Open Access

Alternatives to antibiotics as growth promoters for use in swine production: a review

Journal of Animal Science and Biotechnology20134:35

https://doi.org/10.1186/2049-1891-4-35

Received: 3 July 2013

Accepted: 12 September 2013

Published: 14 September 2013

Abstract

In the past two decades, an intensive amount of research has been focused on the development of alternatives to antibiotics to maintain swine health and performance. The most widely researched alternatives include probiotics, prebiotics, acidifiers, plant extracts and neutraceuticals such as copper and zinc. Since these additives have been more than adequately covered in previous reviews, the focus of this review will be on less traditional alternatives. The potential of antimicrobial peptides, clay minerals, egg yolk antibodies, essential oils, eucalyptus oil-medium chain fatty acids, rare earth elements and recombinant enzymes are discussed. Based on a thorough review of the literature, it is evident that a long and growing list of compounds exist which have been tested for their ability to replace antibiotics as feed additives in diets fed to swine. Unfortunately, the vast majority of these compounds produce inconsistent results and rarely equal antibiotics in their effectiveness. Therefore, it would appear that research is still needed in this area and that the perfect alternative to antibiotics does not yet exist.

Keywords

Antimicrobial peptides Clay minerals Egg yolk antibodies Essential oils Eucalyptus oil-medium chain fatty acids Rare earth elements Recombinant enzymes

Background

Antibiotics have played a major role in the growth and development of the swine industry for more than 50 years. Their efficiency in increasing growth rate, improving feed utilization and reducing mortality from clinical disease is well documented [1]. However, consumers are becoming increasingly concerned about drug residues in meat products [2]. In addition, it has been suggested that the continuous use of antibiotics may contribute to a reservoir of drug-resistant bacteria which may be capable of transferring their resistance to pathogenic bacteria in both animals and humans [3]. As a result, many countries have banned or are banning the inclusion of antibiotics in swine diets as a routine means of growth promotion.

In the past two decades, an intensive amount of research has been focused on the development of alternatives to antibiotics to maintain swine health and performance and many excellent reviews have already been published on this subject. The most widely researched alternatives include probiotics [46], prebiotics [4, 7], enzymes [810], acidifiers [1114], plant extracts [4, 15, 16] and neutraceuticals such as copper and zinc [17, 18]. Since these additives have been more than adequately covered, the focus of this review will be on less traditional alternatives.

Antimicrobial peptides

Antimicrobial peptides, as the name implies, are peptides with antimicrobial properties. They have been isolated and characterized from virtually all living organisms ranging from prokaryotes to humans [19]. They are important components of the host’s defense system and are effector molecules of innate immunity with direct antimicrobial and mediator function [20]. Most antimicrobial peptides contain between 30 and 60 amino acids and are polar molecules with spatically separated hydrophobic and charged regions. Antimicrobial peptides have been identified that have activity against Gram-positive and Gram-negative bacteria as well as against fungi and enveloped viruses [20].

More than 700 antimicrobial peptides are known to exist [20]. Bioscreening, cloning strategies and computer-based database searches have been used to identify antimicrobial peptides which have potential to be used as alternatives to antibiotics [20]. Once identified, it is possible to chemically synthesize most antimicrobial peptides but the high cost of this process precludes the production of peptides through this method for use as feed additives. However, several research groups have developed recombinant systems for expression of antimicrobial peptides.

Antimicrobial proteins produced by bacteria are called bacteriosins. These proteins have several characteristics that make them desirable alternatives to conventional antibiotics for use in swine production. Most importantly, bacteria have difficulty in developing resistance against these peptides [21]. Peptides have a narrow spectrum of activity so they can be used to target specific pathogenic bacteria without affecting the normal native flora. There is almost no risk of residues in meat because they are proteins and therefore will not be absorbed as an intact molecule. In addition, antimicrobial peptides can tolerate a wide range of pH and temperatures [22].

The antimicrobial activity of peptides is based on several mechanisms. In most cases, interactions between the peptide and the surface membranes of the target bacteria are thought to be responsible for their killing activity [20]. These interactions are proposed to lead to a loss of membrane function including breakdown of membrane potential, leakage of metabolites and ions, and alteration of membrane permeability [19]. These alterations in the bacterial membrane can result in cell lysis or, alternatively, can lead to the formation of transient pores and the transport of peptides inside the cell bringing them into contact with intracellular targets. Other mechanisms of antimicrobial activity include the inhibition of protein and RNA synthesis [20].

To date, the most prevalent use of antimicrobial peptides has been in the preservation of foods and few studies have been conducted using antimicrobial peptides with swine. One promising research area has been in the use of the antimicrobial peptide colicin. Colicins are a class of bacteriocin produced by and effective against Escherichia coli (E. coli) and closely related species. They have been shown to be effective against many pathogenic E. coli strains including those responsible for post-weaning diarrhea and edema disease in pigs [23, 24].

A chemically synthesized antimicrobial peptide A3 has been shown to have beneficial effects on weanling pig performance, nutrient digestibility, intestinal morphology as well as intestinal and fecal microflora [25, 26]. In addition, an antimicrobial peptide isolated from the intestine of the Rongchang pig improved performance but had no effect on diarrhea incidence in weanling pigs [27]. However, the antimicrobial peptide appeared to act synergistically with zinc as the two additives in combination were superior to either additive fed separately.

The results of a feeding trial in which the antimicrobial peptide cecropin, originally isolated from the silkworm Hyalophora cecropia, was fed to weanling pigs challenged with enterotoxigenic E. coli K88 are shown in Table 1. Use of the antimicrobial peptide cecropin resulted in similar performance to pigs fed a combination of antibiotics [21]. The improvement in performance appeared to be related to improvements in nutrient digestibility and intestinal morphology. Cecropin treatment decreased total aerobes while increasing total anaerobes in the ileum compared with the control (Table 2). Cecropin also increased the numbers of beneficial lactobacillus in the cecum. Cecropin increased serum IgA and IgG and the inflammatory cytokines interleukin-1β and interleukin 6 indicating that cecropin activates both systemic and local immune systems in response to E. coli challenge.
Table 1

Effects of antibiotics or an antimicrobial peptide cecropin on the performance of four week old weaned pigs after challenge with E. coli as well as nutrient digestibility before challenge

Items

Control

Antibiotics1

Cecropin

SEM

P-value

Performance (day 13-19)

 Weight gain, g/d

312a

367b

358b

6.4

<0.01

 Feed intake, g/d

566

597

592

9.8

0.08

 Feed efficiency

0.55a

0.62b

0.61b

0.01

<0.01

 Diarrhea incidence, %

37.50

17.86

19.64

  

Nutrient digestibility

 Nitrogen retention, g/d

10.1a

11.5b

10.7ab

0.38

0.04

 Nitrogen digestibility, %

73.2

76.9

75.0

1.20

0.17

 Energy retention, MJ/kg/d)

2.5a

3.0b

2.8ab

0.13

0.04

 Energy digestibility, %

84.6

88.2

86.4

1.71

0.14

Wu et al. [21].

1Kitasamycin and colistin sulfate.

a,bWithin row, means followed by same or no letter do not differ (P>0.05).

Table 2

Effects of antibiotics or the antimicrobial peptide cecropin on intestinal morphology and intestinal microflora of four week old weaned pigs after challenge with E. coli

Items

Control

Antibiotic1

Cecropin

SEM

P-value

Intestinal Morphology

 Duodenum

 Villus height, μm

418

439

431

10.7

0.53

 Crypt depth, μm

233

227

232

5.3

0.41

 Villus height to crypt depth ratio

1.83

1.96

1.89

0.24

0.18

 Jejunum

 Villus height, μm

401

448

420

18.4

0.37

 Crypt depth, μm

212b

233a

220b

6.8

0.04

 Villus height to crypt depth ratio

1.89b

1.97a

1.91ab

0.01

0.03

 Ileum

 Villus height, μm

357b

396a

384a

12.4

0.04

 Crypt depth, μm

211

217

213

5.6

0.37

 Villus height to crypt depth ratio

1.74b

1.85a

1.82ab

0.04

0.04

Intestinal Microflora (log 10 CFU/g of digesta)

 Ileum

 E. coli

4.37

4.14

4.25

0.18

0.85

 Lactobacillus

9.38

10.00

9.62

0.20

0.42

 Total aerobes

6.69a

6.60ab

6.43b

0.08

0.04

 Total anaerobes

9.36b

9.87ab

10.12a

0.23

0.03

 Cecum

 E. coli

3.37a

3.09b

3.22ab

0.12

0.04

 Lactobacillus

8.89b

9.47a

9.23a

0.14

0.03

 Total aerobes

3.88

3.77

3.49

0.44

0.63

 Total anaerobes

8.79

9.37

9.26

0.28

0.38

Wu et al. [21].

