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Effects of fermented soybean meal on immune response of weaned calves with experimentally induced lipopolysaccharide challenge.

INTRODUCTION

Weaning remains a critical phase in domestic animal production in association with digestive disorders causing growth retardation and diarrhea. Weaning is known to heighten susceptibility of calves to a variety of infectious diseases due to the attenuation of the immune system under high stress conditions including weaning, diet changes, and group rearrangement (Hickery et al., 2003). Thus, there is a tremendous interest in finding effective dietary stress reducers and/or immune enhancers that may improve the disease resistance in weaned calves. As a protein source, soybean meal (SBM) is a common and widely used component in farm animal diets. However, due to the existence of various anti-nutritional factors (ANFs), the application of SBM as a diet for young animals has been limited (Dunsford et al., 1989; Li et al., 1990; Jiang et al., 2000). It has been known that the fermentation process with elimination of microbes and/or reduction of ANFs will make high-quality components available to young animals and thus increase the digestibility (Feng et al., 2007; Yoo et al., 2009; Chiang et al., 2010). Fermented soybean meal (FSBM) contains a variety of important nutrients including calcium and vitamins produced during the fermentation process, which should provide functional properties, such as growth promoting effect, and enhacing effect in feed efficiency (Lee, 1998; Kim et al., 1999; Feng et al., 2007). Moreover, previous studies have shown that small-sized peptides in FSBM increased the concentration of immunoglobulins in domestic animal (Wang et al., 2003; Feng et al., 2007). Some data on the effect of FSBM in enhancing immune responses through the increase of serum proteins in calves have been reported (Wolfswinkel, 2009; Kim et al., 2010). Cortisol is a representative stress hormone and is secreted at high levels in response to stress. Under environmental and metabolic stress, the secretion of cortisol is associated with stress-related changes in the animal such as the down-regulation of interferon-[gamma] (IFN-[gamma]), interleukin-1 (IL-1), interleukin-2 (IL-2), interleukin-3 (IL-3), granulocyte-macrophage colony-stimulating factor (GM-CSF), tumor necrosis factor (TNF-[alpha], interleukin-6 (IL-6), and interleukin-8 (IL-8) (Fingerle-Rowson et al., 2003). Haptoglobin (Hp), a hemoglobin binding protein, is a representative acute phase protein (APP) in cattle, which is stimulated by inflammatory mediators and produced by liver. It has been shown that concentration of Hp increased up to 100-1,000 folds within 24 h after inflammatory response following gram-negative bacterial infection (Chan et al., 2004).

The hypothesis of this study was that supplementation of FSBM, instead of regular SBM, might reduce the stress response against weaning and improve the production of immune function-related serum proteins against lipopolysaccharide (LPS) challenge in calves. Therefore, the current study was carried out to evaluate the effects of FSBM (fermented A. oryzae) in calf diet based on the level of cortisol hormone and production of immune-related serum proteins in weaned calves after LPS challenge.

MATERIALS AND METHODS

Animal, management and diet

The present experiments were carried out at Dairy Science Division, National Livestock Research Institute, Korea. All experimental procedures were reviewed and approved by the ethics committee on the use of animals in research, National Livestock Research Institute, Korea. Holstein calves (n = 21; 8 males and 13 females, mean BW = 42.2 [+ or -] 6.15 kg) were separated from their mothers within 2 hr of birth, weighed, and moved to pens with automatic milk-feeders offering no possibility of direct contact among calves, and fed colostrum at 10% of their body weight for the first 3 days. The calves were allowed free access to a calf starter, mixed grass hay, and water from a plastic bucket. All calves were fed a milk replacer using automatic milk-feeders according to step-down milking method (Khan et al., 2007). The milk replacer was provided at the rate of 20% of body weight until 28 days of age, then this rate gradually reduced to 10% at 29 to 30 days old and fed for the remaining 21 days of the preweaning period. All calves were weaned at 7 weeks old. The ingredients and major chemical composition are shown in Table 1. Calves were randomly allocated to two experimental diet groups (FSBM group = 8 calves, 3 males and 5 females; SBM group = 8 calves, 2 males and 6 females). Two experimental diets were given ad libitum throughout the experimental period. Additional Holstein calves (n = 5; 3 males and 2 females, mean BW = 44.6 [+ or -] 7.89 kg) were assigned as a negative control group (fed SBM diet) and received phosphate buffered saline (PBS) only. FSBM calf starter diet contained fermented SBM (a commercial product produced by Gene Biotech Corp., Gongju, Chungnam, Korea) substituting SBM diet. The major chemical composition of calf starter was similar between the groups.

