J. Anim Sci. 2006. 84:2101-2109. doi:10.2527/jas.2005-616
© 2006 American Society of Animal Science
ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Supplementing drinking water with Solutein did not mitigate acute morbidity effects of porcine reproductive and respiratory syndrome virus in nursery pigs
J. Escobar*,1,
T. L. Toepfer-Berg*,
J. Chen*,
W. G. Van Alstine
,
J. M. Campbell
and
R. W. Johnson*,2
* Department of Animal Sciences, University of Illinois, Urbana 61801;
and
Animal Disease and Diagnostic Laboratory, Purdue University, West Lafayette, IN 47907;
and
American Protein Corporation Inc., Ankeny, IA 50021
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Abstract
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The objective of this study was to determine whether providing nursery pigs drinking water supplemented with spray-dried animal plasma (Solutein, American Protein Corporation Inc., Ankeny, IA) would reduce the detrimental impact of porcine reproductive and respiratory syndrome virus (PRRSV) infection. Sixty-four pigs were subjected to 1 of 4 treatment combinations (2 x 2 factorial arrangement) of Solutein [0 or 2.5% (wt/wt) in drinking water] and PRRSV (sterile medium or 5 mL of tissue culture infectious dose of high-virulence strain ATCC VR-2385). Pigs were provided the water treatments during a 1-wk period before inoculation as well as during a 2-wk period after inoculation. Growth performance was determined throughout the study, and several indicators of the immunological response to PRRSV and disease pathology were assessed in blood and tissue samples collected from pigs killed 7 or 14 d after inoculation. Before inoculation, pigs provided water supplemented with Solutein tended to eat less (P = 0.08) but tended to gain more BW (P = 0.13) than pigs provided tap water. Thus, Solutein markedly improved G:F (P < 0.01), after accounting for the DM provided by Solutein. Inoculation with PRRSV reduced ADG and ADFI (P < 0.01) irrespective of water treatment; however, the beneficial effects of Solutein on G:F persisted. Infection with PRRSV also reduced (P < 0.009) villus height and crypt depth in cranial, medial, and caudal segments of the small intestine and increased (P < 0.05) lung and spleen weight, the number of leukocytes in lung lavage fluid, and serum concentrations of interferon-
and IL-1ß regardless of water treatment. Collectively, these results indicate that supplementing water with spray-dried animal plasma improved feed efficiency but did not afford nursery pigs protection from the effects of PRRSV on growth and certain hematological traits.
Key Words: cytokine • disease • growth • pig • porcine reproductive and respiratory syndrome virus • soluble plasma
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INTRODUCTION
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The porcine reproductive and respiratory syndrome virus (PRRSV) is highly prevalent in US swine herds. It preferentially infects and replicates within mononuclear phagocytic cells located within the mucosal surface of the respiratory tract. In endemically infected herds, predominant signs of PRRSV infection occur in nursery-grower pigs where acute infection of immunologically naive pigs induces signs of illness, including fever, lethargy, anorexia, and depressed growth. The negative effects of PRRSV on growth performance are highly reproducible under experimental conditions (Greiner et al., 2000
; Escobar et al., 2004; Toepfer-Berg et al., 2004).
Spray-dried animal plasma is routinely added to diets for early weaned pigs because various studies have shown it improves growth performance (Kats et al., 1994; de Rodas et al., 1995; Grinstead et al., 2000). The improved performance caused by spray-dried plasma is most marked when pigs are maintained in a conventional environment where exposure to infectious and noninfectious microorganisms is relatively high (Coffey and Cromwell, 1995; Bergstrom et al., 1997). In fact, the growth-promoting properties of dietary spray-dried plasma vanished when pigs were kept in an experimental setting where presumably good hygiene was emphasized (Coffey and Cromwell, 1995). Thus, spray-dried plasma may improve growth performance by reducing exposure to pathogenic and nonpathogenic microorganisms, modulating the immune response, or both. If spray-dried plasma enhances the immune system or reduces pathogenic microorganisms that may result in secondary infections, we thought it might mitigate the acute effects of PRRSV infection. Therefore, the objective of the current study was to investigate the efficacy of supplementing water with a new spray-dried animal plasma product (Solutein, American Protein Corporation, Ankeny, IA) to reduce the detrimental impact of PRRSV infection in nursery pigs.
