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Department of Animal Science, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada
2 Correspondence—phone:
204-474-7323; fax: 204-474-7628; E-mail:
martin_nyachoti{at}Umanitoba.ca.
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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Key Words: Antibiotics • Antibodies • Diarrhea • Fumaric Acid • Pigs • Zinc Oxide
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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A major challenge currently facing the swine industry is to identify means for controlling diarrhea in young pigs that are not only cost effective, but also suitable for sustainable pork production. Thus far, various strategies, including use of in-feed antibiotics (Hays, 1986), spray-dried plasma proteins (SDPP) (Godfredson-Kisk and Johnson, 1997; Gomez et al., 1998), pro- and prebiotics (Stavric and Kornegay, 1995), organic acids (Paulicks et al., 1996), and zinc and copper salts (Carlson et al., 1999; Mavromichalis et al., 2000), have been tried with mixed results. Furthermore, serious concerns, such as antibiotic resistance, associated with use of in-feed antibiotics (Mathew et al., 1998), animal proteins in feed (Orr and Powell, 2001) and environmental implications of excess zinc and copper (Windisch, 2000) have been raised regarding the use of some of these products.
Egg yolk antibodies (EYA) from laying hens hyperimmunized with specific bacterial fimbrial antigens have been proposed as an effective means for controlling diarrhea in early weaned pigs (Yokoyama et al 1992; Kim et al., 1999). However, little is known about the efficacy of EYA relative to conventional alternatives. Therefore, the primary objective of the current study was to assess the effectiveness of EYA in controlling ETEC relative to conventional additives in early weaned pigs fed pea protein isolate (PPI)-based diets.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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The experimental protocol was approved by the University of Manitoba Animal Care Committee and pigs were cared for according to the guidelines of Canadian Council on Animal Care (CCAC, 1993). A total of 90 piglets weaned at 10 ± 1 d of age (3.8 ± 0.1 kg initial BW) and balanced for initial BW and litter origin were used in a 14-d trial. Piglets were randomly allotted to each of six dietary treatments in a completely randomized design. Each treatment was assigned to five pens each with three pigs. Room temperature was maintained at 31 ± 1°C throughout the study.
Diets, Feeding, and Experimental Procedure
Pea protein isolate and SDPP were obtained from Parrheim Foods (Portage La Prairie, MB, Canada) and Farmlands Proteins Plant (Maquoketa, IA), respectively. Egg yolk antibodies were produced in our laboratory as described previously (Marquardt et al., 1999). The six experimental diets included a SDPP without EYA control (SDPP - EYA) and five PPI-based diets. The PPI-based diets were PPI without EYA (PPI - EYA), PPI with EYA (PPI + EYA), PPI with ZnO (PPI + ZnO), PPI with fumaric acid (PPI + FA), and PPI with carbadox (PPI + AB). The SDPP control and PPI - EYA contained egg yolk powder from hens not immunized with K88 and F18 fimbrial antigens. The specialty ingredients were added at levels similar to those previously proven to be efficacious in the literature with zinc at 2,880 mg/kg, which is similar to the 3,000 mg/kg used by Hahn and Baker (1993), FA at 20 mg/kg (Blank et al., 1999), and carbadox at 55 mg/kg (Hill et al., 2001). The EYA contained 0.3 and 0.2% egg yolk powder containing specific anti-K88 and anti-F18 antibodies, respectively. All experimental diets were formulated to meet NRC (1998) nutrient requirements for piglets weighing 3.0 to 6.0 kg BW (Tables 1
and 2). Pigs had unlimited access to feed and water. The ADG, ADFI, and feed conversion efficiency (gain:feed) were determined. On d 0, 7, and 14, blood samples (10 mL) were collected from all pigs via jugular vein puncture into heparinized vacuum container tubes (Becton Dickinson, Rutherford, NJ), and immediately centrifuged at 2,000 x g for 10 min at 5°C to recover plasma, which were immediately stored at - 20°C until required for plasma urea N (PUN) analysis.
