Effects of dietary deoxynivalenol and zearalenone on apparent ileal digestibility of amino acids in growing pigs

Accepted Manuscript Title: Effects of dietary deoxynivalenol and zearalenone on apparent ileal digestibility of amino acids in growing pigs Author: H. Jo C. Kong M. Song B.G. Kim PII: DOI: Reference:

S0377-8401(16)30212-7 http://dx.doi.org/doi:10.1016/j.anifeedsci.2016.06.006 ANIFEE 13559

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Please cite this article as: Jo, H., Kong, C., Song, M., Kim, B.G., Effects of dietary deoxynivalenol and zearalenone on apparent ileal digestibility of amino acids in growing pigs.Animal Feed Science and Technology http://dx.doi.org/10.1016/j.anifeedsci.2016.06.006 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Effects of dietary deoxynivalenol and zearalenone on apparent ileal digestibility of amino acids in growing pigs

H. Jo,a,† C. Kong,a,† M. Song,b and B. G. Kima,*

a

Department of Animal Science and Technology, Konkuk University, Seoul 05029,

Republic of Korea b

Department of Animal Science and Biotechnology, Chungnam National University,

Daejeon 34134, Republic of Korea

Abbreviations: AA, amino acids; AID, apparent ileal digestibility; ATTD, apparent total tract digestibility; BW, body weight; CP, crude protein; DM, dry matter ; DON, deoxynivalenol ; ZON, zearalenone * Corresponding author: Tel.: +82 2 2049 6255. E-mail address: [email protected] (B.G. Kim).

1

†

These authors contributed equally to this work.

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Highlights ○ Protein digestibility was not affected by the dietry mycotoxins. ○ Digestibility of some indispensable amino acid was reduced by deoxynivalenol. ○ The dietary zearalenone did not affect digestibility of amino acids except Trp.

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ABSTRACT This experiment was conducted to investigate the effects of deoxynivalenol (DON) and zearalenone (ZON) on the apparent ileal digestibility (AID) of AA in growing pigs. Twelve pigs (initial mean body weight = 20.6 ± 2.1 kg) cannulated at the distal ileum were assigned to 3 dietary treatments in a quadruplicated 3 × 2 incomplete Latin square design with 3 diets and 2 periods. Three experimental diets consisted of a corn-soybean meal-based control diet, a DON-supplemented diet at 10 mg/kg and a ZON-supplemented diet at 10 mg/kg. All diets contained 5 g/kg chromic oxide as an indigestible index. Each experimental period was comprised of a 5-d adaptation period and a 3-d ileal digesta collection period. The concentration of DON or ZON in the mycotoxin-supplemented diet was analyzed to be 11.2 mg/kg or 11.6 mg/kg, respectively. Pigs fed the DONsupplemented diet had less AID of Lys (0.799 vs. 0.839, P= 0.08), Thr (0.695 vs. 0.751, P=0.08), Trp (0.766 vs. 0.840, P=0.02), and Val (0.687 vs. 0.749, P=0.08) than those fed the control diet, but the AID of other AA were not affected by DON supplementation. With the exception of Trp (0.771 vs. 0.840, P=0.04), the supplementation of ZON to the control diet did not affect the AID of AA. In conclusion, dietary DON, but not ZON, may reduce the AID of some indispensable AA.

Key words: Amino acid, Ileal digestibility; Mycotoxin; Swine

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1. Introduction Mycotoxins are secondary metabolites produced by fungi and potentially lower the productivity of pigs (Chaytor et al., 2011a). Both deoxynivalenol (DON) and zearalenone (ZON) are produced by Fusarium fungus and received considerable attention due to the frequency of occurrence and the concentration of mycotoxins relative to their guidance value by toxicity in swine diets (CEC, 2006; Rodrigues and Naehrer, 2012). Pigs are known to be very sensitive to dietary DON (Pestka, 2007) which may cause reduced feed intake, weight loss and immune system disorders (CAST, 2003; Pinton et al., 2008; Chaytor et al., 2011b). The DON has also been reported to damage the intestinal tract by altering barrier function of epithelial cells (Pinton et al., 2010), which may adversely affect the digestion and absorption of nutrients in diets. However, limited data are available on the effect of DON on nutrient utilization of pigs (Dänicke et al., 2004; Kong et al., 2015). Zearalenone and its metabolites affect the reproductive and urinary systems by acting as a mycoestrogen which can bind to estrogen receptors (Takemura et al., 2007; Kanora and Maes, 2009; Jiang et al., 2010; Chaytor et al., 2011a). Due to the estrogenic properties of ZON and its metabolites, most of the published research focused on the reproductive responses (Green et al., 1990; Rainey et al., 1990) and little data from study of the effect of ZON on nutrient utilization is available (Dänicke et al., 2004; Kong et al., 2015). To our knowledge, the influence of DON and ZON on the ileal digestibility of crude protein (CP) and amino acids (AA) for pigs have not been documented. Therefore, the objective of this study was to investigate the effects of DON and ZON on the apparent 5

