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J. Anim Sci. 2008. 86:94-101. doi:10.2527/jas.2005-686
© 2008 American Society of Animal Science
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ANIMAL NUTRITION

Use of mannanoligosaccharides and zinc chelate as growth promoters and diarrhea preventative in weaning pigs: Effects on microbiota and gut function1

M. Castillo*, S. M. Martín-Orúe*,2, J. A. Taylor-Pickard{dagger}, J. F. Pérez* and J. Gasa*

* Animal Nutrition, Management and Welfare Research Group, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain; and {dagger} Alltech, Alltech Biotechnology Centre, Sarney, Summerhill Road, Dunboyne, Co. Meath, Ireland


   Abstract
Top
 Abstract
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The efficacy of a commercial source of mannanoligosacharides (BM), organic zinc (BP), or their combination to enhance performance, gastrointestinal health, and immune response in weaned pigs was evaluated. A total of 128 piglets, weaned at 20 ± 2 d, were housed in 32 pens. Animals received 1 of 4 dietary treatments: a control diet (CT) to which 0.2% of BM, 80 mg/kg of Zn as BP, or both additives (BMP) were added. The experiment lasted for 5 wk including a prestarter period of 2 wk and a starter period of 3 wk. Body weight was recorded and daily feed intake was calculated. Fecal consistency was monitored for the first 21 d. After 2 wk, 32 animals were killed, digesta samples from the stomach, ileum, and cecum were collected, and pH and the short-chain fatty acid profile were determined. Microbiological counts for enterobacteria and lactobacilli were evaluated using quantitative PCR. Histological parameters in the jejunum and immunoglobulin concentrations in serum and ileal digesta were also measured. Both additives improved G:F during the starter period (0.63, 0.69, 0.67, and 0.68 for CT, BM, BP, and BMP, respectively; P < 0.04). Mean fecal score values for the first 21 d were improved by BM and BP, showing decreased values compared with the CT diet (1.22, 0.89, 0.87, and 1.06 for CT, BM, BP, and BMP, respectively; P = 0.002). The addition of BM decreased enterobacteria counts in the jejunum (9.13, 8.05, 8.87, and 7.89 log 16S rRNA gene copies/g of matter for CT, BM, BP, and BMP, respectively; P = 0.05). Empty ileal weight, defined as the segment including the continuous Peyer’s patch, tended (P = 0.08) to increase with BP treatment (8.9, 9.6, 11.9, and 10.3 g/kg of BW for CT, BM, BP, and BMP, respectively). Crypt depths in the jejunum were lower in animals fed the combination of the additives (BPM) compared with those fed the control diet (281 vs. 235; P < 0.03). No significant differences were registered in pH, short-chain fatty acids, or serum and ileal immunoglobulin concentrations. The results suggest that the use of BM or BP can improve the efficiency of gain during the starter period.

Key Words: Bio-Mos • Bioplex Zn • growth performance • mannanoligosaccharides • organic zinc • postweaning diarrhea


   INTRODUCTION
Top
 Abstract
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Reducing postweaning diarrhea is one of the main challenges for the pig industry. In commercial practice, the use of different additives has been recommended as a way to help the piglet during this stage. Among these agents, mannanoligosaccharides (MOS) and Zn have been demonstrated to have positive effects on pig health.

Bio-Mos (Alltech Inc., Nicholasville, KY) is a mannanoligosaccharide derived from the outer cell wall of a selected strain of yeast (Miguel et al., 2004Go). Research suggests that BioMos interferes with bacterial attachment to the epithelial cell (Spring et al., 2000Go) and can enhance immunity (Newman and Newman, 2001Go; O’Quinn et al., 2001Go). Zinc oxide (ZnO) at pharmacological concentrations (2,000 to 3,000 mg/kg) has been reported to reduce diarrhea during weaning (Poulsen, 1995Go) and it is used in nursery diets as a growth promotant (although its mode of action is not entirely clear). Various studies suggest that Zn action could be mediated by a luminal (Katouli et al., 1999Go) or an intestinal (Carlson et al., 1999Go) effect. It has also been speculated that Zn could act by systemic effect within the body (Case and Carlson, 2002Go). Recently, Davis et al. (2002)Go studied the possible synergistic effect when high levels of ZnO are combined with BioMos. However, the use of high doses of inorganic Zn has raised concern due to elevated Zn in feces when fed for more than 10 d (Rincker et al., 2005Go). If the mode of action of Zn is based on a systemic effect, an organic form of Zn with greater bioavailability would allow reduced concentration in feed and subsequent release in the environment while maintaining benefits to the animals.