1Kitasamycin and colistin sulfate.

a,bWithin row, means followed by same or no letter do not differ (P>0.05).

Although there is little research on these compounds, the use of antimicrobial peptides appears to have considerable potential as a replacement for antibiotics in rations fed to swine. A commercial entity (Beijing Longkefangzhou Biological Engineering Technology Company, Beijing, China) has started to market cecropin for use in swine rations in China.

Clay minerals

Clay minerals are formed by a net of stratified tetrahedral and octahedral layers [2]. They contain molecules of silicon, aluminum and oxygen. The natural extracted clays (bentonites, zeolite, kaolin) are a mixture of various clays differing in chemical composition. The best known are montmorillonite, smectite, illite, kaolinite, biotic and clinoptilolite [2].

Clays added to the diet can bind and immobilize toxic materials in the gastrointestinal tract of animals and thereby reduce their biological availability and toxicity [2]. Clay minerals can bind aflatoxins, plant metabolites, heavy metals, and toxins. The extent of adsorption is determined by the chemistry of the clay minerals, exchangeable ions, surface properties and the fine structure of the clay particles [2]. An important role is played by pH, dosage and exposure time. As a result of their binding properties, clays have been widely used in swine diets to improve pig performance when diets containing mycotoxins are fed [28, 29].

Clays have also been shown to prevent diarrhea in weaned pigs [2, 30, 31]. Based on this fact, several research groups have attempted to determine whether or not the inclusion of various clays in swine diets can improve pig performance. The results have been inconclusive with some trials demonstrating positive results particularly for younger pigs [30], but the vast majority of the experiments have failed to show improvements [3235]. It would appear that clay minerals are not viable alternatives to antibiotics as growth promoters.

Egg yolk antibodies

One technique that appears to have considerable potential as an alternative to antibiotics for growth promotion in the presence of disease causing organisms is the use of egg yolk antibodies generally referred to as IgY [36]. In order to produce these antibodies, laying hens are injected with organisms that cause specific diseases in swine. The injection of these antigens induces an immune response in the hen which results in the production of antibodies. These antibodies are typically deposited in the egg yolk. Booster immunizations are given to ensure continued transfer of antibodies from the hen to the egg yolk. These antibodies are then extracted from the egg yolk and processed. Antibodies can be administered in the feed in several forms including whole egg powder, whole yolk powder, water-soluble fraction powder or purified IgY [37]. Details concerning IgY production including choice of adjuvant, route of immunization, dose, immunization frequency and techniques for IgY extraction from the yolk have been reviewed by Chalghoumi et al. [37] and Kovacs-Nolan and Mine [38].

Compared with the use of mammals such as rabbits or sheep for antibody production, the immunization of chickens for antibody production is an attractive approach. Chicken housing is inexpensive, egg collection is non-invasive, the IgY antibodies are concentrated in egg yolk and isolation is fast and simple. In addition, chicken immunnoglobin does not react with mammalian IgG or IgM and also it does not activate mammalian complement factors [38]. Finally, the use of IgY elicits no undesirable side effects, disease resistance or toxic residues [36].

IgY antibodies have been tested against a number of enteric pathogens in swine including E. coli, Salmonella and Rotaviru s with varying degrees of success [3943]. Table 3 shows the results of an experiment where the performance of pigs fed egg yolk antibodies was compared with that of pigs fed diets supplemented with zinc oxide, fumaric acid or antibiotics. All four feed additives successfully increased pig performance compared with unsupplemented pigs with significant reductions observed in scour score and piglet mortality. In this experiment, egg yolk antibody was equal to antibiotics in enhancing pig performance.
Table 3

Effect of egg yolk antibody, zinc oxide, fumaric acid and antibiotic on the performance and intestinal morphology of 10 to 24 day old pigs fed diets based on pea protein concentrate

Items

Control

Egg yolk antibody

Zinc oxide

Fumaric acid

Carbadox

SEM

Weight gain, g/d

100.9

151.2

158.9

155.4

152.6

16.6

Feed intake, g/d

141.0

208.1

214.7

211.6

222.4

15.3

Feed conversion

1.39

1.38

1.35

1.36

1.45

0.04

Scour score

2.7

1.3

1.4

1.3

1.1

-

Mortality, %

40.0

6.6

13.3

6.6

13.3

-

Villus height, m

355

564

488

573

570

20.0

Crypt depth, m

204

183

190

207

204

10.1

Villous height:crypt depth

1.7

3.1

2.6

2.8

2.8

0.11

Owusu-Asiedu et al. [41].

Unfortunately, there are several reports where egg yolk antibody failed to improve pig performance [42, 44]. The most likely explanation for the failure of egg yolk antibody to improve performance is that the antibody failed to survive passage through the gastrointestinal tract [45]. It appears that the IgY molecule is less stable than the IgG molecule due to its higher molecular weight, lower percentage of β-sheet structure and reduced flexibility [45]. It has been reported that the activity of IgY was decreased at pH 3.5 or lower and almost completely lost activity with irreversible change at pH 3 [37]. In addition, IgY is fairly sensitive to pepsin digestion [45]. Therefore, a recent avenue of research has been to use microencapsulation techniques to protect IgY from gastric inactivation [46, 47].

Table 4 shows the results of an experiment where chitosan-alginate microcapsules were used for oral delivery of egg yolk immunoglobulin in weaned pigs challenged with enterotoxigenic E. coli C83903 [46]. The percentage of pigs with diarrhea 24 h after treatment and the diarrhea score were improved in pigs receiving encapsulated IgY compared with non-encapsulated IgY. In addition, weight gain over the three day period was significantly higher in pigs receiving encapsulated IgY compared with non-encapsulated IgY. Both encapsulated and non-encapsulated IgY treatments were numerically superior to an aureomycin treated group.
Table 4

Effect of encapuslation of IgY on performance and the incidence of diarrhea in pigs challenged with E. coli

 

Percentage of pigs with diarrhea after specific times (Fecal score in brackets)1

  

Items

9 h

24 h

48 h

72 h

Weight gain (g/d)

Recovery rate (%)

Negative control, unchallenged

0% (0.5)

0% (0.0)

0% (0.4)

0% (0.0)

116.6a

-

Positive control

75% (2.5)

75% (2.5)

75% (2.0)

75% (2.0)

13.5d

0%

Non-encapsulated IgY

100% (2.0)

75% (1.3)

25% (1.0)

0% (0.0)

78.1b

100%

Microencapsulated IgY

75% (2.0)

0% (0.0)

0% (0.0)

0% (0.0)

110.4a

100%

Aureomycin

100% (2.0)

50% (2.0)

75% (1.5)

50% (1.5)

54.1c

50%

Li et al. [46].

1Fecal score is the mean fecal consistency score where 0 = normal, 1 = soft feces, 2 = mild diarrhea, 3 = severe diarrhea.

a,b,c,dWithin column, means followed by same or no letter do not differ (P>0.05).

The mechanism through which IgY counteracts pathogen activity has not been determined. However, several mechanisms were proposed by Xu et al. [36] including agglutination of bacteria, inhibition of adhesion, opsonization followed by phagocytosis and toxin neutralization. Further research is necessary to determine the exact mechanism for the growth promoting activity of IgY.

Essential oils

Essential oils are aromatic oily liquids obtained from plant material and usually have the characteristic odor or flavor of the plant from which they are obtained [48]. They are typically mixtures of secondary plant metabolites and may contain phenolic compounds (i.e. thymol, carvacrol and eugenol), terpenes (i.e. citric and pinapple extracts), alkaloids (capsaicine), lectins, aldehydes (i.e. cinnamaldehyde), polypeptides or polyacetylenes [49]. They can be extracted from plants with organic solvents or steam distillation [49]. An estimated 3000 essential oils are known to exist but cinnamaldehyde, carvacrol, eugenol and thymol have received the most interest for use in swine production.