Feed intake and growth performance

Automatic milk-feeders were used to record the intake of milk replacer, calf starter, and forage from week 1 to week 7. Overall average body weight (BW) gain was calculated from change of BW measured at weekly basis.

LPS challenge

Each calf was injected subcutaneously with 100 ng/kg BW of Salmonella typhimurium LPS (Sigma-Aldrich Co., St.Louis, MO), reconstituted with non-pyrogenic PBS, on day 7 (D7) after weaning (56 days old).

Blood sampling and hematology

The blood sampling was done as shown in Figure 1. For the hematological test and serum proteins, 5 ml of blood was drawn from jugular vein at 54 (D5), 61 (D12) and 68 (D19) days old. Additional 10 ml of blood samples were collected into evacuated tubes coated with the anticoagulant lithium-heparin vacutainer (BD-plymouth, PL6 7BP, UK) at 32 (D-17) and 39 (D-10) days old for cortisol assay and at 57 (D8) and 59 (D10) days old for the haptoglobin ELISA assay. Additional blood (10 ml) was collected for the ELISA and hematological assay.

[FIGURE 1 OMITTED]

After centrifugation of the blood sample at 1,600xg at 4[degrees]C for 15 min, plasma was harvested from anti-coagulated blood and stored at -80[degrees]C until further assays were conducted. Neutrophil, lymphocyte, platelet, monocyte and leukocyte population in whole blood were measured with an automatic analyzer (Hemavet 850, Drew Scientific Group Company, USA).

Enzyme-linked immunosorbent assay (ELISA)

The concentration of haptoglobin (Life Diagnostics, Inc), cortisol (Oxford Biomedical Research Inc., Oxford) and total immunoglobulins (Bethyl laboratory Montgomery, TX) was determined using an ELISA assay kit according to the procedure of the manufacturer. The concentration of specific IgG, IgM and IgA antibodies in serum against LPS was determined as described by Trautmann et al. (1998). In brief, LPS was coated in 96-well immunoplates (Nalgene Nunc International) and incubated overnight at 4[degrees]C. Then, the plates were washed with washing buffer (0.05% Tween 20 in PBS) 3 times and blocked with washing buffer (0.05% Tween 20 in PBS) for 2 h. The plates were incubated with diluted serum samples for 3 h at room temperature and washed 3 times with washing buffer. Anti-bovine antibodies (IgG, IgA and IgM) conjugated with horseradish peroxidase (HRP) was added to the plates and incubated for 2 h. After the washing, specific binding was detected using streptavidin-HRP and tetramethylbenzidine (TMB) substrate (Sigma-Aldrich). To stop the reaction, 2 N [H.sub.2]S[O.sub.4] was added to the plates. Absorbance was measured at 450 nm using a microplate reader (Molecular Devices).

Statistical analysis

All data were analyzed by ANOVA procedure for randomized complete block desings using the GLM procedures of SAS (SAS Inst. Inc., Cary, NC). Differences among means were tested using tukey procedure of SAS. Effects were considered significant at p<0.05.

RESULTS

Changes of immunophysiological characteristics in negative control calves

Overall changes of immunophysiological parameters in serum from negative control calves are presented in Table 3. The level of platelet was significantly (p<0.05) increased at D19 when compared to D5. No significant changes in the other hematological profiles were detected during the experimental period.

