licheniformis diet or the Enramycin diet was both improved (P<0.05) compared with birds fed the control diet.

Table 5. Effect of dietary Flavomycin, Bacillus licheniformis and Enramycin supplementation on the small intestinal morphology of broilers (d 42).

Control FLV FLC ENR SEM P-value
Duodenum (µm)
  Villus height 1925  1948   1955  1960  26.28 0.32
  Crypt depth 318  307   310  306  7.89 0.72
  Villus: Crypt ratio 6  7   6  6  0.18 0.32
Jejunum (µm)
  Villus height 1367b 1388ab 1403a 1403a 7.83 0.02
  Crypt depth 196  187   175  173  8.19 0.22
  Villus: Crypt ratio 7  8   8  8  0.32 0.08
Ileum (µm)
  Villus height 1186b 1226a  1238a 1243a 8.18 <0.01
  Crypt depth 188  178  171  170  8.17 0.41
  Villus: Crypt ratio 6  7   7  7  0.28 0.09
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Control: basal diet; FLV: basal diet+5 ppm Flavomycin; FLC: basal diet+5 ppm Flavomycin+1.35× 109 CFU/kg Bacillus licheniformis; ENR: basal diet+5 ppm Enramycin.

a, b

Means in the same row with different superscripts differ (P<0.05).

Microbial Populations in the Cecal Digesta

The effect of the dietary additives on the intestinal microflora of broiler chickens is shown in Table 6. The Lactobacillus colony forming units in the ceca of birds fed the Enramycin diet were significantly (P<0.05) lower than for birds fed the control diet, the Flavomycin diet or the Flavomycin combined with Bacillus licheniformis diet on d 21 (P=0.02) and d 42 (P<0.01), while no differences were found between birds fed the Flavomycin diet and the Flavomycin and Bacillus licheniformis diet compared with the control diet. E. coli numbers in the cecum of birds fed the Flavomycin, Flavomycin and Bacillus licheniformis or Enramycin diets tended to be lower (P=0.09) in comparison with the control diet during the starter period while they were significantly decreased (P<0.01) during the grower period.

Table 6. Effect of dietary Flavomycin, Bacillus licheniformis and Enramycin supplementation on the cecal microflora of broilers (log10 CFU g−1 digesta).

Control FLV FLC ENR SEM P-value
Day 21
  Lactobacillus 8.57a 8.3a 8.14a 7.25b 0.26 0.02
  E. coli 7.14 6.60 5.94 5.82 0.38 0.09
Day 42
  Lactobacillus 8.16a 7.83a 7.55a 6.48b 0.27 <0.01
  E. coli 5.57a 5.05b 4.98b 4.18c 0.17 <0.01
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Control: basal diet; FLV: basal diet+5 ppm Flavomycin; FLC: basal diet+5 ppm Flavomycin+1.35× 109 CFU/kg Bacillus licheniformis; ENR: basal diet+5 ppm Enramycin.

a–c

Means in the same row with different superscripts differ (P<0.05).

Discussion

In the present study, no differences were found in ADG during either the starter or grower phases but differences were observed over the entire experimental period. During the grower phase and over the entire experimental period, only the FCR in birds fed the combination of Flavomycin and Bacillus licheniformis or the Enramycin diet was improved indicating that Flavomycin combined with Bacillus licheniformis and Enramycin has a greater effect on broiler performance than Flavomycin fed alone. The lack of a response in ADG and ADFI is consistent with previous findings for broiler chickens or turkeys (Mohamed et al., 2008; Haque et al., 2010; Wasilewska et al., 2010).

There is an abundance of data in the scientific literature on the benefits of antibiotics in improving the growth and health of poultry. For example, Hooge et al. (2003) showed that the addition of bacitracin methylene disalicylate followed by virginiamycin to broiler diets increased body weight compared with a negative control. Diets supplemented with Flavomycin and Enramycin have also been shown to improve the feed conversion of broiler chickens and turkeys (Esteive et al., 1997; Parks et al., 2001; Kamran et al., 2013).

The digestibility of most nutrients in birds fed the combination of Flavomycin and Bacillus licheniformis or Enramycin diets was enhanced compared with the control. Nutrient digestibility was also improved in birds fed Flavomycin alone but this improvement in digestibility was not reflected in improved performance in the current experiment. Similar results were reported by Haque et al. (2010).

For young chicks, a longer villus increases the absorptive surface of the intestines, while shorter crypt depths indicate lower tissue turnover as well as a lower demand for tissue development (Khodambashi et al., 2012). In the starter period, additive inclusion increased the villus height and reduced the crypt depth and thus increased nutrient digestibility compared with the control, which was also demonstrated by Baurhoo et al. (2007) and Parsaie et al. (2007). During the grower phase, broilers fed diets supplemented with Flavomycin or Enramycin showed no improvement in gut morphology in comparison with the control diet with the exception of an increase in villus height in the jejunum and ileum. This result is in accordance with the study of Gunal et al. (2006) and may be explained by the fact that an increase in age may reduce the beneficial effects of these growth promoters.

Enterocytes undergo a continued cycle of proliferation in the intestinal crypt, cell maturation and migration up the villus with desquamation at the tip of the villus. The depth of the crypts is correlated with cell replacement rate (Savage et al., 1997). Accelerated replacement of enterocytes requires energy and proteins and the diversion of these nutrients can reduce the growth rate of broilers as well as the development of other tissues and organ systems (Markovicva et al., 2009). The gastrointestinal tract is the front line of defense against the constant invasion of microbes (Markovicva et al., 2009). The makeup of the gastrointestinal fauna of the bird is an important factor in improving poultry performance and flock health (Markovicva et al., 2009). In the current experiment, birds fed diets containing the feed additives showed significant reductions in the abundance of E. coli during the grower phase but not during the starter phase. This result may be explained by changes in the environment (i.e. a build up of manure over time) and possible cumulative effects of feed additive inclusion. When the birds were young, pathogens were rarely seen so the effect of antibiotic inclusion may be limited during this period. This conclusion is in close agreement with previous research (Kling et al., 1976; Jang et al., 2007; Hassan et al., 2010; Amaechi et al., 2014).

Of potential concern is the fact that Lactobacillus numbers were decreased in birds fed the Enramycin diet. This finding was also made by Butaye et al., (2003) and Brenes et al., (1989). Lactobacillus are generally considered to be beneficial bacteria which compete with pathogens in order to reduce their number in the gastrointestinal tract. However, the performance of birds fed the Enramycin diet was still improved relative to the control suggesting that the reduction in Lactobacillus was not sufficient to negatively affect broiler performance.

On the basis of the overall results of this experiment, supplementation with Flavomycin and Bacillus licheniformis and Enramycin would appear to be superior to supplementation with Flavomycin alone while all three additives were superior to the control. Therefore, given a choice, poultry producers should use these additives in preference to no additives or Flavomycin alone.

Acknowledgments

Financial support was received from Huvepharm a N. V. (Antwerp, Belgium) and the National Natural Science Foundation of China (No. 31372316).

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