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ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
Department of Animal Sciences, University of Illinois, Urbana 61801
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Abstract |
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0.15), performance (P 0.20), or CORT (P = 0.70) measures. Pig breed and age influenced both baseline immune measures and plasma CORT in growing pigs, suggesting that pig breed and age are important factors influencing the response to various stressors or infectious challenges.
Key Words: Age • Breed • Cortisol • Immune • Performance • Pig
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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), due mainly to decreased productivity and increased mortality. Selecting pigs for greater disease resistance may decrease disease occurrence, while increasing performance and productivity. Furthermore, differences in baseline immune and cortisol (CORT) profiles may reflect the susceptibility of an animal to infection and/or biological response to other stressors (Brown and Nestor, 1974; Hessing et al., 1995; Magnusson et al., 1998).
Genetic selection for antibody or adrenal responsiveness and its relationship to disease resistance have been studied in mice (Covelli et al., 1989), poultry (Brown and Nestor, 1974; Gross and Siegel, 1985), and pigs (Meeker et al., 1987, Magnusson et al., 1998). Yorkshire pigs selected for combined high or low antibody and cell-mediated immune responses differed in their reaction to a challenge by Mycoplasma hyorhinis, but no consistent line-related health advantages were found (Magnusson et al., 1998). Breed effects on immune traits and CORT in response to restraint stress (Rosochacki et al., 2000), a novel environment (Desautes et al., 1999), and bacterial challenge (Nguyen et al., 1998) have been reported in pigs. In pigs, various immune measures and CORT change with age (Hoskinson et al., 1990; Kattesh et al., 1990; Bianchi et al., 1995), and sex differences have been observed in basal CORT (Ruis et al., 1997).
Despite these few studies indicating differences within and between breeds in immune measures associated with stress, limited data are available comparing a wide range of baseline immune measures among several pig breeds, between sexes, or across ages. We hypothesize that breed composition, age, and gender are associated with differences in baseline immune status and CORT among different breeds of growing pigs at different ages. This study represents the establishment of baseline immune measures in diverse pig breeds.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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Body weight was recorded at weaning (17 to 21 d of age) and at each blood sampling time (e.g., 4, 8, and 12 wk of age). Feed disappearance was recorded and G:F calculated. The University of Illinois Institutional Animal Care and Use Committee approved all experimental procedures.
Blood Sample Collection
Pigs were held in a supine position, and 20 mL of blood was obtained by anterior vena cava puncture (procedure lasted approximately 1 min) at 4, 8, and 12 wk of age. Plasma CORT and immune measures were not affected by bleeding order (data not shown). Ten milliliters of blood was collected into Vacutainer tubes containing heparin (143 USP units), and 10 mL was collected into tubes containing EDTA (0.117 mL of 15% [K3] EDTA solution; 17.55 mg). Blood was collected using heparin for CORT and immunoglobulin G (IgG) assays and whole blood analysis. Blood collected using EDTA was used for cell isolation of specific cell populations and all other immune assays. Blood was collected in EDTA tubes specifically for chemotaxis and phagocytosis immune assays because it has been shown that heparin can activate the complement system (Repo et al., 1995), which could interfere with these specific measures.
White Blood Cell and Differential Counts
Heparin-treated whole blood was used to determine total white blood cell (WBC) counts and leukocyte differential counts (DIFF). Total WBC counts were made electronically using a Coulter Z1 particle counter (Beckman Coulter, Miami, FL). Whole blood (10 µL) was added to Isoflow (10 mL; Beckman Coulter), red blood cells (RBC) were lysed, and samples were placed in the counting chamber to determine total WBC count. To determine DIFF percentages, blood smears were made, fixed in methanol, and stained with Hema-3 staining system (Fisher Scientific, Houston, TX). Slides were viewed under a light microscope, and 100 cells per slide were visually counted.
