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Response of early-weaned pigs to an enterotoxigenic Escherichia coli (K88) challenge when fed diets containing spray-dried porcine plasma or pea protein isolate plus egg yolk antibody¹

A. Owusu-Asiedu^*, C. M. Nyachoti^*,2, S. K. Baidoo, R. R. Marquardt^* and X. Yang

^* Department of Animal Science, University of Manitoba, Winnipeg, MB, Canada R3T 2N2, and Southern Research and Outreach Center, University of Minnesota, Waseca 56093-4521, and and Department of Medical Microbiology, University of Manitoba, Winnipeg, MB, Canada R3E 0W3

² Correspondence—phone:
204-474-7323; fax: 204-474-7628; E-mail:
martin_nyachoti{at}Umanitoba.ca.

	Abstract

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Enterotoxigenic E. coli (ETEC) infection and resulting scours is a major problem for young pigs, especially when purified plant proteins are fed rather than spray-dried porcine plasma (SDPP). The effect of supplementing a pea protein isolate (PPI)-based diet with egg yolk antibodies (EYA) from laying hens immunized with ETEC K88 antigen on piglet performance, incidence of scours, and gut histology was studied in a 14-d trial. Ninety-six 10-d-old weaned pigs were assigned to five dietary treatments in a completely randomized design to give six replicate pens per treatment. The treatments were PPI without EYA (PPI-EYA), PPI with EYA (PPI+EYA), SDPP without EYA (SDPP-EYA), SDPP with EYA (SDPP+EYA), or a combination of PPI and SDPP (PPI+SDPP). Diets were formulated to similar nutrient levels and provided for ad libitum intake. Blood from all pigs was taken on d 0, 7, and 14 for determining plasma urea N (PUN). On d 7, pigs were orally challenged with 6 mL of 10¹⁰ cfu/mL ETEC K88. Piglets were weighed on d 7 and 14. On d 7, 8, and 14, four pigs per treatment were sacrificed to study the histology of the small intestine. Weekly feed intake, BW changes, and gain:feed were determined. Fecal swabs from 10 pigs per treatment were taken for a PCR test to detect K88 E. coli. Feed efficiency over the 14-d period was not affected (P > 0.78) by dietary treatment. Mean ADFI on an as-fed basis was lower (P < 0.002) in piglets fed PPI-EYA (64.3 g/d) compared with PPI+EYA (94.8 g/d) or SDPP (102 g/d) during wk 1. Piglets fed PPI-EYA tend to have a lower (P < 0.026) overall ADG (84 g/d) than those fed PPI+EYA (123 g/d) or SDPP (127 g/d) (P < 0.006)-based diets. Although scours was evident in all groups of pigs 6 h after the challenge, most of the piglets fed EYA- or SDPP-containing diets recovered 10 to 72 h postchallenge, whereas those fed PPI-EYA continued to have severe diarrhea, resulting in 33% mortality. The PCR results showed that a greater (P < 0.01) percentage of piglets fed PPI-EYA compared with those fed SDPP- or EYA-containing diets continued to shed ETEC K88 at the end of the 14-d study. Piglets fed PPI-EYA had shorter villi (P < 0.01), higher intestinal pH (P < 0.013), and higher PUN (P < 0.05) than those fed the SDPP- or EYA-containing diets during the entire 14-d study. It was concluded that specific EYA and SDPP could provide passive control of ETEC infection and potentially improve feed intake and weight gain in young pigs fed PPI.

Key Words: Antibodies • Early Weaning • Escherichia coli • Pigs • Plasma • Scours

	Introduction

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Early-weaned pigs (EWP) are unable to effectively utilize dry complex carbohydrate and plant protein-based diets because of their relatively less developed gastrointestinal tracts (Hansen et al., 1993; Cranwell, 1995; Grinstead et al., 2000). Various factors, including a transient hypersensitive response to plant-based proteins (Friesen et al., 1993) and inability to resist enteric diseases (Cranwell, 1995) are thought to be responsible for poor growth in EWP. Addition of spray-dried porcine plasma (SDPP) to EWP diets has been shown to improve feed intake and weight gain (Coffey and Cromwell, 1995) and to reduce incidences of scours (Van der Peet-Schwering and Binnendijk, 1995), particularly from d 0 to 14 postweaning. However, SDPP is expensive and the use of animal plasma has been banned in Europe, a move that may also be adopted in North America to, theoretically, prevent the potential transmission of bovine spongiform encephalomyetis.