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The pure strain of ETEC expressing the K88 (F4) fimbriae (P97-2554B, serotype O149:K91:F4 [K88]) used in the current study was obtained from the University of Montreal Swine Disease Center (Montreal, QC, Canada). The K88 strain of E. coli was used because it is the leading cause of diarrhea disease in early weaned pigs (Nagy and Fekete, 1999). Primary cultures were grown overnight in tryptic soya broth (TSB, CASO-Bouillon, Mikrobiologie Darmstadt, Germany) at 37°C using 1% inoculum from stocks stored at - 20°C in 30% glycerol. The K88 E. coli strain was prepared as described by Marquardt et al. (1999). Briefly, ETEC K88 was grown overnight in blood agar plate (Atlas Laboratories Co. Ltd., Winnipeg, MB, Canada) at 37°C using 0.2 mL of inoculum from stock. Cells were then washed twice with 2 mL of sterilized saline solution (0.9%, pH 7.2), and then the suspension 1010 cfu/mL (calculated on the basis of optical density established by serial dilution before bacterial cell count) was used for oral challenge. On d 7 of the experiment (17-d-old pigs), each pig received 6 mL of bacterial suspension contained in a syringe attached to polyethylene tube held in the oral cavity. Severity of diarrhea was characterized by using the fecal consistency (FC) score system described by Marquardt et al. (1999). Fecal consistency scoring (0, normal; 1, soft feces; 2, mild diarrhea; 3, severe diarrhea) performed by two trained personnel with no prior knowledge of dietary treatment allocation was used to assess the health status of pigs. The total number of days that signs of scours were present in the pens was determined and is expressed as scouring days.
Histological and Other Measurements
On d 14, three pigs (5.2 ± 0.2 kg BW) per treatment, selected randomly from three of the five pens per treatment, were killed to determine the effect of dietary treatments and oral ETEC challenge on weights of visceral organs and morphology of the gastrointestinal tract. Pigs were held under general anesthesia and killed by an intracardiac injection of sodium pentobarbital (50 mg/kg BW). Stomach, spleen, small intestine, and liver were removed, flushed with ice-cold phenylmethyl sulfonyl fluoride saline (2 L of 0.9% saline, pH 7.4 + 2 mL of 100 mM phenylmethyl sulfonyl fluoride) and 20 mL of digesta each from the stomach and the small intestine was obtained for pH measurement. After blotting organs with an absorbent paper, weight and length (small intestine) were determined, and then 10-cm segments of the jejunum taken at 150 cm from the pyloric junction. Segments were stored in 10% formalin to fix the villous and the crypt for subsequent histological measurement. Six cross sections were obtained from each formalin-fixed segment and processed for histological examination using the standard hematoxylin and eosin method. Villous height was measured from the tip to the crypt-villous junction and crypt depth measured from the crypt-villous junction to the base on 10 well-oriented villi per specimen using a Zeiss photomicroscope equipped with a Sony 3 chip CCD color camera. The images were captured using Empix’s Northern Eclipse Image Processing Software (Empix Imaging, Inc., Mississauga, ON, Canada).