Cortisol
Plasma samples from heparin-treated whole blood were assayed for CORT using a Coat-A-Count cortisol kit, following the manufacturer’s protocol (Diagnostic Products Corp., Los Angeles, CA). Briefly, in duplicate, 25 µL of sample or standard were added to antibody-coated tubes. Radiolabeled (I125) CORT was added to tubes and incubated 45 min at 37°C in a water bath. The liquid phase was decanted and radioactivity counted with a gamma counter. A standard curve based on 0, 10, 50, 100, 200, and 500 µg/mL was used. Intra- and interassay CV were 7.0 and 16.5%, respectively. Minimal detectable concentration of CORT using this assay was approximately 2 ng/mL.
Immunoglobulin G
An enzyme-linked immunosorbent assay was performed to measure total porcine IgG, as described by Morrow-Tesch et al. (1994), with minor modifications. Porcine plasma samples were diluted 1:3,000 in 0.05% Tween-PBS. In duplicate, 120 µL of diluted sample or standard was added to 96-well microtiter plates coated with porcine IgG (Jackson Immunoresearch, West Grove, PA). Rabbit anti-pig IgG (120 µL; Sigma, St. Louis, MO) was added to each well. Plates were incubated for 2 h at room temperature and washed three times with 0.05% Tween-PBS. Enzyme-linked anti-rabbit IgG (200 µL; Jackson Immunoresearch) was added at 1:7,500 and incubated for 1 h, and plates decanted and washed three times. Substrate solution (200 µL; 1 mg/mL of p-nitrophenyl phosphate; Sigma) was added to each well. After 30-min incubation, the reaction was stopped with 100 µL of 2 M NaOH, and plates were read using a microplate reader (Bio-Tek Instruments, Winooski, VT) at a wavelength 405 nm. A standard curve (0, 0.1, 0.5, 1, 5, 10, 20, and 40 µg/mL) was used.
Cell Isolation
Porcine lymphocytes and neutrophils were isolated from EDTA-treated blood by density gradient centrifugation using Histopaque-1077 (density = 1.077 g/mL; Sigma) and Histopaque-1119 (density = 1.119 g/mL; Sigma). Briefly, whole blood was diluted with Roswell Park Memorial Institute (RPMI) and layered over Histopaque-1077 and 1119 (Sigma), then centrifuged at 700 x g for 30 min at room temperature. Lymphocytes were collected from the 1077 layer, washed twice in RPMI, resuspended, and counted. Neutrophils and RBC were removed from the 1119 layer and washed once in RPMI. Cold endotoxin-free water (27 mL) was added to the neutrophil and RBC combination to lyse the RBC, and after 1 min, 3 mL of 10x PBS was added to restore isotonicity. Neutrophils were centrifuged for 10 min at 475 x g, supernatant fractions were decanted, and the pellet was resuspended and washed twice in RPMI.
Natural Killer Cytotoxicity
Natural killer (NK) cytotoxicity was measured using a commercially available nonradioactive cytotoxicity detection kit, following the manufacturer’s protocol (Roche Diagnostics, Indianapolis, IN) and a radioactive NK assay protocol originally described by Lumpkin and McGlone (1992) with modifications. Briefly, porcine lymphocytes were used as the effector cells and K-562 chronic human myelogenous leukemia cells (American Tissue Type Culture Collection, Manassas, VA) as the target cells. Lymphocytes were adjusted to 1 x 107 cells/mL and K562 cells were adjusted to a constant 10,000 cells per well. Samples were run in triplicate at effector (lymphocytes) to target-cell (K-562) ratios of 12.5:1, 25:1, 50:1, and 100:1. Plates were read using a microplate reader (Bio-Tek Instruments) at a wavelength 490 nm with a reference wavelength of 690 nm. The assay was considered valid if maximum release divided by spontaneous release was <30%. Percent cytotoxicity was calculated as described in Lumpkin and McGlone (1992).