A current interest in swine nutrition is to identify inexpensive protein sources to replace SDPP in diets for EWP. Processed plant protein sources such as pea protein isolate (PPI) could potentially be used as an alternative to SDPP. Unfortunately, PPI does not provide any specific antienterotoxigenic Escherichia coli (ETEC) antibodies, which are present in SDPP and thought to be partly responsible for the reduced incidence of scours in piglets fed SDPP-based diets (Owusu-Asiedu et al., 2000). Chicken egg yolk antibody (EYA) from hyperimmunized laying hens containing specific anti-ETEC antibodies has been shown to reduce incidence of diarrhea, mortality, and to improve performance when fed to EWP (Kim et al., 1999; Marquardt et al., 1999). We therefore postulated that adding EYA to diets of EWP could prevent the negative effects associated with feeding plant-based proteins (e.g. PPI) to EWP. The objective of the current research was to evaluate the use of PPI supplemented with EYA as an alternative to SDPP in diets for EWP.

	Materials and Methods

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Animal Care, Housing, and Experimental Design

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 96 piglets weaned at 10 d of age (3.5 ± 0.3 kg initial BW) were used in a 14-d trial. Piglets were randomly allotted to each of five dietary treatments in a completely randomized design. Each treatment was assigned to six pens (1.2 x 1.5 m) each with three pigs, except for the PPI without EYA diet (PPI-EYA), which had four pigs per pen as a higher mortality rate was expected in this treatment group based on previous observations by Kim et al. (1999). Room temperature was maintained at 31 ± 1°C throughout the study.

Feed, Feeding, and Experimental Procedure

PPI and SDPP were obtained from Parrheim Foods (Portage La Prairie, MB, Canada) and Farmlands Proteins Plant (Maquoketa, IA), respectively. EYA was produced in our laboratory as described previously (Marquardt et al., 1999). The experimental diets were PPI-EYA, PPI with EYA (PPI+EYA), SDPP without EYA (SDPP-EYA), SDPP with EYA (SDPP+EYA), and a combination of PPI and SDPP in a 1:1 ratio (PPI+SDPP). The EYA contained 0.3 and 0.2% egg yolk powder each containing specific anti-K88 and -F18 antibodies, respectively. All experimental diets were formulated to exceed NRC (1998) nutrient requirements for piglets of 3.0 to 6.0 kg of BW and contained similar CP (26.5%), lysine (1.6%), methionine (0.7%), and threonine (1.2%) (Table 1). Pigs had unlimited access to feed and water at all times. Average daily gain, ADFI, and feed conversion efficiency (gain:feed) were determined. On d 7, 8, and 14, blood samples (10 mL) were collected from all pigs via jugular vein puncture into vacutainer tubes (Becton Dickinson, Rutherford, NJ), and immediately centrifuged at 2,000 x g for 10 min at 5°C to recover plasma, which was immediately stored at -20°C until required for PUN analysis.

All pigs were orally challenged with a local strain of ETEC expressing the K88 (F4) fimbriae, obtained from the Animal Health Center, Veterinary Services Branch, Manitoba Department of Agriculture (Winnipeg, MB, Canada). The K88 strain of E. coli was used since it is one of the most common causes of diarrheal disease in EWP (Nagy and Fekete, 1999). Primary cultures of the ETEC strain were grown overnight in tryptic soya broth (TSB, CASO-Bouillon, Mikrobiologie, Darmstadt, Germany) at 37°C using 1% inoculum volume 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 1% inoculum volume from stock. Cells were washed twice with 2 mL of sterilized saline solution (0.9%, pH 7.2), and then the 10¹⁰ cfu/mL suspension was used for oral challenge. On d 7, each pig orally received 6 mL of bacterial suspension from a syringe attached to polyethylene tube. Severity of diarrhea was characterized using the fecal consistency (FC) score described by Marquardt et al. (1999). Fecal consistency scoring (0, normal; 1, soft feces; 2, mild diarrhea; 3, severe diarrhea) performed by two individually trained personnel with no prior knowledge of dietary treatments allocation was used to ascribe the diarrhea score of pigs.