The main objective of this work was to evaluate the efficacy of a source of mannanoligosacharides (Bio-Mos), organic zinc (Bioplex Zn, Alltech Inc.), or their combination to enhance growth performance, gastrointestinal health, and immune response in weaned pigs.


   MATERIALS AND METHODS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
The experiment was carried out on the Experimental Farms of the Universitat Autònoma de Barcelona in Spain and received prior approval from the Animal Protocol Review Committee of this institution.

Animals and Diets

A total of 128 weaned pigs [Pietrain x (Large White x Landrace), 66 males and 62 females] were selected from a commercial herd. The animals were weaned between 18 and 22 d of age with an average initial BW of 6.7 ± 1.17 kg. Pigs were free of the principal swine infectious agents at the beginning and end of the study. Agents evaluated included porcine circovirus type 2, porcine parvovirus, porcine respiratory and reproductive syndrome virus, swine influenza virus, Aujeszky’s disease virus, Mycoplasma hyopneumoniae, and Law-sonia intracellularis.

The animals were housed in 32 pens (4 pigs/pen) taking litter and initial BW into account. The dietary treatments were: 1) a control diet formulated to meet the NRC (1998)Go requirements (CT); 2) CT plus 0.2% BioMos (BM; Alltech Inc.); 3) CT plus 80 mg/kg of organic Zn as Bioplex Zn (BP; Alltech Inc.); or 4) CT plus 0.2% BioMos and 80 mg/kg Zn as Bioplex Zn (BMP). Inclusion levels are on an as-fed basis. No medication or other additives were included in any of the diets.

The 5-wk experiment included a prestarter period (2 wk) and a starter period (3 wk). Diets (Table 1Go) were slightly modified according to the requirements of the animals, but maintained constant levels of BM and organic Zn. Animals were allowed ad libitum access to feed and water.


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  		Table 1. Composition of prestarter and starter control diets, as-fed basis
 
To assess the usefulness of the additives tested to prevent disorders associated with environmental stress, animals were challenged by a controlled stress before the starter period. Stress consisted of lowering the room temperature from 27 to 17°C with feed deprivation for 10 h.

Performance and Collection Procedures

The BW and feed disappearance were recorded weekly and used to calculate ADFI, ADG, and G:F.

Two persons, blinded to treatments, scored fecal consistency daily for the first 3 wk. The fecal scoring was classified using a scale ranking from 0 to 3, with 0 = normally shaped feces, 1 = shapeless feces, 2 = soft feces, and 3 = thin, liquid feces.

On d 14, 32 pigs (1 per pen) were killed with an i.v. injection (200 mg/kg of BW) of sodium pentobarbital (Dolethal, Vetoquinol, S.A., Madrid, Spain). The pigs selected from each pen were those with individual BW closest to the mean pen BW. Blood samples for immunoglobulin analysis were taken from the jugular vein before euthanization. After that, animals were completely bled, the abdomen was immediately opened, and the gastrointestinal tract was tied at the esophageal orifice of the stomach, pylorus, ileocecal valve, and rectum, and excised. Empty weight of the small intestine and ileum were recorded. Lengths of the small intestine and ileum were also recorded. The ileum was considered as the terminal section of the small intestine containing the continuous Peyer’s patches. Samples for histology were taken from the distal jejunum and transferred to 10% neutral buffered formaldehyde.