Detection of Antibody Titer
Enzyme-linked immunosorbent assay with purified fimbrial antigen was used to determine anti-K88 (F4), -K99 (F5), -987P (F6), -F41, and -F18 antibody titers in SDPP, PPI, EYA, and all experimental diets using the procedure of Kim et al. (1999). Wells of Microtest III flexible assay plates (Falcon 3911, Immunol 4, Dynatec Laboratories, Chantilly, VA) were coated with 100 µg of the fimbrial antigen suspended in 20 mL of PBS (pH 7.2) at 37°C for 2 h. The plates were washed three times with PBS and Tween 20 (0.5%; PBS-T), and then blocked with 5% (wt/vol) skim milk in PBS at 37°C for 2 h, followed by washing with PBS-T as above. Experimental diets, EYA, and SDPP were prepared by dissolving (suspending) 0.5 g of each sample in 4.5 mL of PBS and the antibody extracted in a reciprocal shaker (Lab-Line Instruments Inc., Melrose Park, IL) for 1 h. The plates were then inoculated with dilutions of samples (100 mg/mL) and kept for 2 h at 37°C. After washing with PBS-T, the plates were incubated with 100 µL of alkaline phosphatase conjugated affinipure rabbit secondary antibody anti-chicken IgY (to detect antibody in chicken egg yolk) or alkaline phosphatase affinipure goat anti-swine IgG (to detect antibody in plasma protein) (Jackson ImmunoResearch Laboratory Inc., West Grove, PA; diluted 1:3,000) depending on the sample and incubated for 2 h at 37°C. The plates were washed three times with PBS-T and 100 µL of enzyme substrate (10% diethanolamine with 0.5 mM MgCl2, pH 9.8) were added to each well and incubated at room temperature for 20 to 30 min. The optical density of the wells was read at 405 nm with a microplate reader (Bio-Rad, model 3550, Richmond, CA). The titer was the dilution of antibody required to give one half of the maximal absorbency reading. Assays at different times were corrected using standard samples containing known K88, K99, F18, 987P, or F41 antibody titers.
Chemical Analyses
All analyses were done in duplicate. All experimental diets were ground through a 1-mm screen (Cyclotec 1093 sample mill, Tecator, Hoganas, Sweden) prior to analysis. Samples were dried in a convection oven at 105°C for 16 h for DM determination, whereas CP (N x 6.25) content was determined using Leco NS 2000 nitrogen analyzer (Leco Corp., St. Joseph, MI). A 100-mg sample was prepared for acid hydrolysis according to AOAC (1984) and analyzed for AA as modified by Mills et al. (1989). The method involved digestion in 4 mL of 6N HCl in vacuo for 24 h at 110°C followed by neutralization with 4 mL (wt/vol) of NaOH and cooling to room temperature. The mixture was then made to 50 mL volume with sodium citrate buffer (pH 2.2). Methionine and cysteine were analyzed as methionine sulfone and cysteic acid, respectively, after oxidation with performic acid. Amino acids were then analyzed using a LK 4151 Alpha analyzer (LKB Biochrom, Cambridge, U.K.). Plasma samples were analyzed for urea nitrogen concentrations according to Crocker (1967) with a standard kit (procedure No. 535, Sigma Diagnostics, St. Louis, MO).
Polymerase Chain Reaction
Fecal swab samples for microbial analysis were collected in duplicate from all pigs using the culture swab transport system (Difco) prior to challenge at 8, 24, and 48 h, and on 7 d post-ETEC challenge. Samples were plated onto TSB, and the PCR procedure described by Sambrook et al. (1989) was used on the individual colonies for the detection of K88 adhesive E. coli. The sense and anti-sense primers that encoded the specific K88 fimbrial gene were used. The PCR was performed in a thermocycler (Techne Genius, model FGENO2TP, Duxford, Cambridge, U.K.) with the following program: 30 cycles of 94°C for 1 min, 50°C for 1 min, 72°C for 2 min, and an extension step at 72°C for 5 min at the end of the cycle. The product of the PCR reaction was then electrophoresed on a 0.8% agarose gel and viewed following exposure to UV light. The resultant PCR product corresponded in size (594 base pairs) to structural subunits of the K88 operon that was selected. The sample was deemed positive for the K88 fimbrial gene when it produced a distinctive band consistent with its expected migration on the agarose gel as determined by comparison with the DNA fragment standards.