Neutrophil Chemotaxis, and Phagocytosis
Porcine neutrophils were adjusted to 3 x 106 cells/mL in RPMI. The ability of neutrophils to migrate toward assay medium (control; random migration) or RPMI plus recombinant human complement-5a (hC5a; Sigma; chemotaxis [CHTX]; directed migration] was measured using an assay described by Salak et al. (1993). Briefly, in duplicate, 30 µL of medium, hC5a (10–7 M), was added to the bottom wells of a 48-well microchemotaxis chamber (Neuro Probe, Gaithersburg, MD), and the chamber placed in an incubator for thermal equilibration. In the top wells of the chamber, 50 µL of purified porcine neutrophils was added, and the chamber incubated for 45 min at 37°C under 5% CO2 in a humidified incubator. A polyvinyl pyrrolidone-free filter (pore size 5 µm; Neuro Probe) was fixed and stained using the Hema-3 system (Fisher Scientific). A technician having no knowledge of treatments counted cells that migrated to the underside of the filter. Four fields per well were counted using a light microscope at 100x, and duplicates were averaged.
Neutrophil phagocytosis (PHAGO) was measured using a flow-cytometry–based assay as described by Jolie et al. (1997), with minor modifications. Porcine neutrophils were counted and adjusted to 2 x 106 in RPMI. Fluorescent beads (yellow-green, 1.0 µm; Molecular Probes, Eugene, OR) were added to each sample at 10:1. Before being added to each sample, beads were incubated for 45 min at room temperature in nonheat-inactivated porcine serum. Samples were protected from light and incubated for 40 min at 37°C while rotating, then centrifuged for 5 min at 1,000 x g. Samples were washed once in RPMI, decanted, and fixed in 4% paraformaldehyde. Samples were protected from light and held at 4°C until analyzed. Percent fluorescence was measured using an XL flow cytometer (Beckman Coulter). Data were transformed logarithmically. Results are expressed as total percentage of neutrophils engulfing one or more beads.
Statistical Analyses
All traits were tested for departures from normal distribution. Measures lacking normality and on which a natural logarithmic transformation was applied included neutrophil counts, percentages of eosinophils, IgG, and CORT, respectively, and NK cytotoxicity. Minimum values for percentages of monocytes, eosinophils, and PHAGO, respectively, were zero; thus, a value smaller than the lowest nonzero number was added to all observed values to allow for logarithmic transformation. A linear mixed-effects model was used to analyze these variables using the Mixed procedure of SAS (SAS Inst., Inc., Cary, NC). The main fixed effects included in the model were breed (five levels), sex (two levels), and age (three levels). All second-order interactions were evaluated and removed from the model when not significant at an 
level of 0.05. Random effects included in the model were litter and pen. The model had a repeated structure on age allowing incorporation of heterogeneity of variances across ages. Residuals were tested for departures from assumptions.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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0.15), performance measure (P 0.20), or plasma CORT (P = 0.70; Table 1).
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. At 4 and 8 wk of age, White X and Yorkshire pigs had the greatest (P < 0.001) BW gains compared with Meishans and Durocs. By 12 wk of age, BW gains were similar among Duroc, White X, and Yorkshire pigs; the Meishans gained the least (P < 0.001). Yorkshires had the greatest BW gain over the study duration and the least (P < 0.001) G:F. At 12 wk of age, Duroc pigs had the greatest (P < 0.001) G:F, and Meishans had the least (P < 0.001). Data from Berkshire pigs are not shown because of missing observations.
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). At 4 wk of age, Berkshire pigs had the greatest (P < 0.001) neutrophil and lymphocyte counts compared with all other breeds. Conversely, at 12 wk of age, Berkshires had the least (P < 0.001) neutrophil and lymphocyte counts.
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), whereas the percentage of lymphocytes increased (age: P < 0.001; breed x age: P < 0.001; due to decreasing percentage neutrophils). At all ages, Berkshire pigs had the greatest (P < 0.001) percentage of neutrophils and least (P < 0.001) percentage of lymphocytes. The percentage of monocytes and eosinophils differed among breeds and over time (breed: P < 0.001; breed x age: P < 0.001), but there was no consistent breed or age trend.
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). At 4 wk of age, Meishans and Durocs had the greatest (P < 0.05) plasma CORT, and Yorkshires had the least (P < 0.05). At 8 wk, Meishans still had the greatest (P < 0.05) CORT, but Berkshire, Duroc, and White X pigs had similar CORT concentrations, and Yorkshires had the least (P < 0.05). By 12 wk of age, however, Meishans had the greatest (P < 0.05) plasma CORT, whereas all other breeds had similar concentrations.