Digesta from the stomach, ileum, and cecum were homogenized and their pH was determined. Samples (approximately 5 g) were quick frozen (–20°C) until analyzed for short-chain fatty acids (SCFA). Digesta samples from the ileum, cecum, and rectum were also frozen (–20°C) and lyophilized until analyzed for purine bases (PB). Samples of jejunal digesta (approximately 1 g) were taken and preserved in ethanol for DNA extraction and posterior microbiological studies (Castillo et al., 2006Go).

Analytical Methods

SCFA Analysis. Analysis of SCFA was performed by GLC using the method of Richardson et al. (1989)Go, as modified by Jensen et al. (1995)Go.

PB Analysis. Purine bases (adenine and guanine) in lyophilized digesta samples (40 mg) were determined by HPLC (Makkar and Becker, 1999Go). For the analysis, PB were hydrolyzed from the nucleic acid chain following incubation of the digesta samples with 2 mL of 2 M HClO4 at 100°C for 1 h, and including 0.5 mL of 1 mM allopurinol as an internal standard.

Immunoglobulins. The concentration of IgA, IgG, and IgM in serum was quantified using the pig IgA, IgG, and IgM ELISA Quantitation Kits (Bethyl Laboratories, Inc., Montgomery, TX). Serum was obtained from blood collected into nonheparinized evacuated tubes. Immediately after blood collection, serum was obtained from each sample after centrifugation at 2,000 x g for 15 min. For the determination of IgA in ileum digesta samples, the method of Swanson et al. (2002)Go was used. Samples (2 g) were lyophilized and crushed with a mortar before being placed into an Erlenmeyer flask along with 20 mL of PBS solution, pH 7.2. Samples were mixed for 30 min at room temperature and centrifuged at 20,000 x g for 30 min. The supernatant was collected and ileal Ig concentrations were determined using the same kits used for the serum samples. For calculation of Ig concentration, CP was determined in ileum digesta as total N following the Kjeldahl method (AOAC, 1990Go).

DNA Extraction. Digesta samples (400 mg) preserved in ethanol (3 mL, 96%) were precipitated by centrifugation (13,000 x g for 5 min), and DNA from the precipitate was extracted and purified using the commercial QIAamp DNA Stool Mini Kit (Qiagen, West Sussex, UK). The recommended lysis temperature was increased to 90°C, and an incubation step with lysozyme (Sigma-Aldrich Química S. A., Madrid, Spain) was added (10 mg/mL, 37°C, 30 min) to improve bacterial cell rupture. The DNA was eluted in 200 µL of Qiagen Buffer AE and stored at –80°C.

Quantitative PCR. Microbial populations of enterobacteria and lactobacilli in jejunum digesta samples were quantified by real-time PCR using SyBR Green chemistry (SYBR Green PCR Core Reagents kit, PE Biosystems, Foster City, CA) following the procedures of Castillo et al. (2006)Go. Amplification and detection of DNA by real-time PCR were performed with the ABI 7900 HT Sequence Detection System (PE Biosystems, Warrington, UK) using optical-grade 96-well plates.

Histological Analysis. Formalin-fixed samples were embedded in paraffin and slides were processed for the periodic acid-Schiff reaction. For each sample, villus height and crypt depth were measured. The goblet cells in the villi and crypts were also counted. All measurements were made in 10 well-oriented villi and crypts from each jejunum wall sample, and the average value was used. Measurements were done using a linear micrometer ocular (Olympus, 209–35040, Microplanet, Barcelona, Spain). Villus height was represented by the distance from the crypt opening to the top of the villus. Crypt depth was determined from the base of the crypt to the level of the crypt opening. The villus height:crypt depth ratio was calculated.

Statistical Analysis

The effect of diet on different parameters was tested with an ANOVA using the GLM procedure (SAS Inst. Inc., Cary, NC). For performance analyses, the pen was used as the experimental unit using initial BW as a covariate. Fecal consistency was also analyzed by pen including the effect of sampling day in the model. The effect of sampling day was analyzed as repeated measures using the MIXED procedure of SAS. For other data, the pig was the experimental unit. When treatment effects were established (P < 0.05), treatment least squares means were separated using the PDIFF function with the Tukey-Kramer adjustment.