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MATERIALS AND METHODS
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Animals, Housing, and Experimental Design
All procedures involving animals were approved by the University of Illinois local animal care and use committee. Thirty-two 2-wk-old Ausgene Line 20 dam x Line 5 sire pigs obtained from United Feeds Inc. (Sheridan, IN) were used in each of 2 trials (64 pigs total). Blood samples were collected at 1 wk of age, and virus isolation procedures were performed by the Animal Disease Diagnostic Laboratory (Purdue University, West Lafayette, IN) to verify that the pigs were free of PRRSV.
Pigs were brought to the University of Illinois at 2 wk of age, randomly allotted into 2 groups, and placed in disease-containment chambers. The housing conditions for the disease containment chambers have been previously described (Escobar et al., 2002). Pigs received daily injections of Lincomycin (11 mg/kg of BW; Pharmacia & Upjohn Co., Kalamazoo, MI) for 5 d after arrival as a precautionary measure against Mycoplasma hyopneumoniae (Escobar et al., 2002). Each waterer was made by capping one end of a 0.85-m-long section of 16-cm-diam. PVC pipe and installing a nipple 7 cm above the capped bottom. Waterers of this design were used to supply drinking liquid to pigs allotted to all treatments.
At 3 wk of age, pigs were allotted into uniform blocks based on BW, sex, and litter of origin, and were randomly assigned to 1 of 4 treatments. Pigs began their assigned water treatment immediately after allotment. For each of the 2 trials, 2 pigs (1 barrow and 1 gilt) were placed in each of 16 chambers. The 4 treatments comprised a 2 x 2 factorial arrangement consisting of Solutein [0 or 2.5% (wt/wt) in tap water] and PRRSV (5 mL of sterile medium or tissue culture infectious dose of high-virulence strain ATCC VR-2385). Throughout the study, pigs were given ad libitum access to a pelleted feed that was free of plasma products (Table 1), tap water, or tap water with 2.5% Solutein, unless otherwise indicated. Pigs used in this study did not have access to creep feed or plasma products. Tap water with Solutein was the sole source of drinking water for those pigs assigned to it. Solutein is a water-soluble source of plasma proteins with a guaranteed analysis of 65% CP, minimum; 11% crude fiber, maximum; 0.1% crude fat, minimum; 4.5% ash; and 9% moisture.
At 4 wk of age, one-half of the pigs assigned to the 0 and 2.5% Solutein treatments were inoculated intranasally with PRRSV; the remaining pigs received sterile culture medium. To minimize the chance for cross contamination, pigs in 1 suite (consisting of 8 identical chambers) received PRRSV, whereas pigs in the other suite received sterile culture medium. The PRRSV treatment was imposed in each suite across the 2 trials. Biosafety level 3 procedures (Richmond and McKinney, 1993) were employed at all times. Every morning, leftover tap water and tap water with Solutein were removed while cleaning the chambers. The waterers were washed, disinfected, and restocked with fresh water each day. Water with Solutein was prepared fresh each day for restocking.
Pigs always had access to tap water or water supplemented with Solutein but were deprived of food for 12 h before inoculation and before BW was determined at 7 and 14 d after inoculation. Feeders and waterers were weighed daily to estimate feed and water intake, respectively. In each of the 2 trials, 2 chambers of pigs (4 pigs total) from each treatment were randomly selected, anesthetized by i.m. injection of TKX (telazol:ketamine:xylazine, 2:1:1; 4.4 mg/kg of BW) solution, and killed by exsanguination at d 7 and 14 after inoculation for tissue sample collection.
Sampling and Assay Techniques
Determination of Hematocrit and Total Blood Leukocyte Counts and Differentials.
Blood samples were collected from the vena cava into Vacutainer tubes containing EDTA (BD Vacutainer, Franklin Lakes, NJ) on d 3, 7, and 14 after inoculation. Whole blood was drawn from each sample into duplicate capillary tubes and centrifuged for 2 min in a microcapillary centrifuge. The percentage of the volume of the blood sample occupied by cells (the hematocrit) was determined using a microcapillary reader. Complete white blood cell (WBC) counts were performed on whole blood using a Z1 Coulter Counter (Coulter Corp., Miami, FL), and differential counts were performed manually on blood smears (2 per pig) that were stained with Hema 3 (Fisher Scientific Co., Pittsburgh, PA). Two hundred cells were counted on each slide. The average number of cells present was determined by averaging the 2 counts, and the percentage of neutrophils, lymphocytes, monocytes, and eosinophils was determined.