Calculations and Statistical Analysis
Villi height and crypt depths were determined by averaging the individual measurements in similarly treated pigs. Mean villi height and crypt depth were obtained by averaging the measurements from three pigs. The ADG was calculated based on surviving pigs. The ADFI was calculated as follows:
Total feed added - feed weighed back/
pidi where pi and di are individual pigs and the number of days in the pen, respectively. Data were analyzed as a completely randomized design using the GLM procedures of SAS (SAS Inst., Inc., Cary, NC). Pen was considered the experimental unit for all parameters measured. When a significant F-value (P < 0.05) for treatment means was observed in the ANOVA, treatments were compared using Duncan’s multiple range-test, and 
2 was used to test PCR, scour scores, and mortality (Cody and Smith, 1991).
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Results and Discussion |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionImplicationsLiterature Cited |
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. All experimental diets had similar nutrient compositions (Table 2). All diets except SDPP - EYA and PPI + EYA contained no specific anti-K88 or anti-F18 antibodies, which confirmed our previous observation that PPI-based diets are devoid of specific ETEC (K88 and F18) antibodies (Marquardt et al., 2001; Table 1). Thus, the only differences between the diets used in the study was either the presence or absence of specific anti-ETEC antibodies and the type of "anti-microbial agent" (ZnO, fumaric acid, or carbadox). Piglet Performance
Treatment effects on ADG, ADFI, and gain:feed ratio during wk 1 (prechallenge), wk 2 (postchallenge), and overall (d 0 to 14) are presented in Table 3. The ADG for piglets fed diets containing SDPP - EYA, PPI - EYA, PPI + EYA, PPI + ZnO, PPI + FA, and PPI + AB were not different (P < 0.05) during all three phases.
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). During wk 1 and the overall trial period, pigs fed diets containing SDPP - EYA, PPI + EYA, PPI + ZnO, PPI + FA, and PPI + AB had only numerically better (P < 0.05) ADFI than those fed the PPI - EYA-based diet. There were no differences in gain:feed ratio among dietary treatments (P > 0.05; Table 3). The current results are in close agreement with previous studies showing that piglet performance is improved with the addition of EYA (Kim et al., 1999; Marquardt et al., 1999), ZnO (Mavromichalis et al., 2000), organic acids (Paulicks et al., 1996), and antibiotics (Hill et al., 2001). Although addition of ZnO did not significantly improve (P > 0.05) gain:feed ratio and overall ADFI compared with the control diet in the current study, Hill et al. (2001) observed significant improvements in ADG, ADFI, and gain:feed of nursery pigs with increasing levels of dietary ZnO concentrations up to a maximum of 2,000 mg of Zn/kg.
Plasma urea N levels during wk 1 were not different (P > 0.05) among treatments, but at the end of wk 2, pigs fed the PPI - EYA diet had higher (P < 0.05) PUN levels than piglets fed all other diets (Table 3). The higher PUN concentration in pigs fed the PPI - EYA diet following ETEC infection could either be an indication of increased muscle protein breakdown to release AA for synthesizing acute phase proteins in the liver and/or to serve as an energy source because of lower feed intake in this group of pigs. It has been suggested that during infection or inflammation, feed intake is greatly reduced due to overproduction of cytokines, resulting in a redistribution of nutrients away from growth processes in aid of the immune system (Wannemacher, 1977). The lower PUN levels in piglets fed the PPI-containing diets with added EYA, ZnO, FA, or AB suggest that these additives were able to reduce the severity of ETEC (K88) challenge, which in turn might have prevented or reduced the extent of the immune system activation in these groups, thus allowing for a more efficient utilization of dietary protein and AA for growth or body protein deposition.