Detection of Antibodies Titer

Enzyme-linked immunosorbent assay with purified fimbrial antigen was used to determine anti-K88, -K99, -987P, -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 was 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) was 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. When necessary, samples of SDPP, PPI, and experimental diets were ground through a 1-mm screen (Cyclotec 1,093, sample mill, Tecator, Hoganas, Sweden) prior to analysis. Samples were dried in a convection oven at 105°C for 16 h for DM determination, while CP (N x 6.25) content was determined using a 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). 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) using a standard kit (procedure No. 535, Sigma Diagnostic, St. Louis, MO).

Polymerase Chain Reaction

Fecal swab samples for microbial analysis were collected in duplicate from 10 pigs randomly selected per treatment using the Culture Swab Transport System (Difco) at 6, 24, and 48 h, as well as 7 d after the ETEC challenge. Samples were plated onto TSB and the individual colonies were used for the PCR-based method for detection and differentiation of K88 adhesive E. coli. The PCR technique was based on the procedure described by Sambrook et al. (1989). The sense and anti-sense primers that encoded the specific K88 fimbrial gene were used. PCR was performed following a standard procedure in a thermocycler 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 recovered with glass beads (Qbiogene, Inc., Carlsbad, CA). The resultant PCR product corresponded in size (2.6 kDa) to structural subunits of the K88 operon that was selected. A product was deemed positive when it produced a distinctive band consistent with its expected migration on the agarose gel as determined by comparison with the DNA fragment standards.

Histological and Other Measurements

On d 7, 8, and 14, four pigs per treatment were selected randomly from four pens per treatment and sacrificed to determine the effect of dietary treatments and oral ETEC challenge on weight and morphology of the gastrointestinal tract. Pigs were held under general anesthesia and killed by an intracardiac injection of sodium pentobarbital (50 mg/kg of BW). Stomach, spleen, small intestine, and liver were removed and 20 mL of digesta each from the stomach and the small intestine was obtained for pH measurement. The pH of the digesta was determined by inserting a combination electrode directly into aqueous suspension. The organs or sections were flushed with ice-cold phenylmethyl sulfonyl fluoride (PMSF) saline (2 L of 0.9% saline, pH, 7.4 + 2 mL of 100 mM PMSF). The weights and length (small intestine) of these organs were determined. A 10-cm segment of three sections of the small intestine were removed at 20 and 150 cm from the pyloric junction and 40 cm from the ileocecal junction to represent the duodenal, jejunal, and ileal regions. The sections were stored and processed as described by Rooke et al. (1998). Briefly, after dehydration in 70% alcohol, six cross sections of the formalin-fixed intestinal samples were embedded in paraffin, sliced to approximately 5 µm and stained with hematoxylin and eosin. The measurement of villous height (VH) and crypt depth (CD) was made on 10 well-oriented villi per specimen and averaged per pig 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). The height of the villus was measured from the tip to the crypt-villus junction and the depth of the crypt from the crypt-villus junction to the base.

Statistical Analysis

Single measurements of VH and CD for each pig were obtained by averaging the 10 measurements of villi and the crypt per specimen to provide four observations per treatment. All data were analyzed as a completely randomized design. For ADFI, ADG, and gain:feed, the pen was considered the experimental unit. Treatment means were compared using Fisher’s protected least significant difference procedure, and ² was used to test PCR, scour scores, and mortality (Cody and Smith, 1991). Statistical significance was accepted at P < 0.05. All statistical analyses were performed using the GLM procedure of SAS (SAS Inst., Inc., Cary, NC).

	Results and Discussion

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Crude protein and AA compositions were similar in PPI and SDPP (Table 1). Also, analyzed and calculated nutrient composition indicated that all of the experimental diets had similar CP, AA, and digestible GE levels (Table 1). An analysis of EYA, SDPP, PPI, and experimental diets demonstrated that all preparations contained their own unique combination of specific anti-ETEC (anti-K88 and -F18) antibodies in very different amounts (Table 2). SDPP contained good titers of anti-K88 (18,000) and anti-F18 (15,000). The presence of antibodies in SDPP have been attributed to exposure of pigs to ETEC that express the K88 and F18 fimbrial antigens, which are also the prime cause of diarrheal disease (Alexander, 1994). In contrast to SDPP, EYA from hens immunized with either the K88 or F18 fimbrial antigens had much higher titers of the corresponding specific anti-K88 and -F18 antibodies, with the values being 600,000 and 450,000, respectively (Table 2). The amount of EYA required to protect pigs against ETEC-K88 or ETEC-F18 should therefore be 38- or 30-fold less than that for SDPP. As a result, the amount of egg yolk that would have to be added to the diet to provide the same anti-K88 antibody titers as those present in a diet containing 10% SDPP would be only 0.33%. The other component used to replace SDPP in the diet was PPI, which was prepared by wet milling peas. PPI contained a high concentration of protein with the balance of essential AA being similar to that of SDPP (Table 1). The PPI, however, was devoid of both anti-K88 and -F18 antibodies (Table 2). Therefore, the addition of EYA to PPI diets resulted in the addition of specific anti-K88 and -F18 ETEC antibodies (immunoglobulins) that were approximately equal in concentration to those present in the SDPP diet.