Interest in the use of essential oils as a potential replacement for antibiotics in swine rations has been generated as a result of in vitro studies showing that essential oils have antimicrobial activity against microflora commonly present in the pig gut [50]. The exact mode of action of essential oils has not been established but the activity may be related to changes in lipid solubility at the surface of the bacteria [48]. The hydrophobic constituents of essential oils allow them to disintegrate the outer membrane of E. coli and Salmonella and thus inactivate these pathogens [48]. This would result in a shift in the microbial ecology in favor of lactic acid producing bacteria and reducing the number of pathogenic bacteria [50]. Essential oils containing phenolic compounds tend to have greater antimicrobial activity than oils containing other compounds [51].

Based on the fact that essential oils appear to control pathogenic bacteria, several research groups have attempted to determine whether or not the inclusion of essential oils in swine diets can improve pig performance [52]. The results have been inconclusive with some trials demonstrating positive results [5355] while others have reported no beneficial effects [56, 57]. The most compelling evidence for including essential oils in diets fed to swine can be obtained from the results of Li et al. [55]. This trial compared the performance of pigs fed an unsupplemented control diet with that of pigs fed a diet supplemented with antibiotics or a combination of thymol and cinnamaldehyde (Table 5). Weight gain, feed conversion and fecal consistency of pigs fed essential oils was essentially equal to that of pigs fed antibiotics. The improved performance appeared to be mediated by improvements in dry matter and protein digestibility arising from improvements in intestinal morphology. In addition, total antioxidant capacity and levels of the cytokines interleukin-6 and tumor necrosis factor-α were altered by inclusion of essential oils (Table 6).
Table 5

Effect of essential oils on weanling pig performance, nutrient digestibility and fecal consistency

Items

Control

Antibiotic1

Essential oil

SEM

Performance

 Weight gain, g/d

442a

505b

493b

15

 Feed intake, g/d

783

846

789

24

 Feed conversion

1.79

1.67

1.62

0.06

 Fecal consistency

1.53a

1.22b

1.30b

0.06

Nutrient digestibility

 Dry matter

84.33a

87.03b

86.92b

0.65

 Crude protein

76.51a

83.53b

81.34b

1.25

Li et al. [55].

1Chlortetracycline, colistin sulfate and kitasamycin.

a,b Within row, means followed by same or no letter do not differ (P>0.05).

Table 6

Effect of essential oils on intestinal morphology, antioxidant capacity, and cytokine levels in weanling pigs

Items

Control

Antibiotic1

Essential oil

SEM

Villus height, μm

466

509

535

24

Crypt depth, μm

164

156

162

8

Villus height:crypt depth

2.96a

3.41b

3.38b

0.09

Total antioxidant capacity, U/mL

10.46a

11.97ab

12.37b

0.52

Interleukin-6, ng/L

44.21a

40.39a

27.40b

2.76

Tumor necrosis factor-α, ng/L

208a

237ab

260b

13

Li et al. [55].

1Chlortetracycline, colistin sulfate and kitasamycin.

a,bWithin row, means followed by same or no letter do not differ (P>0.05).

The reason for the variability in results when essential oils are fed is likely due to differences in the type of essential oils used and the dose provided [55]. As noted previously, oils containing phenolic compounds tend to have greater antimicrobial activity than those based on other compounds. In addition, if the dose used is too high, the strong smell can reduce feed intake and thereby limit pig performance [48]. Another important consideration is the stability of essential oils during pelleting. Maenner et al. [54] reported considerable loss of activity of essential oils when a pelleting temperature of 58°C was applied.

Eucalyptus oil-medium chain fatty acids

Eucalyptus oil is obtained from the leaves of the eucalyptus, a tree which belongs to the plant family Myrtaceae and is cultivated worldwide. In humans, eucalyptus oil has been shown to have antibacterial effects on pathogenic bacteria in the respiratory tract [58]. Eucalyptus oil has also been shown to stimulate the immune system by affecting the phagocytic ability of monocyte-derived macrophages [59]. In poultry, dietary inclusion of eucalyptus has been shown to improve production performance and stimulate the immunity of commercial laying hens [60].

Medium-chain fatty acids have been suggested as an alternative feed additive to antibiotics for piglets [6163]. Medium chain fatty acids have been shown to have antimicrobial activity against Salmonella[64] and E. coli[61]. Hong et al. [63] reported that feeding a blend of caprylic and caproic acids improved performance and nutrient digestibility in 3 and 4 week old weaned pigs during the first two weeks following weaning.

Micro-encapsulation of medium chain fatty acids is a process in which medium chain fatty acids are nano-micronized to extremely small particles and then encapsulated. Han et al. [65] tested a product where eucalyptus extract was mixed with caprylic and carpric acids and encapsulated with palm oil in comparison with antibiotics or zinc oxide (Table 7). The performance of pigs fed the eucalyptus-medium chain fatty acid blend was essentially equal to that of antibiotics or zinc oxide. The performance enhancing effects of the blend appeared to be mediated through improvements in nutrient digestibility (Table 8). The process used to produce the micro-encapsualted eucalyptus-medium chain fatty acid blend has been patented by the Korean Intellectual Property Office under patent number 10-2009-0025329.
Table 7

Effects of antibiotics, zinc oxide, and eucalyptus-medium chain fatty acids (MCFA) on nursery pig performance

Items

Control

Antibiotics1

ZnO ( 1,500 ppm)

ZnO (2,500 ppm)

Eucalyptus-MCFA

SEM

P

Weight gain, g/d

243a

315b

298b

308b

310b

13.6

<0.01

Feed intake, g/d

361a

431b

426b

429b

448b

18.1

<0.01

Feed conversion

1.53

1.41

1.44

1.41

1.46

0.05

0.35

Han et al. [65].

1Tiamulin and lincomycin.

a,bWithin row, means followed by same or no letter do not differ (P>0.05).

Table 8

Effects of antibiotics, zinc oxide, and eucalyptus-medium chain fatty acids (MCFA) on nutrient digestibility for weaned pigs

Items

Antibiotics1

ZnO (1,500 ppm)

ZnO (2,500 ppm)

Eucalyptus-MCFA

SEM

P

Dry matter

91.74a

90.58b

90.44b

92.17a

0.26

< 0.01

Crude protein

74.18a

72.01a

71.23a

78.93b

1.13

< 0.01

Calcium

56.31a

48.26b

46.75b

65.93c

1.56

<0.01

Phosphorus

54.48a

38.25b

42.77b

66.10b

2.01

<0.01

Energy

82.92a

81.60b

81.00b

86.00c

0.61

< 0.01

Lysine

79.13a

80.25b

78.25a

83.80b

0.88

< 0.01

Methionine

83.94a

80.95b

80.78b

84.23a

0.63

<0.01

Threonine

73.56b

73.57b

73.43b

79.40a

1.40

0.02

Han et al. [65].

1Tiamulin and lincomycin.

a,bWithin row, means followed by same or no letter do not differ (P>0.05).

Rare earth elements

Rare earth elements comprise the elements scandium, yttrium, lanthanum and the 14 chemical elements following lanthanum in the periodic table called lanthanoids [66]. The application of rare earth elements as feed additives for livestock has been practiced in China for decades [66]. There are many articles in the Chinese literature concerning the performance enhancing effects of rare earth elements for swine [67, 68] and many more have been reviewed by Rambeck and Wehr [69] and Redling [66]. In the Chinese literature, body weight gain was shown to be improved by 5 to 23% and feed conversion between 4 and 19% under the influence of rare earth elements.