All piglets appeared healthy with no scours observed during wk 1. However, 8 h after oral ETEC challenge, PPI - EYA-fed piglets had severe diarrhea with a scour score of 2.4 that lasted for more than 7 d, resulting in 40% mortality. In contrast, piglets fed diets containing SDPP - EYA PPI + EYA, PPI + ZnO, PPI + FA, and PPI + AB had only mild diarrhea, and most of the piglets recovered within 4 d of the ETEC challenge (Table 4). Polymerase chain reaction analysis of fecal swab samples indicated that prior to ETEC challenge all piglets were free of ETEC-K88. However, between 53 and 87% of piglets on the different dietary treatments gave positive identification for ETEC (K88) 8 h after ETEC challenge (Table 4). The majority of PPI - EYA-fed piglets continued to shed ETEC (K88) in the feces compared to those fed diets containing SDPP or PPI supplemented with EYA, ZnO, F, or AB, at 24 h, 48 h, and 7 d after ETEC challenge (Table 4). The current observations indicate that ETEC K88 was able to colonize and proliferate in the small intestine of pigs fed PPI - EYA diet, thus causing the severe scours seen in this group. Nagy and Fekete (1999) proposed that colonization of the small intestine by ETEC adhering to the epithelium is responsible for most of the digestive tract disorders seen in early weaned pigs.
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. Liver weight, small intestinal length, and crypt depth were not different (P > 0.05) among dietary treatments. Piglets fed PPI - EYA diet had higher (P < 0.05) digesta pH in the stomach compared to piglets fed SDPP - EYA- or PPI-based diets with added EYA, ZnO, FA, or AB. Therefore, the high gastric pH seen in pigs fed the PPI - EYA diet was the result of increased proliferation of ETEC, thus resulting in the severe incidence of diarrhea and increased mortality seen in this group of pigs. According to Mathew et al. (1991), proliferation of coliform bacteria is strongly correlated to increased gut pH. A higher gastric pH might result from inefficient digestion of protein, thus providing an optimal environment for the ETEC to colonize the surface of the villi, resulting in the initiation of scours in postweaned piglets (Smith and Jones, 1963). Acidifiers have been shown to be partially effective in the diet of early weaned pigs since piglets are not able to maintain the appropriate gastric pH during the transition from sow’s milk to dry plant-based proteins (Risley et al., 1992).
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). Intestinal morphology was not measured during the prechallenge period in the current study. However, based on the result of our previous study (Owusu-Asiedu et al., 2001) and that of the current study, it can be speculated that feeding a PPI-containing diet to early weaned pigs without the presence of antimicrobial agents such as EYA, Zn, organic acid, antibiotics, or SDPP, in combination with ETEC (K88) infection, compromises the integrity of the intestinal mucosa, thus resulting in diarrhea and the associated effects. This observation is in close agreement with previous studies showing that feeding plant-based protein to young pigs is associated with the occurrence of diarrhea, damage of the microvilli, and postweaning growth lag (Hornich et al., 1973; Li et al., 1990). It has been reported that damaged intestinal mucosa as indicated by villous atrophy, and crypt hyperplasia causes an immune response at the intestinal level, which results in immediate or delayed type hypersensitivity and mucosal inflammation (Li et al., 1990; 1991). This reaction can be severe and lead to reduced performance, immune stress, and a subsequent increase in the incidence of diarrhea (Lalles, 1993), which may have been the case, with PPI - EYA fed pigs. It has been suggested that antimicrobial agents used in swine diets act either by directly suppressing effect on microbes in the gastrointestinal tract, such as pathogenic E. coli, or by a nutrient-sparing effect (Yen et al., 1987). Nutrient-sparing effects, most likely, are the result of an increase in the amount of absorbable nutrients, such as AA and carbohydrates, which in turn is a result of a reduction in nutrients used by bacteria for growth. The current observation suggesting that ZnO, FA, EYA, and SDPP may be functioning as specific or general antimicrobial agents is well supported by numerous studies in the literature. However, it must be noted that the impact of these additives may be partly attributed to their effect on feed intake. Increased feed intake in young pigs is known to reduce the severity of diarrhea in young pigs (Vannier et al., 1983). Also, because an unchallenged group was not included during the change period (d 7 to 14), additional research in which challenged pigs are compared with unchallenged pigs receiving diets containing these additives will provide insights as to how these additives may be acting to control E. coli infection.