ileal digestibility (AID) of CP and AA in the diet fed to growing pigs.

2. Materials and methods The experimental protocol was approved by the Institutional Animal Care and Use Committee at Konkuk University. 2.1. Animals, diets, and experimental design Twelve crossbred barrows with an initial mean body weight (BW) of 20.6 ± 2.1 kg were used to determine the AID of CP and AA in diets. Pigs were surgically fitted with a Tcannula at the distal ileum using procedures described by Stein et al. (1998). After the surgery, the pigs were individually housed in pens (2.0 × 2.2 m) that were equipped with a feeder and a nipple drinker. After recovery from the surgery, the pigs were allotted to 3 dietary treatments in a quadruplicated 3 × 2 incomplete Latin square design with 3 diets and 2 periods (Kim and Kim, 2010). The DON and ZON culture materials (Biomin Inc., Seoul, Republic of Korea) were used to achieve target concentrations (10 mg/kg) of each mycotoxin in the experimental diets. The concentrations of DON and ZON in the culture materials were 34800 and 19100 mg/kg, respectively (Table 1). A control diet was formulated mainly based on corn containing 0.30 mg/kg DON and 0.09 mg/kg ZON and soybean meal containing 0.53 mg/kg DON and 0.16 mg/kg ZON, and two additional diets contained 0.29 g/kg DON or 0.53 g/kg ZON culture material at the expense of corn starch in the control diet (Tables 1 and 2). Vitamins and minerals were included in all diets to meet or exceed nutrient requirement estimates of growing pigs (NRC, 2012). All diets contained 5 g/kg chromic oxide as an indigestible index. 6

2.2. Feeding and sample collection The pigs were fed allocated diets at 3 times the daily maintenance requirement for energy (i.e., 0.825 MJ metabolizable energy/kg BW0.60; NRC, 2012). The amount of feed allowance per pig was divided into 2 equal meals and fed to pigs at 0800 and 1700 h. Water was available at all times. For pigs fed the DON-supplemented diet, the amount of feed allowance was re-adjusted after each meal. Twenty minutes after each meal, leftover feed (if any) was removed and weighed. The amount of feed allowance of the next meal was calculated by subtracting a half of the amount of the leftover from the amount of original feed allowance. Each experimental period was comprised of a 5-d adaptation period to the experimental diet and a 3-d ileal digesta collection period. The ileal digesta samples were collected for 9 h between the meals each day during the collection period using a plastic sample bag that was fixed to the T-cannula. Sample bags were changed whenever they were filled with ileal digesta, or at least once every 30 mins. Collected ileal digesta were immediately stored at −20°C to prevent bacterial fermentation of AA in the digesta. 2.3. Chemical analysis The frozen ileal digesta samples were dried in a freeze drier, pooled for each pig, and subsampled. The ileal digesta, ingredients, and diets were finely ground prior to chemical analysis. The experimental diets, ingredients, and ileal digesta samples were analyzed for dry matter (DM, AOAC, 2005; method 930.15), CP (AOAC, 2005; method 990.03), and AA (Table 3; AOAC, 2005; method 982.30). Methionine and cysteine were analyzed as methionine sulfone and cysteic acid after cold performic acid oxidation 7