Hematology

Hematological parameters in calves before and after LPS administration are presented in Table 4. Similar to negative control group, the concentration of platelet in SBM group was significantly (p<0.05) increased at D12 and D19 when compared to the value at D5. Interestingly, however, the changes on the concentration of platelet in FSBM group were not significant.

Cortisol level

Overall concentration of cortisol in FSBM group was lower than that of SBM group (Figure 2). The level of cortisol in calves fed with FSBM diet had significantly (p<0.05) lower than those fed with SBM diet at 1 day after milk reduction (D-17) and after LPS challenge (D8).

Total serum and antigen-specific immunoglobulin (Ig) production

Total serum IgG and IgA concentration was significantly (p<0.05) increased at D19 in calves fed both experimental diets when compared to those at D5 (Table 5). The concentration of LPS-specific IgG in FSBM group was significantly (p<0.05) higher than that of SBM group at D12 and D19 (Figure 3A). Although there was a tendency to increase in LPS-specific IgM level in both groups during the experimental period, it was not significant when compared to those at D5 (Figure 3C).

Haptoglobin (Hp) level

After LPS challenge, the significant (p<0.05) elevation of serum haptoglobin (Hp) was observed in FSBM group at D8 compared to D5 (Figure 4). The level of serum Hp from calves fed FSBM diet was significantly (p<0.05) higher than calves fed SBM diet at D8 (Figure 4).

DISCUSSION

An acute stress response can be provoked by rapid nutritional and environmental changes, for instance weaning, which may result in reduced resistance to disease and loss of normal body condition partly due to a decrease in feed intake. Therefore, effective dietary stress reducer or immune enhancer is a great interest in animal feed industry. The current study was conducted to evaluate effects of FSBM as a stress reducer based on on immune responses in calves after LPS challenge following weaning.

[FIGURE 2 OMITTED]

In the current study, no difference in BW was found between treatments and milk intake in calves fed two different calf starters (Table 2). The data from calves without LPS challenge indicated that there was no time effect on immunophysiological characteristics during the experimental period. In other words, significant changes on immunophysiological parameters were not observed by natural aging during the experimental period. Therefore, it is reasonable to conclude that if any significant changes of biomarkers for immune function including hematological changes and immunoglobulin levels in serum were observed in the present study, then it would be the effects of dietary treatment and/or LPS challenge.

In the present study, the concentration of serum cortisol known as a stress marker was significantly higher in SBM group than FSBM group at one day after 1st milk reduction. Many studies have evaluated essential amino acids, such as tryptophan, glutamine, and arginine, and their impact on the response of animals to stress (Yi et al., 2005; Guzik et al., 2006; Jiang et al., 2009; Zheng et at., 2010). The results showed that feeding supplementation of amino acids reduced the cortisol response when an acute stressor including weaning or infection with microbes was introduced. Meanwhile, Chan et al. (1975) and Min et al. (2009) suggested that the FSBM might have a growth promoting activity owing to higher supply of essential amino acids and possibly vitamins synthesized during the fermentation. Therefore, lower cortisol in FSBM group in present study may also be explained in a similar manner in that FSBM could alleviate the stress response due to a greater supply of essential amino acids and possible vitamins synthesized by the fungi fermentation. Current results also showed that total serum IgA and IgM levels significantly increased in both groups compared to those before the challenge, which may indicate that the LPS challenge model successfully induced humoral response. It is to note that the significant increase in LPS-specific IgG and IgA levels after LPS challenge were observed in calves fed with FSBM and the level was higher than those fed with SBM, indicating that calves fed FSBM diet coped with LPS challenge more efficiently. It is widely accepted that nutritional and environmental stresses enhance the secretion of cortisol, which intensely suppresses immunoglobulin production (Sabbele et al., 1983; Wiik et al., 1989; Nagae et al., 1994). Besides, during an infection with microbes, the demand for essential amino acids such as glutamine and arginine dramatically increases. Under the stressed condition, glutamine is used as a carbon source by immune cells for proliferation (Newsholme and Calder, 1997) and arginine is also required for the production of nitric oxide, a potent immunoregulatory mediator (Evoy et al., 1998). Hence, our results suggested that FSBM may have benefical effects on attenuating stress response and enhancing B-cell response partly through supply of essential amino acids and small peptides.