The conventional additives used in the current study have all been shown to control bacterial infection in early weaned pigs. For instance, the efficacy of using pharmacological doses of ZnO in preventing and/or alleviating diarrhea in young pigs has also been documented in a number of studies (Kavanagh, 1992). In the current study, supplementing a PPI-based diet with 2,880 mg of Zn/kg not only reduced the incidence of diarrhea, but also speeded recovery of piglets in this treatment group to within 4 d of ETEC administration. By contrast, piglets fed a PPI-based diet without ZnO continued to shed E. coli K88 and had severe diarrhea (Table 4). Similarly, in agreement to the current study, antibiotic (carbadox) has been shown to improve postweaning performance of pigs (Hill et al., 2001).
Numerous studies have shown that the use of organic acids may reduce coliform burden along the gastrointestinal tract (Thomlinson and Lawrence, 1981; Mathew et al., 1991) and reduce scours and piglets mortality. In the current study, adding FA to a PPI-based diet reduced the incidence and severity of diarrhea compared with feeding PPI - EYA. Kershaw et al. (1966) reported that addition of 1% lactic acid to the drinking water improved growth rate and feed efficiency and reduced the E. coli count in the duodenum and jejunum of pigs. Subsequently, Thomlinson and Lawrence (1981) demonstrated that the multiplication of E. coli 0141:K85 was reduced by acidification with a corresponding reduction in piglet mortality. Recently, Callessen et al. (1999) also observed a considerable decrease in frequency of diarrhea in piglets fed organic acid compared with piglets fed control diet.
Spray-dried porcine plasma has been used widely in the diet of early weaned pigs since it has been shown to greatly improve weight gains (10 to 50%) as a result of increased feed intake (Coffey and Cromwell 1995; Jiang et al., 2000). It has also been shown that the feeding of SDPP reduces the incidence and severity of diarrhea in young pigs (Van der Peet-Schwering and Binnendijk, 1995; Owusu-Asiedu et al., 2000) and that its effects are more dramatic in low health compared to high-health herds (Coffey and Cromwell, 1995). It has been proposed that the immunoglobulins and complex protein fractions present in SDPP provide antimicrobial protection (Coffey and Cromwell, 1995; Godfredson-Kisc and Johnson, 1997; Jiang et al., 2000) and might also influence intestinal immune status in the transition to weaning (Jiang et al., 2000). The latter might protect against the development of mucosal damage by enteric pathogens thereby restricting passage of inert large molecules through the intestinal wall (Walker et al., 1975; Van Dijk et al., 2001). Blood plasma immunoglobulins, by preventing bacterial damage of the intestinal gut wall, help maintain optimal intestinal function and gastrointestinal growth, which in turn benefits piglet health and performance (Gomez et al., 1998).
Chicken EYA has been shown to control diarrhea caused by E. coli K88, K99, and 987P in neonatal (Yokoyama et al., 1992) and weaned piglets (Marquardt et al., 1999; Kim et al., 1999). In the current study, piglets fed the PPI + EYA-based diet recovered 3 d after ETEC challenge (Table 4), indicating that the presence of the specific anti-ETEC antibody binds the E. coli, thereby preventing colonization and proliferation, resulting in subsequent removal of the E. coli. Recently, Jin et al. (1998) demonstrated in an in vitro study that purified antibody from the yolk of chicken immunized against E. coli (K88) was able to block the binding of ETEC K88 to the mucosal receptor and that the interaction was fairly rapid.
Overall, the current observation demonstrated that antibodies prepared from the yolk of eggs from laying hens immunized with fimbrial antigens of E. coli (K88) containing specific anti-K88 and anti-F18 antibodies, as well as ZnO, FA, carbadox, and SDPP reduced and/or prevented infection in piglets challenged with an homologous ETEC strain K88, thus reducing the severity of diarrhea and incidence of mortality. The study further demonstrates that these "antimicrobial agents" prevented colonization and proliferation of bacteria and subsequent damage of the intestinal wall, thereby maintaining gut integrity.
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Footnotes |
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Received for publication March 1, 2002. Accepted for publication March 13, 2003.
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