overnight prior to acid hydrolysis. Tryptophan was analyzed following 4 N NaOH hydrolysis for 22 h at 110℃. Also, all ileal digesta and diet samples were analyzed for chromium (method AOAC, 2005; 990.08). The concentrations of DON and ZON in the ingredient and experimental diet were determined by using enzyme-linked immunosorbent assay kits (AgraQuant, Romer Labs Inc., Singapore, Republic of Singapore). 2.4. Calculations and statistical analysis The AID of CP and AA in the experimental diets were calculated based on CP, AA, and chromium concentration of diets and ileal digesta (Kong and Adeola, 2014). Experimental data were analyzed using the MIXED procedure of SAS (SAS Inst. Inc., Cary, NC, USA). The statistical model included dietary treatment as a fixed variable and animal within replication, period, and replication as a random variable. After AID of CP and AA for each treatment was calculated by the least mean square, pre-planned contrasts were used to compare the pigs fed the DON or ZON-supplemented diet with the pigs fed the control diet. Individual pig was the experimental unit and statistical significance and tendency were accepted at P-value less than 0.05 and 0.10, respectively.

3. Results and discussion One pig fed the ZON-supplemented diet refused to consume the diet during collection period and was excluded from the observations. The level of feed intake for pigs fed the DON-supplemented diet (633 g/d) was lower than those for pigs fed the control diet (1105 g/d) and ZON-supplemented diet (1102 g/d) during the collection period. Albin et al. (2001) reported that the AID of AA for 8

growing pigs was not affected by lowering the feed intake to a half of ad libitum. Therefore, the lower feed intake of pigs fed the DON-supplemented diet in the present study may not have directly affected the AID of AA.

3.1. Effect of deoxynivalenol on apparent ileal digestibility The AID of CP in control diet and DON-supplemented diet fed to pigs were 0.727 and 0.700, respectively, and they were not significantly different each other. There have been contradictory reports on the effect of DON on the CP digestibility. Dänicke et al. (2004) reported that diets containing wheat naturally contaminated with DON did not affect the apparent total tract digestibility (ATTD) of CP in diets fed to growing pigs. On the contrary, other researchers reported a significant DON-related increase in the ATTD of CP in diets naturally contaminated with DON (Goyarts and Dänicke, 2005; Kong et al., 2015). The studies observed DON-related changes of the CP digestibility used diets containing relatively high concentration of DON (≥ 7 mg/kg) whereas Dänicke et al. (2004) which did not observe DON-related improvement used diets with relatively low concentration of DON (≤ 4 mg/kg). Although, the concentration of DON in the diets used in the present study was relatively higher (10 mg/kg) compared with studies found the improvement of the CP digestibility, no difference between the control diet and the diet contaminated with DON. This result may be, at least partially, attributed to the source of DON (purified vs. naturally contaminated) in diets. To the best of the authors’ knowledge, there is no digestibility study conducted with purified DON-supplemented diets fed to pigs. In a broiler study, a high concentration of purified DON (12.21 mg of DON/kg) 9

contaminated diet did not affect apparent total tract retention of CP (Yunus et al., 2012). Moreover, Matthäus et al. (2004) observed that the activities of enzymes such as protease, amylase, and non-starch polysaccharide-degrading enzymes in the wheat inoculated with Fusarium culmorum were increased compared with the control wheat. For the indispensable AA, the DON culture material supplementation to the control diet tended to decrease (P<0.10) the AID of Lys (0.799 vs. 0.839), Thr (0.695 vs. 0.751), and Val (0.687 vs. 0.749) and decreased (P=0.023) the AID of Trp (0.766 vs. 0.840) compared with the control diet. The reason for this result is unclear. But it may be speculated that the impaired intestinal barrier function as a consequence of feeding of DON-supplemented diet to the pigs may adversely affect the digestion and absorption of nutrients in the intestinal tract (Maresca et al., 2002; Kolf-Clauw et al., 2009; Antonissen et al., 2014). It was also reported that DON may decrease the expression of tight junction protein such as claudin-4 (Pinton et al., 2010) as well as cause the inhibition of the regeneration of damaged intestinal epithelial cells (Ueno, 1985; Hussein and Brasel, 2001). 3.2. Effect of zearalenone on apparent ileal digestibility The supplementation of ZON to the control diet did not affect the AID of most AA except for Trp, which was significantly lower (P=0.04) compared with the control diet. The reason for this result is unclear. To our knowledge, there is no study that investigated the effect of ZON on the AID of AA in diets fed to pigs. Moreover, the results of studies that investigated the effect of ZON on ATTD of nutrients for pigs have been inconsistent (Hauschild et al., 2007; Wang et al., 2012). Hauschild et al. (2007) reported that feeding 2 mg ZON/kg to nursery pigs did not affect the ATTD of CP and DM, whereas Wang et al. 10

(2012) reported that the ATTD of CP and DM in ZON-supplemented diet fed to gilts decreased as the dietary ZON concentration increased.