Research concerning the effect of rare earth elements on swine performance have been published in the Western literature since about the year 2000 with some reports indicating significant improvements in pig performance [70, 71] while others have observed no change [72]. Table 9 shows the results of a recent trial in which the performance of weaned pigs fed a lanthanum-yeast mixture was similar to that of pigs fed diets supplemented with antibiotics or zinc oxide [73].
Table 9

Effects of zinc oxide, antibiotic, or lanthanum-yeast on the performance of weanling pigs (day 0 to 28)

Items

Control

Antibiotic1

Zinc (1,500 ppm)

Zinc (2,500 ppm)

Lanthanum-yeast

SEM

P Values

Weight gain, g/d

302b

353a

352a

369a

359a

14.0

0.02

Feed intake, g/d

467b

518ab

530ab

558a

501ab

22.6

0.10

Feed conversion

1.55a

1.47ab

1.50ab

1.52ab

1.41b

0.04

0.31

Han and Thacker [73].

1Tiamulin and chlortetraccycline.

a,b Within row, means followed by same or no letter do not differ (P>0.05).

The products commonly used as feed additives for swine are typically mixtures of rare earth elements mainly containing lanthanum, cerium and praseodymium [73]. Both inorganic and organic rare earth compounds have been used as feed additives but it is believed that best results are obtained with organic compounds [66].

Several mechanisms have been proposed for the growth promoting effects of rare earth elements. It has been suggested that rare earth elements may promote growth by influencing the development of undesirable bacterial species within the gastrointestinal tract. For example, lanthanum has been shown to bind to the surface of bacteria [69]. This reduces the surface charge and retards electrophoretic migration. When the surface charge is completely neutralized, flocculation occurs. In addition, bacterial respiration has been shown to be strongly inhibited by lanthanides [69].

Another explanation for the growth promoting effects of rare earth elements is due to improvements in nutrient digestibility and availability as was observed by Han and Thacker [73]; Table 10]. It has been suggested that rare earth elements may influence the permeability of the intestines thereby enhancing the absorption of different nutrients [66]. Enhanced secretion of digestive fluids and increased gastrointestinal motility have also been proposed as explanations for the enhanced digestibility of nutrients following dietary inclusion of rare earth elements [66].
Table 10

Effects of antibiotics, zinc oxide or lanthanum-yeast on nutrient digestibility

Items

Antibiotics1

Zinc(1,500 ppm)

Zinc (2,500 ppm)

Lanthanum-yeast

SEM

P-value

Dry matter

95.19a

93.83b

93.98b

95.46a

0.30

<0.01

Crude protein

74.51ab

71.55b

72.33b

78.34a

1.38

0.01

Calcium

56.59b

46.98c

48.50c

65.10a

1.69

<0.01

Phosphorus

54.87b

43.07c

38.52c

66.11a

2.09

<0.01

Energy

83.51b

81.42b

81.33b

86.89a

0.80

<0.01

Lysine

81.45b

79.42b

80.32b

85.15a

0.95

<0.01

Methionine

83.49b

83.67b

86.76a

87.32a

0.79

<0.01

Phenylalanine

74.21b

73.75b

75.41ab

78.96a

1.32

0.05

Threonine

76.19b

75.13b

75.28b

81.19a

1.58

0.04

Han and Thacker [73].

1Tiamulin and chlortetraccycline.

a,b,cWithin row, means followed by same or no letter do not differ (P>0.05).

Rare earth elements have several properties that make them attractive alternatives to antibiotics. Generally, absorption of orally applied rare earths is low with more than 95% being recovered in the feces of animals [66]. As a result, the chances of residues being present in meat are low with studies reporting no higher levels of rare earth elements in the muscle tissue of supplemented animals than those fed commercial diets [66]. In addition, there have been no reports of the development of bacterial resistance in treated animals [66].

Recombinant enzymes

Enzymes are biologically active proteins that break specific chemical bonds to release nutrients for further digestion and absorption. They accelerate chemical reactions in the body which would otherwise proceed very slowly or not at all [74]. Enzymes used in the feed industry are commonly produced by bacteria (i.e. Bacillus subtilis), fungus (i.e. Trichoderma reesei, Aspergillus niger) or yeast (Saccharomyces cerevisiae).

The supplementation of swine diets with exogenous enzymes to enhance performance is not a new concept and research articles in this field date back to the 1950’s [10]. The most common reasons for enzyme supplementation include degrading feed components resistant to endogenous enzymes (i.e. β-glucanase, xylanase, mannanase, pectinase and galactosidase), inactivating antinutritional factors (i.e. phytase) and supplementing endogenous enzymes that may be present in insufficient amounts (i.e. proteases, lipases and amylases). This review will focus on the use of enzymes to degrade feed components resistant to endogenous enzymes.

The cell walls of cereal grains, legumes and oilseed meals are comprised of complex carbohydrates commonly referred to as non-starch polysaccharides [75]. Non-starch polysaccharides consist of a wide range of polymers which include cellulose, hemicellulose, pectins, β-glucans, α-galctosides (raffinose, stachnyose and verbascose) and xylans [8]. These non-starch polysaccharides reduce the nutritional value of feed ingredients in a number of ways [74]. Firstly, they are indigestible by mammalian enzymes and therefore dilute the energy and nutrient content of the feed. Secondly, non-starch polysaccharides exhibit a so called "cage effect" whereby normally highly digestible nutrients such as starch, fat and protein are entrapped in a coating of non-starch polysaccharides preventing access of the endogenous enzymes to these substrates [76]. In addition, certain non-starch polysaccharides may increase intestinal viscosity. It has also been suggested that non-starch polysaccharides allow microbial populations to assimilate a greater proportion of the nutrients contained in the feed into their own system thereby reducing the availability of these nutrients to the host [8].

Carbohydrases include all enzymes that catalyze a reduction in the molecular weight of polymeric carbohydrate but more than 80% of the global carbohydrase market is accounted for by xylanase and β-glucanase [10]. Other commercially available carbohydrases include α-amylase, β-mannanase, α-galactosidase and pectinase. These carbohydrases have widespread application in the poultry industry but are used less commonly in feeds for swine.

The effect of carbohydrase supplementation on the performance of pigs is inconsistent. There are reports of positive responses to carbohydrase supplementation [77, 78], whereas others have reported no improvement in weight gain in response to enzymes [7981]. Where positive effects on performance are observed, they are commonly associated with increases in nutrient digestibility likely as a result of increased accessibility of endogenous enzymes to nutrients as a result of inhibition of the "cage effect" as well as hydrolysis or partial hydrolysis of the non-starch polysaccharide. There also seems to be an influence on th e composition of the microflora in the digestive tract [76]. Hydrolysis of non-starch polysaccharides results in increased sugar release in the large and small intestine and thereby stimulates the growth of lactobacilli which produce lactic acid. Increased proportions of lactic acid promote gut health by suppressing the growth of coliforms such as pathogenic E. coli.

Based on a review of the literature, it is clear that the response of pigs to supplementation with carbohydrases is less consistent than has been observed with poultry. The question is why? What differences are there in the physiology of the pig and the chicken that might account for the differences in the magnitude of the results obtained. One clear difference is the pH in the gut. In the pig, the duration that feed is exposed to a low pH is significantly longer than in the chicken [82]. Therefore, it is possible that exposure to the low pH in the stomach of the pig is either partially or totally denaturing the enzyme accounting for the lower magnitude of responses obtained when carbohydrases are fed to pigs compared with poultry.

Many of the enzyme preparations used in the past were unsuitable for use in the harsh environment of the pig’s gastrointestinal tract. The pH in the stomach of the pig is usually between 2 and 3.5 and substantial reductions in β-glucanase [82] and xylanase [83] activity were reported when ten commercially available enzyme products were exposed in vitro to a pH of 2.5 or 3.5 for 30 min.

The application of genetic engineering in the process of enzyme production allows the development of enzymes targeted for specific purposes [8486]. Recently, several carbohydrases have been developed by molecular directed evolution which have considerable potential for animal feed application [8486]. Enzymes have been developed which are active over a broad pH range, exhibit thermostability, are resistant to pepsin and trypsin, and viable under simulated gastric conditions.