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). At 4 wk of age, IgG concentrations were greater (P < 0.005) in Meishan than in White X, Yorkshire, or Duroc pigs. Conversely, at 12 wk, Meishans had less (P < 0.005) plasma IgG than either Berkshires or Yorkshires.
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). Natural killer cytotoxicity was less (P < 0.001) in White X pigs than Duroc, Meishan, or Yorkshire pigs.
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). At 4 wk of age, PHAGO was greater (P < 0.001) in Yorkshire pigs than in Duroc, White X, or Meishan pigs; however, at 12 wk, PHAGO did not differ across breeds. Berkshire data are not shown because of missing observations.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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, who reported no gender difference in CORT concentrations between 6-wk-old Large White and Meishan pigs. At the ages evaluated here, pig gender did not influence immune measures; however, in the present study, there were breed and age differences for immune status, CORT, and performance among the five breeds of pigs evaluated.
Overall, we found that BW gain was greatest in Yorkshire pigs and least in Meishans. In previous research, Yen et al. (1991) reported that ADG and G:F were less in purebred Meishan pigs than in Duroc x White cross pigs. Furthermore, BW gain and feed intake have been found to be greater in Large White boars than in Meishans (Weiler et al., 1998). These differences may be attributed to high selection pressure in modern pig breeds, with emphasis on rapid BW gain and increased lean tissue, whereas genetic selection in Meishans has emphasized reproductive traits (Weiler et al., 1998).
Plasma CORT was measured in this study as an indicator of baseline hypothalamic-pituitary-adrenal axis activation and often glucocorticoids have been shown to influence various immune responses. Regardless of age, Meishan pigs had the greatest plasma CORT concentrations of all breeds surveyed here. These results agree with previous findings, in which Meishan, F1 crosses (Meishan x Large White), and F2 crosses (F1 x F1) had greater CORT concentrations than did Large White pigs (Desautes et al., 1997, 1999; Weiler et al., 1998). In contrast, Reed and McGlone (2000) found no differences in CORT concentrations between 25% Meishans and a commercial line of White pigs. Differences in CORT concentrations between Meishans and White pigs may result from increased selection pressure for growth potential and carcass leanness, which may have inadvertently resulted in decreased glucocorticoid secretions in White pigs (Weiler et al., 1998). Furthermore, increased CORT concentrations in Meishans compared with Large Whites might be due to enhanced secretory activity of the adrenal gland. Urinary excretions of CORT, cortisone, and catecholamines are greater in Meishans than in Large Whites (Hay and Mormede, 1998). In addition, differences between Meishans and Large Whites in the mineralocorticoid and glucocorticoid receptor balance in the hippocampus and pituitary gland could contribute to the greater CORT concentrations observed in Meishan pigs (Perreau et al., 1999).
Plasma CORT increased over time in all breeds. It has been reported that CORT concentrations are greatest at birth, decrease by 3 d of age, and then remain unchanged through 42 d of age (McCauley and Hartmann, 1984; Kattesh et al., 1990). In the present study, plasma CORT did increase from 4 to 8 wk of age, but it was not different at 8 and 12 wk. It is assumed that the difference in plasma CORT between 4- and 8-wk-old pigs was not due to bleeding or handling techniques because the same techniques were used at both ages. Furthermore, if the differences in CORT concentrations were due to bleeding and handling techniques, one would expect to see differences in plasma CORT between 8 and 12 wk of age because pigs are more difficult to handle at 12 wk compared with 4 and 8 wk.
Total plasma IgG concentrations were measured in this study to assess baseline antibody concentrations among different pig breeds. Plasma IgG concentrations were greater in Berkshire pigs than in the other pig breeds, except for Meishans. In accordance with our findings, no difference in IgG concentrations were found between 4-wk-old Durocs and Large Whites (Nguygen et al., 1998) or between a commercial White line and 25% Meishan weanling pigs (Reed and McGlone, 2000). In our study, it is possible that the greater IgG concentration found among Berkshire pigs resulted from a cryptic challenge to the immune system in these animals, as evidenced by the unusually high percentages of neutrophils and leukocytes in these animals.