   RESULTS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Growth Performance

Results for BW, ADG, ADFI, and G:F are shown in Table 2Go. Average daily gains and ADFI were not affected by treatment (P > 0.71). The G:F was improved by the addition of BioMos and Bioplex Zn compared with the pigs fed the CT diet during the starter period (P = 0.04). For the 5-wk trial, pigs fed BM and BMP had improved (P < 0.05) G:F compared with CT pigs.


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  		Table 2. Initial and final BW, ADFI, ADG, and G:F of weaned pigs
 
Fecal Consistency

Fecal consistency was scored during the first 3 wk postweaning (Figure 1Go). There was an increase in fecal inconsistency from d 0 to d 4 for all of the diets (P = 0.001). During d 7, pigs consuming BM and BP showed lower fecal score values compared with CT; however, pigs receiving both additives did not show differences (1.43, 0.38, 0.71, and 1.63 for CT, BM, BP, and BMP, respectively; P = 0.02). For the entire period, fecal score was improved by BM and BP compared with CT (1.22, 0.89, 0.87, and 1.06 for CT, BM, BP, and BMP respectively; P = 0.002).


Figure 1
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  		Figure 1. Fecal consistency in pigs receiving a control diet (CT), or the same diet supplemented with 0.2% BioMos (BM), 80 mg/kg of Zn as Bioplex-Zn (BP), or both additives (BMP) during the initial 21 d postweaning (0 = normally shaped feces, 1 = shapeless feces, 2 = soft feces, and 3 = thin, liquid feces). Values represent means ± SEM. Different letters in the same sampling day denote significant differences between diets. P-values for day, diet, and day x diet, as well as SEM values are from the ANOVA for the overall 21-d period.

 
Intestinal Weight and Length

Experimental diets did not affect weight or length of the whole intestine (data not shown). However, the empty ileal weight tended (P = 0.08) to increase with BP treatment resulting in the greatest ileal weights (8.91, 9.56, 11.92, and 10.34 g for CT, BM, BP, and BMP, respectively).

SCFA

The pH was not affected by the experimental diets in any of the gastrointestinal sections (data not shown; 3.2 ± 0.29, 6.7 ± 0.11, and 5.7 ± 0.14 for stomach, ileum and cecum, respectively). Total SCFA including acetate, propionate, butyrate, valerate, and branched-chain fatty acids did not show differences between diets (data not shown; 7.9 ± 1.05, 12.5 ± 2.01, and 134.4 ± 7.49 µmol/g of DM for stomach, ileum, and cecum, respectively). Lactate concentration was also similar among treatments (4.1 ± 0.59, 13.6 ± 3.85, and 3.7 ± 1.65 µmol/g of DM for stomach, ileum, and cecum, respectively).

Quantitative Changes in Microbial Population

The concentration of purine bases in the ileum, cecum, and rectum digesta, as an estimate of the total microbial population size and activity, are shown in Table 3Go. Purine base concentration increased from the ileum to the cecum, without differences (P ≥ 0.19) due to diet (6.46, 47.65, and 35.04 µmol/g of DM for ileum, cecum, and rectum, respectively).


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  		Table 3. Purine bases concentration (µmol/g of DM), in the ileum cecum and rectum, and bacterial populations of lactobacilli and enterobacteria (log 16S rRNA gene copies/g of fresh matter) and their ratio (Lact:Entero, as difference of logarithms) from the distal jejunum measured by real-time PCR in pigs at 14 d postweaning
 
Lactobacilli counts in jejunum digesta did not differ among diets, but there was a decrease in enterobacteria numbers for pigs fed BM and BMP diets compared with pigs fed the CT diet (P < 0.05). Expressed as a ratio of lactobacilli:enterobacteria, the BMP diet promoted the highest ratio compared with CT (P = 0.03).