Inclusion of a recombinant β-mannanase in corn soybean meal diets fed to growing pigs increased weight gain by 16.1% and feed efficiency by 17.7% compared with an unsupplemented diet (Table 11). The magnitude of the improvement was notably greater than previous experiments using β-mannanase produced by traditional fermentation techniques. For example, Pettey et al. [87] reported that weight gain was only increased 3.4% and feed efficiency 3.9% in their experiment in which growing–finishing pigs were fed diets supplemented with β-mannanase.
Table 11

Comparison of the effects of a β-mannase produced using normal fermentation technology with that of a recombinant β-mannase on the performance of growing-finishing pigs

Items

Control

β-mannase

% Improvement

Traditional fermentation 1

 Weight gain, g/d

0.84

0.87

3.4

 Feed intake, g/d

2.50

2.48

-

 Feed efficiency

0.337

0.351

3.9

Recombinant technology 2

 Weight gain, g/d

0.66

0.79

16.4

 Feed intake, g/d

1.66

1.61

3.0

 Feed efficiency

0.404

0.491

17.7

1Pettey et al. [87].

2Lv et al. [85].

Enzymes added to feed are broken down in the digestive tract in the same way as other proteins [74]. Therefore, there are not any issues with residues and it is not necessary to observe any withdrawal periods before animals fed enzymes can be slaughtered [74]. For this reason, the amount of enzyme required is very small compared with the amount of substrate and therefore only small quantities are needed when using enzymes in ration formulation.

Miscellaneous compounds

Many additional compounds have been tested for their potential to replace antibiotics as growth promoters for use in swine production. They are too numerous to be able to go into much detail regarding their effectiveness. Some of the more promising include spray-dried porcine plasma [88, 89], yeast culture [9092], bacteriophages [93], lysozyme [94], bovine colostrum [95], lactoferrin [9698], conjugated fatty acids [99, 100], chito-oligosaccarides [101, 102] and seaweed extract [103].

Conclusions

Clearly, a long and growing list of compounds exist which have been tested for their ability to replace antibiotics as feed additives to maintain swine health and performance. Unfortunately, the vast majority of these compounds produce inconsistent results and rarely equal antibiotics in their effectiveness. Therefore, it would appear that research is still needed in this area and that the perfect alternative does not exist as yet.