Spleen, Liver, and Lungs.
Immediately after exsanguination, the spleen and liver were removed and weighed. The lungs were removed, inspected for gross lesions, weighed, and then lavaged 3 times with RPMI (Roswell Park Memorial Institute) 1640 cell-culture medium. Lungs were filled via the trachea with RPMI and gently massaged for 30 s. Lavage fluid was collected in 50-mL conical tubes, placed on ice, and leukocyte counts were performed using the Z1 Coulter Counter.
Small Intestine.
The small intestine was removed, dissected free, and laid out so that it formed 3 segments of equal length. Three-centimeter segments were collected at the cranial, medial, and caudal regions of the small intestine (defined as 25, 50, and 75% of the intestinal length, respectively) and placed in 10% neutral buffered formalin. Three cross-sections of each intestinal sample were processed in low-melt paraffin, sectioned at 5-µm thickness, mounted on glass slides, and stained with hematoxylin-eosin. Villus height and crypt depth were measured using a microscope (Nikon Diaphot, Fryer Company, Carpentersville, IL) with a mounted video camera and screen connected to a computer. Three villus heights and crypt depths were measured from each slide using the software Image-measure (Microscience Inc., Federal Way, WA).
Serum Interferon- and Interleukin-1ß.
Serum from 1 pig, regardless of sex, that was randomly selected from each chamber on d 7 after inoculation, was assayed for interferon (IFN)- and interleukin (IL)-1ß. Serum IFN- and IL-1ß were measured using porcine-specific ELISA kits purchased from Pierce Endogen (Rockford, IL) and R & D systems (Minneapolis, MN), respectively. The porcine ELISA had been validated by the company. In addition, the ELISA were validated in our laboratory using recovery and parallelism assays with recombinant cytokines and plasma samples obtained from pigs injected with E. coli lipopolysaccharide (LPS; data not shown). The IFN- assay had a sensitivity of 2 pg/mL, and the minimum detectable concentration of IL-1ß was 10 pg/mL. For each cytokine, all samples were assayed in a single assay, and the intraassay coefficient of variation was <10%.
Statistical Analysis
Data were subjected to 2-way (Solutein x PRRSV) ANOVA procedures using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC). The pen was considered the experimental unit for growth performance, whereas the pig was the experimental unit for all other measurements. Means were compared using the LSD option of SAS. The first ANOVA procedure was used to determine main effects and means for the period before inoculation (i.e., wk 1 and 2). A second ANOVA procedure was used to determine main effects and means of the entire 2-wk period after inoculation. Data are presented as means ± SEM.
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RESULTS
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PRRSV Infection
Pigs were tested before the study and determined to be PRRSV-free. They were retested at the end of the study to verify the efficacy of the disease model. As expected, PRRSV was isolated from sera of all pigs inoculated with PRRSV regardless of water treatment, whereas PRRSV was not detected in sera of pigs receiving sterile culture medium. There were no gross pulmonary lesions evident in either control or PRRSV pigs.
Growth Performance
The effects of Solutein and PRRSV on ADG, ADFI, average daily liquid disappearance (ADLD), DMI, and G:F are summarized in Table 2. Before inoculation, pigs provided water supplemented with Solutein tended to eat less feed (P = 0.08) but tended to gain more (P = 0.13) than pigs provided tap water. Thus, Solutein markedly improved G:F (P = 0.001). A reduction in ADLD in pigs provided Solutein was evident during the week before inoculation (P = 0.02) and during the entire 2-wk period after inoculation (P = 0.001), but hematocrit values were not substantially different (P = 0.45 to 0.89) between treatment groups (Table 3) and no indications of dehydration were evident. Because water disappearance was measured (wasted water was not collected), it is possible that the purported difference in ADLD for Solutein and tap water pigs was due to the amount of water wasted rather than actual intake. Exposure to PRRSV reduced (P = 0.02) ADLD during the 2-wk period after inoculation, and a Solutein x PRRSV interaction was evident for the 2-wk period after inoculation (P = 0.004). Hematocrit was significantly reduced (P < 0.003) in PRRSV pigs 3, 7, and 14 d after inoculation (Table 3).