During the prechallenge period (wk 1), ADG was lower (P ≤ 0.02) for PPI-EYA-fed piglets compared to all treatment groups. Adding EYA or SDPP to PPI or feeding SDPP alone improved ADG (P < 0.01) during this phase of growth (Table 3). Also, ADFI for wk 1 was lower (P < 0.02) for PPI-EYA-fed pigs compared to piglets fed all the other treatment. The ADFI and ADG for the postchallenge period (wk 2) were similar (P > 0.37) and (P > 0.28), respectively, for all treatment groups. As shown in Table 3, PPI-EYA-fed piglets, compared with all other treatments, tended to have reduced ADFI (P = 0.07) and ADG (P < 0.05) for the entire 14-d experimental period. The FCE for the prechallenge, postchallenge, and the entire experimental period were similar (P > 0.80) for all dietary treatments (Table 3). Feeding PPI-EYA compared with SDPP or PPI+EYA resulted in a 46 or 38% decline in ADFI and a 51 or 46% decline in ADG, respectively, from d 0 to 14. By feeding a blend of PPI and SDPP (PPI+SDPP, 1:1) compared to feeding PPI-EYA, ADFI and ADG improved by 52 and 56%, respectively. These results also agree with our recent observation that 10-d-old weaned piglets fed diets with no specific anti-ETEC antibody performed more poorly than those fed EYA- and SDPP-containing diets, each of which contained the specific anti-ETEC antibodies (Owusu-Asiedu et al., 2000). Kats et al. (1994) also observed increases of 46% in ADFI and 55% in ADG from d 0 to 14 for pigs fed diets with 8 vs. 0% SDPP. It has been suggested that SDPP improves performance of piglets fed higher levels of SBM from d 0 to 14 postweaning by, among other modes, preventing a transient hypersensitivity response (Hansen et al., 1993).

The protective effect of EYA obtained from hens immunized with antigens from a local strain of ETEC (K88) has been evaluated in a number of studies (Yokoyama et al., 1992; Kim et al., 1999; Marquardt et al., 1999). In a study with 21-d-old weaned pigs fed either EYA or egg yolk powder without antibody and challenged with a high dose of ETEC (10¹⁰ cfu/mL), Kim et al. (1999) observed that control pigs that received egg yolk powder (without EYA) developed severe diarrhea within 12 h and were dehydrated and lost BW within 48 h, resulting in 30% mortality. In contrast, the pigs treated with EYA showed no signs of diarrhea 24 or 48 h after treatment, had positive weight gain, and no mortality. These observations are in close agreement with the findings of the current study. Although the mode of action of specific anti-ETEC antibodies in EYA and SDPP was not determined in the current study, it is likely that this might have involved blocking the binding of E. coli K88 to the mucosal receptors, as demonstrated by Jin et al. (1998). The higher performance of pigs fed SDPP-EYA, SDPP+EYA, and PPI+EYA vs. PPI-EYA, as indicated earlier, can be attributed mainly to the anti-K88 and -F18 antibodies since the only difference between the two diets was that PPI-EYA did not contain the above specific antibodies.

Visceral organ weights and intestinal digesta pH are shown in Table 4. Liver weights were influenced by dietary treatment, with the piglets fed PPI-EYA, PPI+EYA, and SDPP+EYA for 14 d having the smallest (P < 0.05) relative liver weight compared with those fed SDPP-EYA or SDPP+PPI, (Table 4). Piglets fed the PPI-EYA diet for 14 d had higher (P < 0.05) intestinal digesta pH than those fed the other dietary treatments, which may partly explain the severity of diarrhea observed in this group. Higher gastric pH is speculated to provide an optimal environment for ETEC to colonize the surface of the villi, resulting in the initiation of scours in young pigs, particularly after weaning (Smith and Jones 1963; Nagy and Fekete, 1999).