4. Conclusion The present study showed that the supplementation of DON to the corn-soybean meal based control diet may decrease the AID of indispensable AA for growing pigs, whereas dietary ZON did not affect the AID of CP and most of AA except Trp.

Acknowledgements This manuscript is based on research supported by National Institute of Animal Science (Republic of Korea; PJ010932) and the KU Research Professor Program of Konkuk University.

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and deoxynivalenol on growth and immune status of pigs. J. Anim. Sci. 89, 124-135. Dänicke, S., Valenta, H., Klobasa, F., Doll, S., Ganter, M., Flachowsky, G., 2004. Effects of graded levels of Fusarium toxin contaminated wheat in diets for fattening pigs on growth performance, nutrient digestibility, deoxynivalenol balance and clinical serum characteristics. Arch. Anim. Nutr. 58, 1-17. Goyarts, T., Dänicke, S., 2005. Effects of deoxynivalenol (DON) on growth performance, nutrient digestibility and DON metabolism in pigs. Mycotoxin Res. 21, 139-142. Green, M.L.; Diekman, M.A.; Malayer, J.R.; Scheidt, A.B.; Long, G.G., 1990. Effect of prepubertal consumption of zearalenone on puberty and subsequent reproduction of gilts. J. Anim. Sci. 68, 171-178. Hauschild, L., Lovatto, P.A., Lehnen, C.R., Carvalho, A.A., Garciae, G.G., Mallmann, C.A., 2007. Digestibility and metabolism of piglet diets containing zearalenone with addition of organoaluminosilicate. Pesqui. Agropecu. Bras. 42, 219-224. Hussein, H.S., Brasel, J.M., 2001. Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology 167, 101-134. Jiang, S.Z., Yang, Z.B., Yang, W.R., Yao, B.Q., Zhao, H., Liu, F.X., Chen, C.C., Chi, F., 2010. Effects of feeding purified zearalenone contaminated diets with or without clay enterosorbent on growth, nutrient availability, and genital organs in post-weaning female pigs. Asian Australas. J. Anim. Sci. 23, 74-81. Kanora, A., Maes, D., 2009. The role of mycotoxins in pig reproduction: A review. Vet. Med. 54, 565-576. Kim, B.G., Kim, T.M., 2010. A program for making completely balanced Latin square 13

designs employing a systemic method. Rev. Colomb. Cienc. Pecu. 23, 277-282. Kolf-Clauw, M., Castellote, J., Joly, B., Bourges-Abella, N., Raymond-Letron, I., Pinton, P., Oswald, I.P., 2009. Development of a pig jejunal explant culture for studying the gastrointestinal toxicity of the mycotoxin deoxynivalenol: histopathological analysis. Toxicol. In Vitro. 23, 1580-1584. Kong, C., Adeola, O., 2014. Evaluation of amino acid and energy utilization in feedstuff for swine and poultry diets. Asian Australas. J. Anim. Sci. 27, 917-925. Kong, C., Shin, S.Y., Park, C.S., Kim, B.G., 2015. Effect of feeding barley naturally contaminated with fusarium mycotoxins on growth performance, nutrient digestibility, and blood chemistry of gilts and growth recoveries by feeding a noncontaminated diet. Asian Australas. J. Anim. Sci. 28, 662-670. Maresca, M., Mahfoud, R., Garmy, N., Fantini, J., 2002. The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells. J. Nutr. 132, 27232731. Matthäus, K., Dänicke, S., Vahjen, W., Simon, O., Wang, J., Valenta, H., Meyer, K., Strumpf, A., Ziesenib, H., Flachowsky, G., 2004. Progression of mycotoxin and nutrient concentrations in wheat after inoculation with Fusarium culmorum. Arch. Anim. Nutr. 58, 19-35. NRC, 2012. Nutrient Requirements of Swine. 11th ed. National Academy Press, Washington, DC, USA. Pestka, J.J., 2007. Deoxynivalenol: toxicity, mechanisms and health risks. Anim. Feed Sci. Technol. 137, 283-298. 14