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Table 2. Effects of 2.5% (wt/wt) Solutein (American Protein Corporation Inc., Ankeny, IA) water supplementation and porcine reproductive and respiratory syndrome virus (PRRSV) infection on growth performance of pigs
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Table 3. Effects of 2.5% (wt/wt) Solutein (American Protein Corporation Inc., Ankeny, IA) water supplementation and porcine reproductive and respiratory syndrome virus (PRRSV) infection on hematocrit and liver, spleen, and lung weight of pigs
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There was a main effect of PRRSV on ADG for wk 1, wk 2, and the entire 2-wk period after inoculation P < 0.001), but neither Solutein nor the interaction between Solutein and PRRSV was significant (P = 0.36 to 0.68). Thus, infection with PRRSV reduced ADG regardless of water treatment. After inoculation, ADFI was reduced by both Solutein and PRRSV (P < 0.04). There was no interaction (P = 0.59 to 0.96) between Solutein and PRRSV for ADFI for wk 1, wk 2, or the entire 2-wk period after inoculation, indicating their depressive effects on feed intake were additive. Gain:feed was reduced by PRRSV 1 wk after inoculation (P = 0.01) and for the entire 2-wk period after inoculation (P = 0.006). In contrast, G:F was markedly improved by Solutein 1 wk after inoculation (P = 0.007) and for the entire 2-wk period after inoculation (P = 0.002). There was no interaction (P = 0.46 to 0.82) between Solutein and PRRSV, indicating the improved G:F in pigs given Solutein was maintained during PRRSV infection.
Spleen, Liver, and Lung Weights
The PRRSV infects alveolar macrophages and induces interstitial pneumonia and pulmonary edema; therefore, as anticipated, PRRSV increased lung weight (g/kg of BW) 7 (P = 0.003) and 14 (P = 0.001) d after inoculation (Table 3
). Splenomegalia was also evident in PRRSV pigs 7 (P = 0.02) and 14 d (P = 0.009) after inoculation (Table 3). Neither Solutein nor the interaction between Solutein and PRRSV influenced lung and spleen weight (P = 0.23 to 0.65). At d 7 after inoculation, Solutein increased liver weight (P = 0.03) and PRRSV tended to as well (P = 0.08); however, these effects were not evident 14 d after inoculation (P = 0.40 to 0.76).
Small Intestine
Villous height and crypt depth were determined in the cranial, medial, and caudal segments of the small intestine 7 d after inoculation. Infection with PRRSV markedly reduced (P < 0.009) villus height and crypt depth in cranial, medial, and caudal segments (Table 4). Solutein did not affect (P = 0.15 to 0.92) villus height or crypt depth.
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Table 4. Effects of 2.5% (wt/wt) Solutein (American Protein Corporation Inc., Ankeny, IA) water supplementation and porcine reproductive and respiratory syndrome virus (PRRSV) infection on villus height and crypt depth in the segments of the small intestine of pigs1
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Serum IFN- and IL-1ß
Interferon- and IL-1ß were measured in serum collected 7 d after inoculation (Figure 1 and 2, respectively). As anticipated, PRRSV-infected pigs had greater (P < 0.01) concentration of both IFN- and IL-1ß than noninfected pigs. Water supplemented with Solutein did not affect (P = 0.16 to 0.84) serum cytokine concentration in either infected or noninfected pigs.
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Figure 2. Effects of 2.5% (wt/wt) Solutein water supplementation and porcine reproductive and respiratory syndrome virus (PRRSV) infection on serum interleukin (IL)-1ß measured 7 d after inoculation. Pigs infected with PRRSV had greater (P < 0.01) IL-1ß in serum compared with noninfected controls. Values are means ± SEM.