Plasma urea N level of piglets fed a combination of PPI and SDPP was lower (P < 0.05) compared with piglets in the other treatment groups during the prechallenge period (Table 4). However, on d 14 (postchallenge period), PUN levels were higher (P < 0.05) in PPI-EYA-fed piglets compared to those fed the other four diets (Table 4). Infectious diseases or inflammation markedly reduce feed intake and cause a redistribution of nutrients away from growth processes to support the immune system. In such instances, AA are liberated from muscle breakdown and can be utilized for the synthesis of acute-phase proteins in the liver and as an energy source (Wannemacher, 1977). Furthermore, Van Heugten et al. (1994) have shown that the efficiency of protein utilization during an inflammation response is decreased in 21-d-old weaned pigs injected with lipopolysaccharide. Thus, the higher PUN level in the PPI-EYA fed pigs after ETEC challenge is an indication that infection in this treatment group activated the immune system, and might have led to increased body protein breakdown, as well as a reduced efficiency of dietary protein utilization for body protein accretion (Coma et al., 1995).

Compared with piglets fed PPI+EYA, SDPP-EYA, and SDPP+EYA, piglets fed PPI-EYA had shorter (P < 0.05) villi in the duodenum immediately before (d 7) and after (d 8) the E. coli challenge. Also, on d 14, PPI-EYA-fed piglets had the shortest (P < 0.05) villi compared with all other treatments (Table 5). However, crypt depths were similar (P > 0.10) and were not influenced by dietary treatment or oral ETEC challenge (Table 5). Gut morphology has been examined in several weaning studies and reduced villi height has been linked to postweaning growth lag (Cera et al., 1988) and diarrhea (Hornich et al., 1973) in weaned pigs. The reduction in villi height seen in the current study was also associated with a corresponding decrease in ADG and ADFI and an increased incidence of scours in the PPI-EYA-fed pigs. Pigs fed diets containing SDPP or EYA had longer villi, less severe diarrhea, and grew faster than did PPI-EYA-fed pigs, suggesting that piglets in these treatments (i.e., only the pigs that received the antibodies), experienced minimal destruction of the gastrointestinal tract. Intestinal damage as a result of E. coli infection is therefore a possible cause of the observed villous atrophy in the diet without antibody, but not the other diets that contained anti-K88 E. coli antibodies. Presumably pigs from the former but not the latter groups would have absorbed the large PPI molecules, which would have induced an immune (antigenic) response (Li et al., 1990; 1991; Le Guen et al., 1991; Makinde et al., 1996). On the basis of our results and those reported in the literature, it is concluded that the antigenic effect observed with legume diets is not caused by the legume protein per se, but is attributable to the lack of antibodies against intestinal pathogens, especially E. coli K88 (and probably F18), which result in colonization of the gut and destruction of the villi, thus allowing malabsorption of foreign proteins, which are antigenic. Therefore, dietary antibodies prevented damage of the villi by pathogens, thus maintaining normal absorption of nutrients without absorption of intact or partially digested protein. This means that any proteins, vegetable or animal, should induce an antigenic response if villi are damaged by infection and the proteins are absorbed. This speculation, however, needs to be tested.

The results of the current study demonstrated that specific EYA and SDPP can provide passive control of ETEC (K88) infection, thereby improving feed intake and weight gain in EWP, especially those fed diets containing plant protein supplements.

	Implications

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The current results suggest that feeding early weaned pigs diets containing spray-dried plasma proteins, pea protein isolate plus egg yolk antibody, or a combination of pea protein isolate and spray-dried plasma protein during d 0 to 14 after weaning minimizes gastrointestinal disorders associated with Escherichia coli infection. Supplementing weanling pig diets with egg yolk antibody or spray-dried plasma protein will allow utilization of processed plant proteins, such as pea protein isolate, and also offer a means for managing postweaning diarrhea, which is a major problem in the management of early weaned pigs. The current study indicates that supplementing pea protein isolate with egg yolk antibody provides a viable alternative to plasma proteins.

	Footnotes

 
¹ We thank S. Cole for his help with the PCR, L. Fang for culturing the microorganism, and G. H. Crow for his help with experimental design and statistical analysis.

Received for publication September 18, 2001. Accepted for publication March 13, 2003.

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