Pinton, P., Accensi, F., Beauchamp, E., Cossalter, A., Callu, P., Grosjean, F., Oswald, I. P., 2008. Ingestion of deoxynivalenol (DON) contaminated feed alters the pig vaccinal immune responses. Toxicol. Lett. 177, 215-222. Pinton, P., Braicu, C., Nougayrede, J.P., Laffitte, J., Taranu, I., Oswald, I.P., 2010. Deoxynivalenol impairs porcine intestinal barrier function and decreases the protein expression of claudin-4 through a mitogen-activated protein kinase-dependent mechanism. J. Nutr. 140, 1956-1962. Rainey, M.R., Tubbs, R.C., Bennet, L.W., Cox, N.M., 1990. Prepubertal exposure to dietary zearalenone alters hypothalamo hypophyseal function does not impair postpubertal reproductive functions in gilts. J. Anim. Sci. 68, 2015-2022. Rodrigues, I., Naehrer, K., 2012. A three-year survey on the worldwide occurrence of mycotoxins in feedstuffs and feed. Toxins 4, 663-675. Stein, H.H., Shipley, C.F., Easter, R.A., 1998. Technical note: A technique for inserting a T-cannula into the distal ileum of pregnant sows. J. Anim. Sci. 76, 1433-1436. Takemura, H., Shim, J.Y., Sayama, K., Tsubura, A., Zhu, B.T., Shimoi, K., 2007. Characterization of the estrogenic activities of zearalenone and zeranol in vivo and in vitro. J. Steroid Biochem. Mol. Biol. 103, 170-177. Ueno, Y., 1985. The toxicology of mycotoxins. Crit. Rev. Toxicol. 14, 99-132. Wang, J.P., Chi, F., Kim, I.H., 2012. Effects of montmorillonite clay on growth performance, nutrient digestibility, vulva size, faecal microflora, and oxidative stress in weaning gilts challenged with zearalenone. Anim. Feed Sci. Technol. 178, 158166. 15

Yunus, A.W., Blajet-Kosicka, A., Kosicki, R., Khan, M.Z., Rehman, H., Böhm, J., 2012. Deoxynivalenol as a contaminant of broiler feed: Intestinal development, absorptive functionality, and metabolism of the mycotoxin. Poult. Sci. 91, 852-861.

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Table 1 Analyzed mycotoxin concentration of ingredients (mg/kg, as-fed basis). Mycotoxin Ingredients1

DON

ZON

DON culture material

34800

ND2

ZON culture material

ND

19100

Corn

0.30

0.09

Soybean meal

0.53

0.16

Whey powder 1 2

ND

DON = deoxynivalenol; ZON = zearalenone. ND = Not detected.

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ND

Table 2 Ingredient composition and analyzed mycotoxin concentration of experimental diets (asfed basis). Diet1 Mycotoxin supplementation

Item

Control

DON (10 mg/kg)

ZON (10 mg/kg)