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

In the current experimental model, subcutaneous LPS injection induced the changes in serum haptoglobin (Hp). LPS from gram-negative bacteria is known to be potent inducers of inflammation and the acute phase response, giving rise to large changes in the serum concentrations of acute phase proteins such as Hp, serum amyloid A, and albumin (Boosman et al., 1989; Werling et al., 1996). The concentration of serum Hp from our study was also significantly elevated in FSBM group in response to LPS challenge, similar to results of LPS-specific antibodies. This result implies that small sized peptides and essential amino acids in FSBM facilitated the production of acute phase protein in the same way as antibody production.

In conclusion, feeding FSBM as calf starter in calves reduced cortisol response and enhanced production of immune-related serum proteins, particularly LPS-specific IgG and IgA, and haptoglobin against LPS challenge. Therefore, FSBM may have beneficial effects on alleviating weaning stress and enhancing immune status of weaned calves.

doi: 10.5713/ajas.2011.10419

ACKNOWLEDGEMENTS

This work was supported by the Korea Science and Engineering Foundation (KOSEF) granted by the Korean government (MEST) (R01-2008-000-10854-0).

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In Hyuk Kwon (1), Myung Hoo Kim (1), Cheol-Heui Yun (1,2), Jong Yeol Go (3), Chan Ho Lee (4), Hyun June Lee (5), Wisut Phipek (6) and Jong K Ha (1) *

(1) Department of Agricultural Biotechnology and Research Institute for Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University, Seoul 151-742, Korea

* Corresponding Author : Jong K. Ha. Tel: +82-2-880-4809, Fax: +82-2-785-8710, E-mail: jongha@snu.ac.kr

(2) Center for Agricultural Biomaterials, Seoul National University, 599 Gwanangno, Gwanak-gu, Seoul 151-921, Korea.

(3) Nonghyup Feed Inc., Seoul 134-763, Korea.

(4) Genebiotech co., Ltd., Gongju 314-831, Korea.

(5) Dairy Science Division, National Institute of Animal Science, Cheonan 330-801, Korea.

(6) Phranakhon Rajabhat University, Bangkok 10220, Thailand.

Received November 19, 2010; Accepted March 18, 2011
Table 1. Ingredient and major chemical composition of diets

Ingredient (% DM)         SBM group     FSBM1 group

Ground corn                 42.50          45.14
Soybean meal (SBM)          16.00
Fermented SBM (FSBM)                       13.36
Rapeseed meal                2.00           2.00
Corn germ meal               4.00           4.00
Corn gluten meal            12.00          12.00
Wheat hulls                 12.00          12.00
Whole soybean                3.00           3.00
Alfalfa pellet               1.50           1.50
Milk replacer                2.00           2.00
Molasses                     4.00           4.00
Salt                         0.20           0.20
Ca[Co.sub.3]                 0.25           0.25
Mixed mineral                0.46           0.46
Vitamin AD3                 0.072          0.072
L-lysine                     0.01           0.01
Virgininamycin              0.008          0.008
DM                          86.36          86.88
TDN (2)                     74.33          74.42
CP                          23.31          23.51
Ca                           0.42           0.38
P                            0.48           0.46

(1) FSBM = Fermented SBM, A.orzae.

(2) TDN = Total digestible NFC+total digestible CP+total digestible FA
x2.25 +total digestible NDF-7.