Declarations

Authors’ Affiliations

(1)
Department of Animal and Poultry Science, University of Saskatchewan

References

  1. Cromwell GL: Why and how antibiotics are used in swine production. Anim Biotechnol. 2002, 13: 7-27. 10.1081/ABIO-120005767.PubMedView ArticleGoogle Scholar
  2. Vondruskova H, Slamova R, Trckova M, Zraly Z, Pavli I: Alternatives to antibiotic growth promotors in prevention of diarrhea in weaned piglets: a review. Vet Med. 2010, 55: 199-224.Google Scholar
  3. Van der Fels-Klerx HJ, Puister-Jansen LF, Van Asselt ED, Burgers SL: Farm factors associated with the use of antibiotics in pig production. J Anim Sci. 2011, 89: 1922-1929. 10.2527/jas.2010-3046.PubMedView ArticleGoogle Scholar
  4. Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS: Feed additives for swine: fact sheets-prebiotics and probiotics, and phytogenics. J Swine Health Prod. 2010, 18: 132-136.Google Scholar
  5. Simon O: An interdisciplinary study on the mode of action of probiotics in pigs. J Anim Feed Sci. 2010, 19: 230-243.Google Scholar
  6. Cho JH, Zhao PY, Kim IH: Probiotics as a dietary additive for pigs: a review. J Anim Vet Adv. 2011, 10: 2127-2134.View ArticleGoogle Scholar
  7. Halas V, Nochta I: Mannan oligosaccharides in nursery pig nutrition and their potential mode of action. Animals. 2012, 2: 261-274. 10.3390/ani2020261.PubMed CentralPubMedView ArticleGoogle Scholar
  8. Thacker PA: Recent advances in the use of enzymes with special reference to β-glucanases and pentosanases in swine rations. Asian-Aust J Anim Sci. 2000, 13: 376-385. (Special Issue)View ArticleGoogle Scholar
  9. Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS: Feed additives for swine: fact sheets-carcass modifers, carbohydrate-degrading enzymes and proteases, and anthelmintics. J Swine Health Prod. 2009, 17: 325-332.Google Scholar
  10. Adeola O, Cowieson AJ: Opportunities and challenges in using exogenous enzymes to improve nonruminant animal production. J Anim Sci. 2011, 89: 3189-3218. 10.2527/jas.2010-3715.PubMedView ArticleGoogle Scholar
  11. Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS: Feed additives for swine: fact sheets-acidifiers and antibiotics. J Swine Health Prod. 2009, 17: 270-275.Google Scholar
  12. Kil DY, Kwon WB, Kim BG: Dietary acidifiers in weanling pig diets: a review. Revista Colombian de Diencias Pecuarias. 2011, 24: 1-22.Google Scholar
  13. Suruanarayana MV, Suresh J, Rajasekhar MV: Organic acids in swine feeding: a review. Agric Sci Res J. 2012, 2: 523-533.Google Scholar
  14. Papatsiros VG, Billinis C: The prophylactic use of acidifiers as antibacterial agents in swine. Antimicrobial agents. Edited by: Bobbarala V. 2012, 295-310. InTech, DOI:10.5772/32278. Available from: http://www.intechopen.com/books/antimicrobial-agents/the-prophylactic-use-of-acidifiers-as-antibacterial-agents-in-swine. 978-953-51-0723-1Google Scholar
  15. Windisch W, Schedle K, Plitzner C, Kroismayr A: Use of phytogenic products as feed additives for swine and poultry. J Anim Sci. 2008, 86 (E. Suppl): E140-E148.PubMedGoogle Scholar
  16. Liu HW, Tong JM, Zhou DW: Utilization of Chinese herbal feed additives in animal production. Agric Sci China. 2011, 10: 1262-1272. 10.1016/S1671-2927(11)60118-1.View ArticleGoogle Scholar
  17. Pettigrew JE: Reduced use of antibiotic growth promoters in diets fed to weanling pigs: dietary tools, part 1. Anim Biotechnol. 2006, 17: 207-215. 10.1080/10495390600956946.PubMedView ArticleGoogle Scholar
  18. Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS: Feed additives for swine: fact sheets-high dietary levels of copper and zinc for young pigs, and phytase. J Swine Health Prod. 2010, 18: 87-91.Google Scholar
  19. Li YM, Xiang Q, Zhang QH, Huang YD, Su ZJ: Overview on the recent study of antimicrobial peptides: origins, functions, relative mechanisms and application. Peptides. 2012, 37: 207-215. 10.1016/j.peptides.2012.07.001.PubMedView ArticleGoogle Scholar
  20. Koczulla AR, Bals R: Antimicrobial peptides: current status and therapeutic potential. Drugs. 2003, 63: 389-406. 10.2165/00003495-200363040-00005.PubMedView ArticleGoogle Scholar
  21. Wu SD, Zhang FR, Huang ZM, Liu H, Xie CY, Zhang J, Thacker PA, Qiao S: Effect of the antibacterial peptide cecropin AD on performance and intestinal health in weaned piglets challenged with Escherichia coli. Peptides. 2012, 35: 225-230. 10.1016/j.peptides.2012.03.030.PubMedView ArticleGoogle Scholar
  22. Yusuf MA, Hamid TH: Lactic acid bacteria: bacteriocin producer: a mini review. IOSR J Pharm. 2013, 3: 44-50.Google Scholar
  23. Stahl CH, Callaway TR, Lincoln LM, Lonergan SM, Genovese KJ: Inhibitory activities of colicins against Esherichia coli strains responsible for postweaning diarrhea and edema disease in swine. Antimicrob Agents Chemother. 2004, 48: 3119-3121. 10.1128/AAC.48.8.3119-3121.2004.PubMed CentralPubMedView ArticleGoogle Scholar
  24. Cutler SA, Lonergan SM, Cornick N, Johnson AK, Stahl CH: Dietary inclusion of colicin E1 is effective in preventing postweaning diarrhea caused by F18-positive Esherichia coli in pigs. Antimicrob Agents Chemother. 2007, 51: 3830-3835. 10.1128/AAC.00360-07.PubMed CentralPubMedView ArticleGoogle Scholar
  25. Yoon JH, Ingale SL, Kim JS, Kim KH, Lohakare J, Park YK, Park JC, Kwon LK, Chae BJ: Effects of dietary supplementation with antimicrobial peptide-P5 on growth performance, apparent total tract digestibility, faecal and intestinal microflora and intestinal morphology of weanling pigs. J Sci Food Agric. 2013, 93: 587-592. 10.1002/jsfa.5840.PubMedView ArticleGoogle Scholar
  26. Yoon JH, Ingale SL, Kim JS, Kim KH, Lee SH, Park YK, Kwon IK, Chae BJ: Effects of dietary supplementation of antimicrobial peptide-A3 on growth performance, nutrient digestibility, intestinal and fecal microflora and intestinal morphology in weanling pigs. Anim Feed Sci Technol. 2012, 177: 98-107. 10.1016/j.anifeedsci.2012.06.009.View ArticleGoogle Scholar
  27. Wang JH, Wu CC, Feng J: Effect of dietary antibacterial peptide and zinc-methionine on performance and serum biochemical parameters in piglets. Czech J Anim Sci. 2011, 56: 30-36.Google Scholar
  28. Schell TC, Lindemann MD, Kornegay ET, Blodgett DJ: Effects of feeding aflatoxin-contained diets with and without clay to weanling and growing pigs on performance, liver function and mineral metabolism. J Anim Sci. 1993, 71: 1209-1218.PubMedGoogle Scholar
  29. Schell TC, Lindemann MD, Kornegay ET, Blodgett DJ: Effects of different types of clay for reducing the detrimental effects of aflatoxin-contained diets on performance and serum profiles of weanling pigs. J Anim Sci. 1993, 71: 1226-1231.PubMedGoogle Scholar
  30. Trckova M, Vondruskova H, Zraly Z, Alexa P, Kummer V, Maskova J, Mrlik V, Krizova K, Slana I, Leva L, Pavlik I: The effect of kaolin feeding on efficiency, health status and course of diarrheoal infections caused by enterotoxigenic Esherichia coli strains in weaned piglets. Vet Med. 2009, 54: 47-63.Google Scholar
  31. Song M, Liu Y, Soares JA, Che TM, Osuna O, Maddox CW, Pettigrew JE: Dietary clays alleviate diarrhea of weaned pigs. J Anim Sci. 2012, 90: 345-360. 10.2527/jas.2010-3662.PubMedView ArticleGoogle Scholar
  32. Thacker PA: Performance of growing-finishing pigs fed diets containing graded levels of Biotite, and alumninosilicate clay. Asian-Aust J Anim Sci. 2003, 16: 1666-1672.View ArticleGoogle Scholar
  33. Chen YJ, Kwon OS, Min BJ, Son KS, Cho JH, Hong JW, Kim IH: The effects of dietary Biotite V supplementation as an alternative substance to antibiotics in growing pigs. Asian-Aust J Anim Sci. 2005, 18: 1642-1645.View ArticleGoogle Scholar
  34. Prvulovic D, Jovanovic-Galovic A, Stanic B, Popovic M, Grubor-Lajsic G: Effects of a clinoptilolite supplement in pig diets on performance and serum parameters. Czech J Anim Sci. 2007, 52: 159-164.Google Scholar
  35. Yan L, Hong SM, Kim IH: Effect of bacteriophage supplementation on the growth performance, nutrient digestibility, blood characteristics, and fecal microbial shedding in growing pigs. Asian-Aust J Anim Sci. 2012, 25: 1451-1456. 10.5713/ajas.2012.12253.View ArticleGoogle Scholar
  36. Xu Y, Li X, Jin L, Zhen Y, Lu Y, Li S, You J, Wang L: Application of chicken egg yolk immunoglobulins in the control of terrestrial and aquatic animal diseases: a review. Biotechnol Adv. 2011, 29: 860-868.PubMedView ArticleGoogle Scholar
  37. Chalghoumi R, Beckers Y, Portetelle D, Thewis A: Hen egg yolk antibodies (IgY) production and use for passive immunization against bacterial enteric infections in chicken: a review. Biotechnol Agron Soc Environ. 2009, 13: 295-308.Google Scholar