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Total Leukocyte Counts and Differentials
Total leukocyte counts and differentials were determined in whole blood at d 3, 7, and 14 after inoculation (Table 5). Pigs infected with PRRSV had an increased number of circulating neutrophils (P = 0.02), lymphocytes (P = 0.07), and total leukocytes (P = 0.01) 14 d after PRRSV inoculation. Also, infection with PRRSV increased (P < 0.01) the neutrophil:lymphocyte ratio at 3, 7, and 14 d after inoculation. Solutein reduced circulating neutrophils (P = 0.02), lymphocytes (P = 0.05), and total leukocytes (P = 0.02) 3 d after inoculation but otherwise had no effect (P = 0.08 to 0.92) on hematological traits measured. There was a trend for Solutein to reduce circulating neutrophils (P = 0.09) and total leukocytes (P = 0.06) in PRRSV-infected pigs on d 3 and to reduce the neutrophil:lymphocyte ratio (P = 0.09) on d 7. The number of leukocytes in lung lavage fluid was not affected by Solutein (P = 0.69) or PRRSV (P = 0.45) 7 d after inoculation (Table 6). However, infection with PRRSV dramatically increased leukocytes in lavage fluid collected 14 d after inoculation (P = 0.001). Supplementing water with Solutein did not mitigate (P = 0.64) the effects of PRRSV on the number of leukocytes in lung lavage fluid.
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Table 5. Effects of 2.5% (wt/wt) Solutein (American Protein Corporation Inc., Ankeny, IA) water supplementation and porcine reproductive and respiratory syndrome virus (PRRSV) infection on circulating white blood cell distribution in pigs1
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Table 6. Effects of 2.5% (wt/wt) Solutein (American Protein Corporation Inc., Ankeny, IA) water supplementation and porcine reproductive and respiratory syndrome virus (PRRSV) infection on total leukocytes in lung lavage fluid1
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DISCUSSION
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Inoculation with PRRSV induced a marked reduction in ADFI and ADG. Consistent with previous studies in our lab (Escobar et al., 2004), infection with PRRSV reduced ADFI and ADG by 32 and 40%, respectively, during the 2-wk period after inoculation. Addition of Solutein to drinking water did not mitigate the effects of PRRSV on growth performance. This finding is consistent with a previous study that showed dietary spray-dried plasma did not diminish the effects of LPS challenge on the growth performance of nursery pigs (Dritz et al., 1996a). Infection with PRRSV reduced water intake (i.e., disappearance) over the 2-wk period after inoculation, and the decrease in water intake caused by PRRSV was further exacerbated when Solutein was included. Nonetheless, based on water disappearance, we estimate PRRSV-infected pigs received 56 g of Solutein daily, which is substantially more than what they would receive in a typical nursery pig diet containing 2.5 to 5% spray-dried plasma (11 to 22 g/d, respectively).
Spray-dried plasma has been investigated primarily as a feed ingredient for early weaned pigs. To our best knowledge, there is just one published study in pigs that involved supplementing drinking water with soluble spray-dried plasma (Steidinger et al., 2002). Although Solutein in water did not mitigate the effects of PRRSV on growth performance, it had a unique and potentially important effect. Supplementing water with Solutein significantly reduced feed intake before as well as after inoculation with PRRSV; however, ADG was numerically greater for pigs given Solutein, so feed efficiency was markedly improved after accounting for the DM provided by Solutein. Pigs provided water with Solutein consumed 10% less feed but gained 6% more weight during the 2 wk after PRRSV inoculation; similar responses were evident before inoculation. These findings are generally consistent with those reported by Steidinger et al. (2002) when nursery pigs were provided drinking water supplemented with water-soluble plasma protein. Feeding diet containing spray-dried plasma has been reported to increase feed intake and weight gain (Coffey and Cromwell, 1995; Dritz et al., 1996b; Bergstrom et al., 1997), but several studies indicate that the efficacy of feeding spray-dried plasma wanes in experimental settings or management systems (e.g., segregated early weaning) where hygiene is superior (Coffey and Cromwell, 1995; Bergstrom et al., 1997). Therefore, the finding that providing Solutein in water reduced feed intake but maintained growth in a highly sanitized environment is noteworthy. Perhaps the extra nutrients obtained from drinking the Solutein contributed to the improved feed efficiency.