Plasma IgG concentrations increased in all breeds over time, except that it decreased in Meishans. In pigs, serum IgG concentrations decrease after birth, then increase once again starting at 7 wk of age (Bianchi et al., 1995). The maternally derived IgG in serum decreases shortly after birth, so the increase at approximately 7 wk may be due predominantly to de novo synthesis of IgG (Klobasa et al., 1986; Bianchi et al., 1995). Therefore, in this study, it is speculated that the differences in IgG concentrations detected among the different breeds at 8 and 12 wk of age reflect actual breed differences and not maternally derived IgG concentrations. In contrast, at 4 wk of age IgG concentrations are most likely due predominantly to maternally derived IgG concentrations; thus, these differences in IgG concentrations may be more reflective of maternal antibodies or the disease status of the sow.
It is unclear why plasma IgG had decreased by 12 wk in the Meishans. We speculate this response might be related to the immunologic competence or maturation of pigs of this particular breed. Meishan pigs have been reported to reach puberty approximately 100 d earlier than Large White pigs (Bazer et al., 1988), and this difference in maturation rate of the reproductive system may be associated with faster maturation of other systems, as well. Furthermore, lower IgG concentrations in Meishans at 12 wk of age may be associated with decreased innate immunity in these animals compared with pigs of other domestic breeds. A study that involves an immune challenge comparing Meishan pigs with other domestic pig breeds could provide important information that would enable one to determine whether the lower IgG concentrations found among the Meishans piglets at 12 wk of age reflect a lower innate immune response or simply a breed difference. Furthermore, it is imperative to measure the relative concentrations of the different immunoglobulin isotopes to increase our understanding of breed differences in antibody production that could be associated with differences in disease resistance among pig breeds.
In the present study, NK cytotoxicity served as an in vitro measure of innate immunity associated with natural killer lymphocyte function. Natural killer cytotoxicity was greater in Meishans than in White X or Duroc pigs, and White X pigs had less NK activity than Durocs or Yorkshires. Reed and McGlone (2000) reported that 25% Meishan pigs had a 17% increase in NK activity compared with a White commercial line pig. It has been suggested that increased adrenal corticosteroid concentrations are immunosuppressive (Brown-Borg et al., 1993; Deguchi and Akuzawa, 1998). In this study, however, we found no correlation between plasma CORT concentrations and NK activity in Meishan pigs (data not shown). Furthermore, Salak-Johnson et al. (1996) reported that normal physiologic concentrations of CORT did not influence NK activity in 7- to 9-wk-old crossbred pigs. Wrona et al. (2001) showed that NK activity in 10- to 12-wk-old Landrace pigs was not directly related to CORT concentrations. Suppressed NK activity in animals and humans has been associated with increased likelihood of illness associated with a viral infection (Glaser and Kiecolt-Glasser, 1998). Therefore, the enhanced NK activity in Meishans could lead to increased resistance to a viral challenge. In fact, improved healing of lung lesions in PRRS virus-infected Meishan pigs compared with Hampshires suggests that enhanced NK activity in Meishans may be beneficial to their defenses against viral infections (Halbur et al., 1998). Furthermore, it would be useful to include a target cell infected with a specific swine pathogen in conjunction with the K-562 cell line as a comparison of functional activity of pig NK cells among breeds when evaluating in vitro NK cytotoxicity to enhance our understanding of genetic potential of pig breeds.