  38. Kovacs-Nolan J, Mine Y: Egg yolk antibodies for passive immunity. Annu Rev Food Sci Technol. 2012, 3: 163-182. 10.1146/annurev-food-022811-101137.PubMedView ArticleGoogle Scholar
  39. Marquardt RR, Jin LZ, Kim JW, Fang L, Frohlich AA, Baidoo SK: Passive protective effect of egg-yolk antibodies against enterotoxigenic Esherichia coli K88+ infection in neonatal and early-weaned piglets. FEMS Immunol Med Microbiol. 1999, 23: 283-288.PubMedView ArticleGoogle Scholar
  40. Owusu-Asiedu A, Nyachoti CM, Baidoo SK, Marquardt RR, Yang X: Response of early-weaned pigs to an enterotoxigenic Esherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody. J Anim Sci. 2003, 81: 1781-1789.PubMedGoogle Scholar
  41. Owusu-Asiedu A, Nyachoti CM, Marquardt RR: Response of early-weaned pigs to an enterotoxigenic Esherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody, zinc oxide, fumaric acid or antibiotic. J Anim Sci. 2003, 81: 1790-1798.PubMedGoogle Scholar
  42. Hong JW, Kwon OS, Min BJ, Lee WB, Shon KS, Kim IH, Kim JW: Evaluation effects of spray-dried egg protein containing specific egg yolk antibodies as a substitute for spray-dried plasma protein or antibiotics in weaned pigs. Asian-Aust J Anim Sci. 2004, 17: 1139-1144.View ArticleGoogle Scholar
  43. Zhang ZF, Kim IH: Effects of egg yolk immunoglobulin on growth performance, diarrhea score, diarrhea incidence and serum antibody titer in pre-and post-weaned pigs. Wayamba J Anim Sci. 2013, 578X: 590-597.Google Scholar
  44. Chernysheva LV, Friendship RM, Dewey CE, Gyles CL: The effect of dietary chicken egg-yolk antibodies on the clinical response in weaned pigs challenged with a K88+ Esherichia coli isolate. J Swine Health Prod. 2003, 12: 119-122.Google Scholar
  45. Kovacs-Nolan J, Mine Y: Microencapsulation for the gastric passage and controlled intestinal release of immunoglobulin Y. J Immunol Methods. 2005, 296: 199-209. 10.1016/j.jim.2004.11.017.PubMedView ArticleGoogle Scholar
  46. Li XY, Jin LJ, Uzonna JE, Li SY, Liu JJ, Li HQ, Lu YN, Zhen YH, Xu YP: Chitosan-alginate microcapsules for oral delivery of egg yolk immunoglobulin (IgY): in vivo evaluatin in a pig model of enteric colibacillosis. Vet Immunol Immunopathol. 2009, 129: 132-136. 10.1016/j.vetimm.2008.12.016.PubMedView ArticleGoogle Scholar
  47. Li XY, Jin LJ, McAllister TA, Stanford K, Xu JY, Lu YN, Zhen YH, Sun YX, Xu YP: Chitosan-alginate microcapsules for oral delivery of egg yolk immunoglobulin (IgY). J Agric Food Chem. 2007, 55: 2911-2917. 10.1021/jf062900q.PubMedView ArticleGoogle Scholar
  48. Stein HH, Kil DY: Reduced use of antibiotic growth promoters in diets fed to weanling pigs: dietary tools, Part 2. Anim Biotechnol. 2006, 17: 217-231. 10.1080/10495390600957191.PubMedView ArticleGoogle Scholar
  49. Gatnau R: Use of plant extracts in swine. 2009, Available at http://www.pig333.com/nutrition/use-of-plant-extracts-in-swine_957/Google Scholar
  50. Michiels J, Missotten JA, Fremaut D, De Smet S, Dierick NA: In vitro characterization of the antimicrobial activity of selected essential oil components and binary combinations against the pig gut flora. Anim Feed Sci Technol. 2009, 151: 111-127. 10.1016/j.anifeedsci.2009.01.004.View ArticleGoogle Scholar
  51. Brenes A, Roura E: Essential oils in poultry nutrition: main effects and modes of action. Anim Feed Sci Technol. 2010, 158: 1-14. 10.1016/j.anifeedsci.2010.03.007.View ArticleGoogle Scholar
  52. Ragland D, Stevenson D, Hill MA: Oregano oil and multi-component carbohydrases as alternatives to antimicrobials in nursery diets. Swine Health Prod. 2008, 16: 238-243.Google Scholar
  53. Cho JH, Chen YJ, Min BJ, Kim HJ, Kwon OS, Shon KS, Kim IH, Kim SJ, Asamer A: Effects of essential oils supplementation on growth performance, IgG concentration and fecal noxious gas concentration of weaned pigs. Asian-Aust J Anim Sci. 2006, 19: 80-85.View ArticleGoogle Scholar
  54. Maenner K, Vahjen W, Simon O: Studies on the effects of essential-oil based feed additives on performance, ileal nutrient digestibility, and selected bacterial groups in the gastrointestinal tract of piglets. J Anim Sci. 2011, 89: 2106-2112. 10.2527/jas.2010-2950.PubMedView ArticleGoogle Scholar
  55. Li PF, Piao XS, Ru YJ, Han X, Xue LF, Zhang HY: Effects of adding essential oil to the diet of weaned pigs on performance, nutrient utilization, immune response and intestinal health. Asian-Aust J Anim Sci. 2012, 25: 1617-1626. 10.5713/ajas.2012.12292.View ArticleGoogle Scholar
  56. Ahmed ST, Hossain ME, Kim GM, Hwang JA, Ji H, Yang CJ: Effect of resveratrol and essential oils on growth performance, immunity, digestibility and fecal microbial shedding in challenged piglets. Asian-Aust J Anim Sci. 2013, 26: 683-690. 10.5713/ajas.2012.12683.View ArticleGoogle Scholar
  57. Huang Y, Yoo JS, Kim HJ, Wang Y, Chen YJ, Cho JH, Kim IH: Effects of dietary supplementation with blended essential oils on growth performance, nutrient digestibility, blood profiles and fecal characteristics in weanling pigs. Asian-Aust J Anim Sci. 2010, 23: 607-613.View ArticleGoogle Scholar
  58. Salari MH, Amine G, Shirazi MH, Hafezi R, Mohammadypour M: Antibacterial effects of Eucalyptus globulus leaf extract on pathogenic bacteria isolated from specimens of patients with respiratory tract disorders. Clin Microbiol Infect. 2006, 12: 194-196. 10.1111/j.1469-0691.2005.01284.x.PubMedView ArticleGoogle Scholar
  59. Serafino A, Vallebona PS, Andreola F, Zonfrillo M, Mercuri L, Federici M, Rasi G, Garaci E, Pierimarchi P: Stimulatory effect of Eucalyptus essential oil on innate cell-mediated immune response. BMC Immunol. 2008, 9: 17-10.1186/1471-2172-9-17.PubMed CentralPubMedView ArticleGoogle Scholar
  60. Abd El-Motaal AM, Ahmed AMH, Bahakaim ASA, Fathi MM: Productive performance and immunocompetence of commercial laying hens given diets supplemented with Eucalyptus. Int J Poult Sci. 2008, 7: 445-449. 10.3923/ijps.2008.445.449.View ArticleGoogle Scholar
  61. Dierick NA, Decuypere JA, Molly K, Van Beek E, Vanderbecke E: The combined use of triacylglycerols containing medium-chain fatty acids and exogenous lipolytic enzymes as an alternative for nutritional antibiotics in piglet nutrition: I: in vitro screening of the release of MCFAs from selected fat sources by selected exogenous lipolytic enzymes under simulated pig gastric conditions and their effects on the gut flora of piglets. Livest Prod Sci. 2002, 75: 129-142. 10.1016/S0301-6226(01)00303-7.View ArticleGoogle Scholar
  62. Dierick NA, Decuypere JA, Molly K, Van Beek E, Vanderbecke E: The combined use of triacylglycerols containing medium-chain fatty acids and exogenous lipolytic enzymes as an alternative for nutritional antibiotics in piglet nutrition: II: in vivo release of MCFAs in gastric cannulated and slaughtered piglets by endogenous and exogenous lipases: effects on the luminal gut flora and growth performance. Livest Prod Sci. 2002, 76: 1-16. 10.1016/S0301-6226(01)00331-1.View ArticleGoogle Scholar
  63. Hong SM, Hwang JH, Kim IH: Effect of medium-chain triglyceride (MCT) on growth performance, nutrient digestibility, blood characteristics in weanling pigs. Asian-Aust J Anim Sci. 2012, 25: 1003-1008. 10.5713/ajas.2011.11402.View ArticleGoogle Scholar
  64. Rossi R, Pastorelli G, Cannata S, Corino C: Recent advances in the use of fatty acids as supplements in pig diets: a review. Anim Feed Sci Technol. 2010, 162: 1-11. 10.1016/j.anifeedsci.2010.08.013.View ArticleGoogle Scholar
  65. Han YK, Hwang UH, Thacker PA: Use of a micro-encapsulated medium chain fatty acid product as an alternative to zinc oxide and antibiotics for weaned pigs. J Swine Health Prod. 2011, 19: 34-43.Google Scholar
  66. Redling K: Rare earth elements in agriculture with emphasis on animal husbandry. 2006, Muenchen: Diss Ludwig-Maximilians-Universitaet, 325.Google Scholar
  67. Zhu X, Li D, Yang W, Xiao C, Chen H: Effects of rare earth elements on the growth and nitrogen balance of piglets. Feed Industry. 1994, 15: 23-25.Google Scholar
  68. He R, Xia Z: Effects of rare earth elements on growing and fattening of pigs. Guangxi Agric Sci. 1998, 5: 243-245.Google Scholar
  69. Rambeck WA, Wehr U: Rare earth elements as alternative growth promoters in pig production. Arch Tierernahr. 2000, 53: 323-334. 10.1080/17450390009381956.PubMedView ArticleGoogle Scholar
  70. He ML, Rambeck WA: Rare earth elements: a new generation of growth promoters for pigs. Arch Anim Nutr. 2000, 53: 323-334.Google Scholar