Immune Proteins and Intestinal Morphology

Serum concentrations of IgG, IgM, and IgA, ileal concentration of IgA, and histological measurements of the distal jejunum are presented in Table 4Go. No differences due to diet were detected in the serum concentration of the immunoglobulins, ileal IgA, or in the number of intraepithelial lymphocytes or goblet cells in the jejunum. However, crypt depth was less in pigs fed BMP diet compared with pigs fed the control diet (P < 0.04). The villus height was not affected; therefore, the villus height:crypt depth ratio was affected (P < 0.05) by the BMP diet compared with pigs fed the other diets.


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  		Table 4. Serum and ileal immunoglobulin concentrations and jejunum histological parameters of pigs 14 d postweaning
 

   DISCUSSION
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Studies have reported that BM supplementation during the postweaning phase improves growth performance of pigs (Dvorak and Jacques, 1998Go; Davis et al., 2002Go, 2004aGo). Recently, a meta-analysis of 54 different experiments in nursery pigs fed BioMos demonstrated a 4.12% improvement in ADG, a 2.11% improvement in ADFI, and an increase in G:F of 2.29% (Miguel et al., 2004Go). Carlson et al. (2004)Go did not demonstrate improvements in growth performance when nursery pigs fed different sources of organic Zn (Zn-polysaccharide or Zn-proteinate as Bioplex Zn). However, other studies demonstrated improvements after the inclusion of Bioplex Zn in young pigs’ diets (Mullan et al., 2002Go, 2004Go). In this study BM or BP dietary additions increased G:F compared with control. This improvement was manifested during the starter period. We did not detect any significant improvement in growth performance with the addition of both additives compared with the additives alone. Le Mieux et al. (2003)Go, in a series of experiments, evaluated BM and ZnO supplementation in nursery pigs and found inconsistent results. Other authors (Davis et al., 2004bGo) did not show any synergistic responses to pharmacological concentrations of Zn and phosphorylated mannans.

Changes in Microbial Ecosystem

Mannanoligosaccharides have been proposed to promote growth by modifying the gastrointestinal ecosystem and reducing intestinal pathogen colonization (Newman, 1994Go; Spring, 2004Go). In poultry, it appears that MOS attach to mucosa-binding proteins on the cell surface of some bacteria, preventing colonization of intestinal epithelium (Spring et al., 2000Go). In this study, we showed a reduction in the enterobacteria population in pigs fed diets supplemented with BM (BM and BMP diets) compared with the BP and CT diets. Likewise, White et al. (2002)Go showed a lower concentration of coliforms in the feces of pigs fed diets with MOS. The decline in enterobacteria numbers is important because of their relationship to outbreaks of postweaning diarrhea (Melin, 2001Go). The ratio of lactobacilli:enterobacteria has routinely been used as an indicator of gut health (Muralidhara et al., 1977Go), with an increase in the ratio considered beneficial for gut health (Ewing and Cole, 1994Go). An inhibition of enterobacteria could prevent or decrease the severity of diarrhea that appears after weaning (Melin et al., 2004Go).

Changes in bacterial populations were not reflected in fermentation patterns that were unaffected by the experimental diets. Mannanoligosaccharides do not always modify fecal pH or SCFA concentration in weaning pigs (White et al., 2002Go) and dogs (Swanson et al., 2002Go). Although nondigestible fermentable oligosaccharides such as fructooligosaccharides are considered SCFA-promoting compounds (Kaplan and Hutkins, 2000Go), their low inclusion rate in the diet compared with other nondigested carbohydrates such as resistant starch or nonstarch polysaccharides of cereals or nondigestible oligosaccharides of soy probably preclude their potential to promote different fermentation patterns.

Katouli et al. (1999)Go reported that pharmacological ZnO increased the stability of the intestinal microflora through a reduction in the diversity of coliform species but without quantitative effect in the total number of coliforms. No effect on coliform populations was reported by Jensen-Waern et al. (1998)Go using 2,500 mg/kg of ZnO in weanling pig with no effects on Escherichia coli and enterococci in feces. This lack of a direct effect on specific bacterial populations with pharmacological concentrations of Zn from ZnO make it difficult to consider that organic sources of Zn at lower concentration may directly affect intestinal microbiota.