Neutrophil PHAGO and CHTX are mechanisms of phagocytic cells, which are essential to host innate defenses against pathogenic microorganisms. Chemotaxis was used to measure the ability of neutrophils to migrate toward a specific chemoattractant, and PHAGO was used to measure the ability of neutrophils to engulf a foreign particle (i.e., serum-coated fluorescent bead). Both PHAGO and CHTX were used in this study, so that one could determine whether there were differences in these basic neutrophil functions among the different breeds of pigs. The percentage of neutrophils that migrated in response to the chemoattractant hC5a was less in Meishans compared with White X pigs. Reed and McGlone (2000) found that 25% Meishans had a less neutrophil CHTX in response to hC5a than did a White commercial line pig. In contrast to results obtained for neutrophil CHTX, for which Yorkshire pigs had the least CHTX, their PHAGO response was the greatest. Despite the fact that, overall, Yorkshire pigs had fewer neutrophils migrating in response hC5a, these pigs had the greatest percentage of neutrophils engulfing beads. These findings indicate, thus, in these Yorkshire pigs, the ability of neutrophils to engulf beads may not depend on the migratory capabilities of the neutrophil. These findings support that different functional aspects of porcine neutrophils are influenced by breed, thereby making it difficult to generalize about the effect a particular breed has on the innate immune system.
Innate immune responses, as measured by neutrophil CHTX and PHAGO were variable among breeds at 4 and 8 wk of age, but this age effect on CHTX and PHAGO does not seem to be related to percentage of neutrophils or neutrophil number, due to the fact that a consistent number of cells are used for both assays. In this study, cell counts and percents were not indicative of a particular cell type’s functional abilities.
In the present study, different aspects of the innate immune system were measured. In future studies, other specific immune variables should be included to help further assess the interactions between pig breed and disease resistance, including the assessment of specific cell phenotypes and the relative frequencies of these different sub-types of leukocytes. Furthermore, the responsiveness of these various cell types to a specific disease challenge should be assessed.
A breed x age interaction was observed for many of the variables that we assessed. Breed effects on baseline immune status across time may reflect differences in developmental aspects of the immune system across breeds. Although our study was not designed to characterize developmental aspects of the immune components assessed here, age of pig seemed to be an important factor influencing baseline immune status across breeds. Neutrophil CHTX and PHAGO varied across breeds at 4 and 8 wk of age, but by 12 wk, they were similar across breeds. Furthermore, plasma IgG concentration increased over time in most breeds, although it decreased in Meishan pigs.
There were marked breed differences in the baseline immune measures assessed as well as plasma CORT concentrations. Natural killer cytotoxicity was greatest in Meishans and least in White X. Conversely, neutrophil CHTX and PHAGO were greatest in the White breeds. These differences in baseline immune status may suggest that breeds with greater basal NK cytotoxicity are more effective at combating viral challenges, and conversely that those breeds with greater basal CHTX and PHAGO activity may be better able to defend themselves against bacterial challenges. It would be of interest to know whether these differentials actually exist and whether the respective efficacies of the different components of the immune system change with age. At present, we do not know whether a greater or less immune response is indicative of altered disease susceptibility. Further research will be required to address these issues.
Because of the apparent effects of age on the immune measures assessed in the present study, caution should be taken with respect to age when designing experiments to study immune traits, especially across breeds. Distinct breed differences in in vitro baseline immune status and plasma CORT may be useful indicators of how a pig of a particular breed will respond to a microbial challenge or some other sort of stress. Baseline immune status also might be a useful indicator of susceptibility of an animal to infection induced by bacteria, viruses, or both, but these relationships remain to be documented.
There were marked breed differences in the baseline plasma CORT and immune measures evaluated in this study among the various pig breeds. To further determine whether these differences among breeds of pigs in baseline immune measures reflect susceptibility of an animal to disease, it would be important to assess the immune system in pigs that were challenged with a specific pathogen. Furthermore, caution should be taken with respect to age when designing experiments to study immune traits because age apparently influences aspects of innate immunity.
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Footnotes |
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2 Correspondence: 392 Animal Science Lab, 1207 West Gregory Drive (phone: 217-333-2118; fax: 217-333-8286; email: johnso17{at}uiuc.edu).
Received for publication March 22, 2005. Accepted for publication May 12, 2005.
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
), Duroc (
), Meishan (
), Landrace x Yorkshire (White X; 
), and Yorkshire (*) pigs at 4, 8, and 12 wk of age. Numbers of pigs per breed group were as follows: Berkshire (36), Duroc (18), Meishan (54), White X (36), and Yorkshire (36). There was a genotype x age interaction for cortisol, P < 0.02. At each age, means with different letters differ, P < 0.05.