  71. He ML, Ranz D, Rambeck WA: Study on the performance enhancing effect of rare earth elements in growing and finishing pigs. J Anim Physiol Anim Nutr. 2001, 85: 263-270. 10.1046/j.1439-0396.2001.00327.x.View ArticleGoogle Scholar
  72. Kraatz M, Taras D, Manner K, Simon O: Weaning pig performance and faecal microbiota with and without in-feed addition of rare earth elements. J Anim Physiol Anim Nutr. 2006, 90: 361-368. 10.1111/j.1439-0396.2005.00594.x.View ArticleGoogle Scholar
  73. Han YK, Thacker PA: Effect of antibiotics, zinc oxide and rare earth mineral yeast on performance, nutrient digestibility and blood parameters in weaned pigs. Asian-Aust J Anim Sci. 2010, 23: 1057-1065. 10.5713/ajas.2010.90569.View ArticleGoogle Scholar
  74. Buhler M, Limper J, Muller A, Schwarz G, Simon O, Sommer M, Spring W: Enzymes in animal nutrition. 2013, German Feed Additives Association Fact Sheet, Available at http://www.awt-feedadditives.de/Publikationen/Enzymbro-engl.pdfGoogle Scholar
  75. Choct M: Feed non-starch polysaccharides: chemical structures and nutritional significance. 1997, Singapore: Proceedings of the Feed Ingredients Asia 97 ConferenceGoogle Scholar
  76. Metzler B, Bauer B, Mosenthin R: Microflora management in the gastrointestinal tract of piglets. Asian-Aust J Anim Sci. 2005, 18: 1353-1362.View ArticleGoogle Scholar
  77. Kiarie E, Nyachoti CM, Slominski BA, Blank G: Growth performance, gastrointestinal microbial activity, and nutrient digestibility in early-weaned pigs fed diets containing flaxseed and carbohydrase enzyme. J Anim Sci. 2007, 85: 2982-2993. 10.2527/jas.2006-481.PubMedView ArticleGoogle Scholar
  78. Emiola IA, Opapeju FO, Slominski BA, Nyachoti CM: Growth performance and nutrient digestibility in swine fed wheat distillers dried grains with solubles-based diets supplemented with a multi-carbohydrase enzyme. J Anim Sci. 2009, 87: 2315-2322. 10.2527/jas.2008-1195.PubMedView ArticleGoogle Scholar
  79. Thacker PA: Effect of enzyme supplementation on the performance of growing-finishing pigs fed barley based diets supplemented with soybean meal or canola meal. Asian-Aust J Anim Sci. 2001, 14: 1008-1013.View ArticleGoogle Scholar
  80. Olukosi OA, Sands JS, Adeola O: Supplementation of carbohydrases or phytase individually or in combination to diets for weanling and growing-finishing pigs. J Anim Sci. 2007, 85: 1702-1711. 10.2527/jas.2006-709.PubMedView ArticleGoogle Scholar
  81. Jones CK, Bergstrom JR, Tokach MD, DeRouchey JM, Goodband RD, Nelssen JL, Dritz SS: Efficacy of commercial enzymes in diets containing various concentrations and sources of dried distillers grains with solubles for nursery pigs. J Anim Sci. 2010, 88: 2084-2091. 10.2527/jas.2009-2109.PubMedView ArticleGoogle Scholar
  82. Baas TC, Thacker PA: Impact of gastric pH on dietary enzyme activity and survivability in swine fed β-glucanase supplemented diets. Can J Anim Sci. 1996, 76: 245-252. 10.4141/cjas96-036.View ArticleGoogle Scholar
  83. Thacker PA, Baas TC: Effect of gastric pH on the activity of exogenous pentosanase and the effect of pentosanase supplementation of the diet on the performance of growing-finishing pigs. Anim Feed Sci Technol. 1996, 63: 187-200. 10.1016/S0377-8401(96)01028-0.View ArticleGoogle Scholar
  84. He J, Yin J, Wang L, Yu B, Chen D: Functional characterization of a recombinant xylanase from Pichia pastoris and effect of the enzyme on nutrient digestibility in weaned pigs. Brit J Nutr. 2010, 103: 1507-1513. 10.1017/S0007114509993333.PubMedView ArticleGoogle Scholar
  85. Lv JN, Chen YQ, Guo XJ, Piao XS, Cao YH, Dong B: Effects of supplementation of β-mannanase in corn-soybean meal diets on performance and nutrient digestibility in growing pigs. Asian-Aust J Anim Sci. 2013, 26: 579-587. 10.5713/ajas.2012.12612.View ArticleGoogle Scholar
  86. Cai H, Shi P, Luo H, Bai Y, Huang H, Yang P, Yao B: Acidic β-mannanase from penicillium pinophilum C1: cloning, characterization and assessment of its potential for animal feed application. J Biosci Bioeng. 2011, 112: 551-557. 10.1016/j.jbiosc.2011.08.018.PubMedView ArticleGoogle Scholar
  87. Pettey LA, Carter SD, Senne BW, Shriver JA: Effect of beta-mannanase adding to corn-soybean meal diets on growth performance, carcass traits and apparent nutrient digestibility in growing-finishing pigs. J Anim Sci. 2002, 80: 1012-1019.PubMedGoogle Scholar
  88. Van Dijk AJ, Everts H, Nabuurs MJA, Margry RJ, Beynen AC: Growth performance of weanling pigs fed spray-dried animal plasma: a review. Livest Prod Sci. 2001, 68: 263-274. 10.1016/S0301-6226(00)00229-3.View ArticleGoogle Scholar
  89. Torrallardona D: Spray dried animal plasma as an alternative to antibiotics in weanling pigs: a review. Asian-Aust J Anim Sci. 2010, 23: 131-148.View ArticleGoogle Scholar
  90. Bontempo V, Di Giancamillo A, Savoini G, Dell’Orto V, Domeneghini C: Live yeast supplementation acts upon intestinal morpho-functional aspects and growth in weanling piglets. Anim Feed Sci Technol. 2006, 129: 224-236. 10.1016/j.anifeedsci.2005.12.015.View ArticleGoogle Scholar
  91. Li JY, Li DF, Gong LM, Ma YX, He YH, Zhai HX: Effects of live yeast on the performance, nutrient digestibility, gastrointestinal microbiota and concentration of volatile fatty acids in weanling pigs. Arch Anim Nutr. 2006, 60: 277-288. 10.1080/17450390600785343.PubMedView ArticleGoogle Scholar
  92. Shen YB, Piao XS, Kim SW, Wang L, Liu P, Yoon I, Zhen YG: Effects of yeast culture supplementation on growth performance, intestinal health, and immune response of nursery pigs. J Anim Sci. 2009, 87: 2614-2624. 10.2527/jas.2008-1512.PubMedView ArticleGoogle Scholar
  93. Yan L, Han DL, Meng QW, Lee JH, Park CJ, Kim IH: Effects of anion supplementation on growth performance, nutrient digestibility, meat quality and fecal noxious gas content in growing-finishing pigs. Asian-Aust J Anim Sci. 2010, 23: 1073-1079. 10.5713/ajas.2010.90609.View ArticleGoogle Scholar
  94. Nyachoti CM, Kiarie E, Bhandari SK, Zhang G, Krause DO: Weaned pig responses to Esherichia coli K88 oral challenge when receiving a lysozyme supplement. J Anim Sci. 2012, 90: 252-260. 10.2527/jas.2010-3596.PubMedView ArticleGoogle Scholar
  95. Huguet A, Le Dividich J, Le Huerou-Luron I: Improvement of growth performance and sanitary status of weaned piglets fed a bovine colostrum-supplemented diet. J Anim Sci. 2012, 90: 1513-1520. 10.2527/jas.2011-3941.PubMedView ArticleGoogle Scholar
  96. Wang Y, Shan T, Xu Z, Liu J, Feng J: Effect of lactoferrin on the growth performance, intestinal morphology and expression of PR-39 and protegrin-1 genes in weaned piglets. J Anim Sci. 2006, 84: 2636-2641. 10.2527/jas.2005-544.PubMedView ArticleGoogle Scholar
  97. Shan T, Wang Y, Liu J, Xu Z: Effect of dietary lactoferrin on the immune functions and serum iron level of weanling piglets. J Anim Sci. 2007, 85: 2140-2146. 10.2527/jas.2006-754.PubMedView ArticleGoogle Scholar
  98. Garcia-Montoya IA, Cendon TS, Arevalo-Gallegos S, Rascon-Cruz Q: Lactoferrin a multiple bioactive protein: an overview. Biochim Biophys Acta. 1820, 2012: 226-236.Google Scholar
  99. Lai CH, Yin JD, Li DF, Zhao LD, Qiao SY, Xing JJ: Conjugated linoleic acid attenuates the production and gene expression of pro-inflammatory cytokines in weaned pigs challenged with lipopolysaccharide. J Nutr. 2005, 135: 239-244.Google Scholar
  100. Lai CH, Yin JD, Li DF, Zhao LD, Chen XJ: Effects of dietary conjugated linoleic acid supplementation on the performance and immunological responses of weaned pigs after an escherichia coli lipopolysaccharide challenge. J Anim Vet Adv. 2005, 2: 299-305.Google Scholar
  101. Liu P, Piao XS, Thacker PA, Zheng ZK, Wong D, Kim SW: Chito-oligosaccharide reduces diarrhea incidence and attenuates the immune response of weanling pigs challenged with E. coli K88. J Anim Sci. 2010, 88: 3871-3879. 10.2527/jas.2009-2771.PubMedView ArticleGoogle Scholar
  102. Liu P, Piao XS, Kim SW, Li XJ, Wang L, Shen YB, Lee HS, Li SY: Effects of chito-oligosaccharide supplementation on the growth performance, nutrient digestibility, intestinal morphology, and fecal shedding of Escherichia coli and Lactobacilli in weaning pigs. J Anim Sci. 2008, 86: 2609-2618. 10.2527/jas.2007-0668.PubMedView ArticleGoogle Scholar
  103. O’Doherty JV, Dillon S, Figat S, Callan JJ, Sweeney T: The effects of lactose inclusion and seaweed extract derived from Laminaria spp. on performance, digestibility of diet components and microbial populations in newly weaned pigs. Anim Feed Sci Technol. 2010, 157: 173-180. 10.1016/j.anifeedsci.2010.03.004.View ArticleGoogle Scholar

Copyright

© Thacker; licensee BioMed Central Ltd. 2013

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Advertisement