Effects on Intestinal Morphology and Gut Function

The weaned piglet has to adjust to challenges from antigens associated with new feed and the establishment of intestinal flora. Facultative pathogens, previously controlled by maternal IgA, can expand and colonize the gut (Kelly and King, 2001Go). The maintenance of intestinal integrity and the digestive and absorptive function during the weaning period depend on the ability of the immune system to adapt to it (Bailey et al., 2001Go). Microorganisms or new feed proteins are associated with an atrophy of intestinal villi, which results in increased turnover of crypt cells with reduced villi height:crypt depth ratio (Miller et al., 1986Go).

Similar to the results reported here, Ferket (2002)Go showed that adding 0.1% BioMos to broilers did not affect villus height, but promoted a decrease in crypt depth and a lower villi height:crypt depth ratio. Iji et al. (2001)Go also observed an increase in this ratio in poultry, but due to a significant increase in villi height rather than an effect on crypt depth. This beneficial effect of BioMos on intestinal morphology may be due to a reduction in the enterobacteria population, but could also be due to other mechanisms. Ferket (2002)Go proposed an increase in the production of the mucus gel layer promoted by BioMos as another mode of action of MOS. However, the current experiment did not detect any increase in the number of goblet cells responsible for the production of mucus on villi or crypts.

O’Quinn et al. (2001)Go reported increased IgA titers in sow’s milk, and Davis et al. (2004b)Go reported an alteration in the leukocyte populations in piglets fed BioMos. Swanson et al. (2002)Go showed greater concentration of IgA in the ileal digesta of dogs receiving MOS and fructoligosaccharides in the diet, but not MOS alone. Other studies with rats (Kudoh et al., 1999Go) have shown an increase in fecal IgA concentrations in rats supplemented with MOS. Secretory IgA can be regulated by the presentation of bacterial antigens in the gut and is important for mucosal immunity because it inhibits the attachment and penetration of bacteria and toxins into the lumen (McKay and Perdue, 1993Go). The prevention of the onset of an acute-phase immune response, by modulating the immune system, has a profound impact on growth performance. No immunological parameters included in this study responded significantly to the inclusion of BM; however, it is possible that these broad indexes are not sensitive to subtle effects on immune response.

Regarding potential effects of supplemental Zn on intestinal morphology and gut function, Li et al. (2001)Go reported an increased villus height and reduced crypt depth in pigs feeding with high levels of dietary zinc. Other authors (Carlson et al., 1999Go) have described increased concentrations of metallothionein (MT) in intestinal mucosa cells of weaned pigs in response to ZnO supplementation. Considering the role of Zn in RNA-DNA cell proliferation, and relevance of MT in Zn homeostasis, an increase in cell proliferation and protein synthesis promoted by supplementary Zn may explain the increase observed in villus:crypt ratio. Similar results were shown by Carlson and Poulsen (2003)Go, who demonstrated that mucosal MT increased when ZnO was supplemented to piglets. In addition to an increased proliferative activity in mucosa, an improvement of the development of the immune response is also a potential mode of action. We did not find significant differences in the serum immunoglobulins related to diets. However, it is interesting to note that, although differences did not reach statistic significance (P = 0.08), animals fed organic zinc had greater mean weight of empty ileum containing continuous Peyer’s patches, which may indicate a greater development of this immunological organ.

The use of BioMos and Bioplex Zn improved G:F in the starter period. Effects appear to be due to different modes of action. BioMos decreased jejunal numbers of enterobacteria, and Bioplex Zn tended to increase the weight of the ileum containing Peyer’s patches (P = 0.08). Complementarity of both additives was manifested by a significant increase in villus:crypt ratio only when both additives were included in the feed.


   Footnotes
 
1 Acknowledgment: Appreciation is expressed to Allech Biotechnology Centre, Ireland, for financial support. Back

2 Corresponding author: susana.martin{at}uab.es

Received for publication November 24, 2005. Accepted for publication September 24, 2007.


   LITERATURE CITED
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 


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