Table 2. Average body weight and milk intake in calves fed with
SBM or FSBM calf starter during the experimental period

                        SBM group                FSBM group

Body weight
  0 day            40.57 [+ or -] 4.65      43.71 [+ or -] 5.82
  7 day            41.71 [+ or -] 6.30      45.36 [+ or -] 4.45
  14 day           42.50 [+ or -] 5.12      46.61 [+ or -] 4.83
  28 day           47.00 [+ or -] 5.75      49.86 [+ or -] 6.90
  42 day           51.21 [+ or -] 6.56      56.14 [+ or -] 6.92
  49 day           58.29 [+ or -] 13.12     61.29 [+ or -] 7.01
Milk intake
  1 week            4.86 [+ or -] 2.95       4.75 [+ or -] 2.66
  2 week           34.21 [+ or -] 8.21      34.11 [+ or -] 17.45
  3 week           42.86 [+ or -] 15.94     36.65 [+ or -] 3.03
  4 week           38.36 [+ or -] 10.38     36.08 [+ or -] 9.80
  5 week           25.99 [+ or -] 6.22      27.69 [+ or -] 3.33
  6 week           26.65 [+ or -] 4.57      30.93 [+ or -] 6.34
  7 week           17.45 [+ or -] 5.30      15.56 [+ or -] 2.82

Table 3. Changes of hematological parameters and total serum and
LPS-specific immunoglobulins in calves fed with SBM diet as
negative-control group at pre-and post-LPS challenge (mean [+ or -]
SD)

                                          D51

Hematological change
  NE (2) (%)                      25.81 [+ or -] 9.30
  LY (3) (%)                      64.28 [+ or -] 8.21
  NE:LY                            0.42 [+ or -] 0.21
  Leukocytes ([10.sup.9]/L)        5.65 [+ or -] 1.68
  Platelet ([10.sup.9]/L)        200.00 [+ or -] 136.0 (b)
Total serum antibodies
  IgG (4)                         17.46 [+ or -] 4.49
  IgA (5)                         59.52 [+ or -] 9.45
  IgM (6)                          0.91 [+ or -] 0.33
LPS specific antibodies (7)
  IgG                             0.325 [+ or -] 0.077
  IgA                             0.132 [+ or -] 0.139
  IgM                             0.754 [+ or -] 0.492

                                          D12

Hematological change
  NE (2) (%)                      54.58 [+ or -] 18.82
  LY (3) (%)                      41.81 [+ or -] 17.01
  NE:LY                            1.54 [+ or -] 0.87
  Leukocytes ([10.sup.9]/L)        9.49 [+ or -] 3.34
  Platelet ([10.sup.9]/L)        380.00 [+ or -] 137.9 (ab)
Total serum antibodies
  IgG (4)                         24.16 [+ or -] 14.64
  IgA (5)                         53.55 [+ or -] 35.74
  IgM (6)                          0.85 [+ or -] 0.17
LPS specific antibodies (7)
  IgG                             0.326 [+ or -] 0.093
  IgA                             0.178 [+ or -] 0.222
  IgM                             0.697 [+ or -] 0.481

                                          D19

Hematological change
  NE (2) (%)                      41.52 [+ or -] 10.42
  LY (3) (%)                      53.46 [+ or -] 10.43
  NE:LY                            0.81 [+ or -] 0.35
  Leukocytes ([10.sup.9]/L)        8.99 [+ or -] 0.44
  Platelet ([10.sup.9]/L)        616.00 [+ or -] 271.5 (a)
Total serum antibodies
  IgG (4)                         24.89 [+ or -] 12.66
  IgA (5)                         80.29 [+ or -] 5.15
  IgM (6)                          0.86 [+ or -] 0.04
LPS specific antibodies (7)
  IgG                             0.338 [+ or -] 0.075
  IgA                             0.165 [+ or -] 0.158
  IgM                             0.870 [+ or -] 0.412

(1) D = Days-post weaning (the day of LPS challenge: D7).

(2) Neutrophil. (3) Lymphocyte. (4) Total serum IgG concentration
(mean [+ or /] SD, mg/ml).

(5) Total serum IgA concentration (mean [+ or -] SD, [micro]g/ml).

(6) Total serum IgM concentration (mean [+ or -] SD, mg/ml).

(7) Relative concentrations of antigen specific antibody
(mean [+ or -] SD, absorbance at 450 nm).