An interesting observation from this study was that PRRSV infection substantially reduced villus height and crypt depth in cranial, medial, and caudal regions of the small intestines. This effect of PRRSV was most likely caused by the reduction in feed intake. Newly weaned pigs experience a similar change in intestinal morphology that has been attributed to decreased feed intake (McCracken et al., 1999). Nonetheless, the fact that a respiratory pathogen can elicit profound and potentially significant changes in the gastrointestinal tract highlights the need for a comprehensive strategy to care for the convalescing animal. Although several studies found no beneficial effects of dietary spray-dried plasma on villus height and crypt depth in healthy pigs (van Dijk et al., 2001; Owusu-Asiedu et al., 2002; Touchette et al., 2002), others have reported improved intestinal morphology in plasma-fed pigs after pathogen exposure (Bosi et al., 2001, 2004). Thus, we thought spray-dried plasma might afford some protection to the small intestine of PRRSV-infected pigs. In this experiment, however, supplementing drinking water with Solutein did not affect villus height or crypt depth in pigs infected with PRRSV or noninfected controls.
There are recent reports that dietary spray-dried plasma may modify immunophysiological responses to pathogens. Consumption of spray-dried plasma for 35 d after weaning in rats reduced the stimulation of specific T-cell populations in gut-associated lymphoid tissue after i.p. injection of a Staphylococcus aureus enterotoxin B super antigen (Perez-Bosque et al., 2004). In pigs, consumption of a diet containing 6% spray-dried plasma for 14 d after weaning reduced intestinal tissue mRNA for tumor necrosis factor 
and IL-8 in pigs orally challenged with E. coli (Bosi et al., 2004). Early weaned pigs fed 7% spray-dried plasma from 14 to 21 d of age had greater serum levels of tumor necrosis factor and IFNafter injection with E. coli LPS compared with pigs fed diet without spray-dried plasma (Touchette et al., 2002). Feeding spray-dried plasma also enhanced the LPS-induced increase in serum adrenocorticotropin and cortisol (Carroll et al., 2002). However, investigating the efficacy of feed ingredients in a LPS-challenge model is difficult. For example, cytokines are necessary for orchestrating immunophysiological responses but can be injurious if overproduced. Because LPS acutely stimulates the immune system and does not mimic infection, it is difficult to know whether increased secretion of cytokines is beneficial or detrimental to the host. The current study overcame this shortcoming by evaluating the efficacy of Solutein in an infectious disease model. This was similar to a study in turkey poults in which spray-dried bovine plasma was provided in drinking water before and after inoculation with Pasteurella multocida, a pathogen that infects the respiratory tract and induces pneumonia (Campbell et al., 2004). In that study, spray-dried bovine plasma reduced mortality in turkey poults inoculated with Pasteurella multocida by more than 30%.
In our study, IL-1ß, an inflammatory cytokine produced primarily by activated macrophages and monocytes, and IFN-, a T-helper-1 cytokine that inhibits viral replication, were measured in control and infected pigs. Both cytokines were elevated in serum 7 d after PRRSV inoculation, and circulating concentration were not affected by addition of Solutein to drinking water. Had Solutein inhibited or enhanced the immune responses to PRRSV, one would have anticipated a concomitant change in circulating cytokines. Circulating WBC counts, WBC counts in lung lavage fluid and spleen, and lung weights provided further evidence that providing Solutein in water did not alter immune responses to PRRSV.
In summary, supplementing water with Solutein improved feed efficiency but did not afford pigs protection from the effects of PRRSV infection on growth and certain hematological traits. Thus, we conclude that it may be difficult to overcome the morbidity effects of PRRSV with Solutein. However, it should be noted that our study focused on the acute response to PRRSV. Furthermore, pigs in our study were housed in a highly sanitized environment, so exposure to secondary pathogens was minimized. In commercial settings, pigs are subjected to multiple pathogens and are more likely to develop secondary infections that may be affected by Solutein. This may be particularly important if virulent gastrointestinal pathogens are present because addition of spray-dried plasma to calf milk replacer was shown to reduce the duration of diarrhea and mortality in dairy calves (Quigley et al., 2002; Quigley and Wolfe, 2003). Furthermore, feeding spray-dried plasma reduced diarrhea and increased ADFI and ADG in nursery pigs orally inoculated with pathogenic E. coli bacteria (van Dijk et al., 2002; Bosi et al., 2004).
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Footnotes
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1 Present address: Department of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 
2 Corresponding author: rwjohn{at}uiuc.edu
Received for publication October 24, 2005.
Accepted for publication March 10, 2006.
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Abstract
INTRODUCTION