Ingredient (g/kg) Ground corn, yellow dent 630.0 630.0 630.0 Soybean meal, 48% crude protein 260.0 260.0 260.0 Whey power 50.0 50.0 50.0 Soybean oil 20.0 20.0 20.0 Cornstarch 1.0 0.71 0.47 2 DON culture material 0.29 2 ZON culture material 0.53 5.0 5.0 5.0 L-Lys·HCl, 78.8% 1.2 1.2 1.2 DL-Met, 99% 1.6 1.6 1.6 L-Thr, 99% 0.7 0.7 0.7 L-Val, 99% Dicalcium phosphate 12.0 12.0 12.0 Ground limestone 9.5 9.5 9.5 3 Vitamin-mineral premix 5.0 5.0 5.0 Salt 4.0 4.0 4.0 Calculated nutrient and energy Crude protein (g/kg) 188.9 188.9 188.9 Metabolizable energy (MJ/kg) 14.15 14.14 14.14 Analyzed mycotoxin (mg/kg) DON 0.40 11.2 0.93 ZON 11.6 1 DON = deoxynivalenol; ZON = zearalenone. 2 DON culture material contains the DON 34.8 mg/g; ZON culture material contains the ZON 19.1 mg/g. 3 Provided the following quantities per kg of complete diet: vitamin A, 25000 IU; vitamin D3, 4000 IU; vitamin E, 50 IU; vitamin K, 5.0 mg; thiamin, 4.9 mg; riboflavin, 10.0 mg; pyridoxine, 4.9 mg; vitamin B12, 0.06 mg; pantothenic acid, 37.5 mg; folic acid, 1.10 mg; niacin, 62 mg; biotin, 0.06 mg; Cu, 25 mg as copper sulfate; Fe, 268 mg as iron sulfate; I, 5.0 mg as potassium iodate; Mn, 125 mg as manganese sulfate; Se, 0.38 mg as sodium selenite; Zn, 313 mg as zinc oxide; and butylated hydroxytoluene, 50 mg. 18

Table 3 Analyzed concentration of nutrients in the experimental diets (g/kg, dry matter basis). Diet1 Control Item Dry matter 911.8 Crude protein 216.8 Indispensable amino acids Arg 12.8 His 5.6 Ile 8.9 Leu 19.1 Lys 16.5 Met 3.8 Phe 11.8 Thr 10.5 Trp 1.8 Val 10.7 Dispensable amino acids Ala 10.9 Asp 21.1 Cys 3.8 Glu 39.8 Gly 8.7 Pro 11.6 Ser 10.6 Tyr 5.4 1 DON = deoxynivalenol; ZON = zearalenone.

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Mycotoxin supplementation DON (10 mg/kg) ZON (10 mg/kg)

911.0 226.3

911.2 214.0

13.0 5.4 8.6 18.6 16.1 3.8 11.3 10.4 1.6 10.6

12.3 5.3 8.3 18.4 15.7 4.0 11.2 10.0 1.4 10.2

10.8 20.7 3.6 39.2 8.6 11.5 10.5 5.6

10.6 20.2 3.7 38.2 8.2 11.3 10.3 5.2

Table 4 Effects of dietary mycotoxins on apparent ileal digestibility of dry matter, crude protein and amino acids in experimental diets. 1,2 Coefficient of apparent ileal digestibility

P-value

Mycotoxin supplementation

Control vs.

Control

DON (10 mg/kg)

ZON (10 mg/kg)

SEM3

DON

ZON

Dry matter

0.662

0.617

0.634

0.036

0.277

0.518

Crude protein

0.727

0.700

0.711

0.029

0.425

0.648

Arg

0.850

0.835

0.846

0.024

0.538

0.868

His

0.780

0.745

0.768

0.030

0.257

0.716

Ile

0.787

0.741

0.759

0.025

0.169

0.414

Leu

0.792

0.763

0.771

0.025

0.369

0.531

Lys

0.839

0.799

0.826

0.020

0.075

0.546

Met

0.834

0.830

0.828

0.023

0.890

0.834

Phe

0.833

0.797

0.809

0.060

0.181

0.394

Thr

0.751

0.695

0.734

0.026

0.082

0.586

Trp

0.840

0.766

0.771

0.030

0.023

0.040

Val

0.749

0.687

0.727

0.025

0.084

0.544

Ala

0.732

0.687

0.705

0.030

0.264

0.520

Asp

0.742

0.712

0.734

0.030

0.347

0.805

Cys

0.613

0.586

0.620

0.048

0.620

0.912

Glu

0.787

0.803

0.776

0.030

0.615

0.759

Gly

0.603

0.543

0.571

0.041

0.243

0.551

Pro

0.680

0.706

0.655

0.046

0.684

0.713

Ser

0.751

0.710

0.738

0.026

0.208

0.700

Tyr

0.659

0.631

0.633

0.092

0.613

0.651

Item

Indispensable amino acids

Dispensable amino acids

1

DON = deoxynivalenol; ZON = zearalenone. Each least squares mean represents 8 observations except ZON-supplemented diet (n = 7). 3 SEM = standard error of the mean. 2