(ab) Means with different letters in the same row differ
significantly at p<0.05.

Table 4. Hematological changes in weaned calves at pre-and post-LPS
challenge (mean [+ or -] SD)

                                      D5 (1)

SBM         NE (2) (%)         38.90 [+ or -] 10.44
  group     LY (3) (%)         50.33 [+ or -] 9.58
            NE:LY               0.82 [+ or -] 0.36
            WBC (4)             8.50 [+ or -] 2.14
            PLT (5)           275.00 [+ or -] 212.62 (b)

FSBM        NE (%)             42.10 [+ or -] 13.53
  group     LY (%)             48.51 [+ or -] 10.68
            NE:LY               0.96 [+ or -] 0.48
            WBC                 6.52 [+ or -] 0.95
            PLT               419.83 [+ or -] 93.21

                                       D12

SBM         NE (2) (%)         46.01 [+ or -] 13.39
  group     LY (3) (%)         46.03 [+ or -] 13.66
            NE:LY               1.18 [+ or -] 0.79
            WBC (4)             7.82 [+ or -] 2.02
            PLT (5)           561.50 [+ or -] 189.04 (a)

FSBM        NE (%)             46.49 [+ or -] 13.74
  group     LY (%)             44.54 [+ or -] 11.13
            NE:LY               1.17 [+ or -] 0.65
            WBC                 7.38 [+ or -] 1.81
            PLT               520.83 [+ or -] 97.08

                                       D19

SBM         NE (2) (%)         41.70 [+ or -] 9.41
  group     LY (3) (%)         49.54 [+ or -] 7.04
            NE:LY               0.87 [+ or -] 0.27
            WBC (4)             7.35 [+ or -] 1.72
            PLT (5)           598.83 [+ or -] 173.19 (a)

FSBM        NE (%)             42.87 [+ or -] 10.85
  group     LY (%)             49.13 [+ or -] 11.04
            NE:LY               0.95 [+ or -] 0.41
            WBC                 7.25 [+ or -] 2.24
            PLT               523.14 [+ or -] 125.67

(1) D = Days-post weaning (the day of LPS challenge: D7). (2)
Neutrophil. (3) Lymphocyte. (4) White blood cells. (5) Platelet.

(ab) Means with different letter in the same row differ
significantly (p<0.05).

Table 5. Change of total serum immunoglobulins in weaned
calves fed with SBM or FSBM calf starter at pre- and post-LPS
challenge (mean [+ or -] SD)

                            SBM                         FSBM
IgG (mg/ml)
  D5 (1)          19.24 [+ or -] 11.62        12.50 [+ or -] 2.75
  D12             24.92 [+ or -] 18.78        15.25 [+ or -] 3.51
  D19             21.37 [+ or -] 7.74         15.38 [+ or -] 3.83

IgA ([micro]g/
    ml)
  D5              78.96 [+ or -] 22.43 (b)   131.73 [+ or -] 47.47 (b)
  D12            120.19 [+ or -] 40.91 (ab)  153.42 [+ or -] 59.47 (ab)
  D19            143.02 [+ or -] 34.33 (a)   204.28 [+ or -] 65.39 (a)

IgM (mg/ml)
  D5               1.01 [+ or -] 0.18 (a)      1.27 [+ or -] 0.33 (a)
  D12              1.30 [+ or -] 0.32 (ab)     1.36 [+ or -] 0.28 (a)
  D19              1.59 [+ or -] 0.51 (b)      2.34 [+ or -] 1.21 (b)

(1) D = Days-post weaning (the day of LPS challenge: D7).

(ab) Means with different letters in the same column differ
significantly (p<0.05).
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Author:Kwon, In Hyuk; Kim, Myung Hoo; Yun, Cheol-Heui; Go, Jong Yeol; Lee, Chan Ho; Lee, Hyun June; Phipek,
Publication:Asian - Australasian Journal of Animal Sciences
Article Type:Report
Geographic Code:1USA
Date:Jul 1, 2011
Words:4644
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