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1 Livestock Science 121 (2009) Contents lists ville t ScienceDirect Livestock Science journl homepge: Protein digestiility of porcine colostrum y neontl pigs,, Crol Lin, D.C. Mhn, Guoyo Wu,c, Sung Woo Kim c,d, Deprtment of Animl nd Food Sciences, Texs Tech University, Luock, TX 79409, United Sttes Deprtment of Animl Science, The Ohio Stte University, Columus, OH 43210, United Sttes c Deprtment of Animl Science, Texs A&M University, College Sttion, TX 77843, United Sttes d Deprtment of Animl Science, North Crolin Stte University, Rleigh, NC 27695, United Sttes rticle info strct Article history: Received 10 Decemer 2007 Received in revised form 20 My 2008 Accepted 13 June 2008 Keywords: Amino cid Colostrum Digestiility Pigs Protein Colostrum plys n importnt role in neontl growth nd development. However, little is known out the digestion of mcronutrients in colostrum of ny species. This study ws conducted with the neontl piglet model to determine the digestiility of proteins in porcine colostrum. Twelve, 1-d-old, mle piglets were selected from 3 litters (4 pigs/litter) nd housed individully in metolism crtes with heting lmps to mintin temperture of 35 C. Colostrum (13 L) ws collected from 400 sows (30 to 40 ml/sow) within 12 h postprtum fter injection of oxytocin. All piglets were fed colostrum contining 0.25% (DM sis) chromium oxide s n externl mrker sed on the following feeding progrm: 6 mels/d for n entire 3-d period; with 40 ml/mel for d 1 (240 ml/d), 55 ml/mel for d 2 (330 ml/d), nd 70 ml/mel for d 3 (420 ml/d). Colostrum ws hnd-fed using y milk ottles. Entire fecl smples with the chromium green color were collected ech dy fter colostrum feeding. Fecl collection ws terminted efore the fding of the green color. Fecl smples were weighed (10.3±1.0 g/pig), stored in 20 C, freeze-dried, nd thoroughly ground for chemicl nlysis. Blood smples were collected t 0900 h of d 3 to otin plsm smples for mino cid nd immunogloulin (Ig) G nlysis. Digestiilities of crude protein nd DM in colostrum, defined s the percentge of ingested colostrl crude proteins nd DM tht disppered in the gut, verged 96.9±0.4% nd 98.3±0.2%, respectively. Digestiility of totl mino cids (protein-ound plus free mino cids) in the colostrum ws 98.3±0.1%, with the vlues eing 98.5±0.3, 98.2±0.4, nd 98.3±0.3%, respectively, for Lys, Thr, nd Arg. Plsm nd colostrl IgG content were 3.4±0.3 nd 3.8±0.7 g/l, respectively. In conclusion, protein-ound nd free mino cids in porcine colostrum were highly digestile nd ville to neontl pigs Elsevier B.V. All rights reserved. 1. Introduction The colostrum of mmmls plys crucil nutritionl role for neontl growth nd development of ody tissues, while providing immunogenic protection nd secretive growth Supported y funds from Texs Agriculturl Experiment Sttion (H-8200); the Ohio Agric. Res. nd Dev. Center, Wooster; The Ohio Stte University, Columus; nd Ntionl Reserch Inititive Competitive Grnt ( ) from the USDA Coopertive Stte Reserch, Eduction, nd Extension Service. Apprecition is expressed to K. Mys for colostrum collection. Author disclosures: C. Lin, D. C. Mhn, G. Wu, nd S. W. Kim, no conflicts of interest. Corresponding uthor. Deprtment of Animl Science, North Crolin Stte University, Rleigh, NC 27695, United Sttes. E-mil ddress: sungwoo_kim@ncsu.edu (S.W. Kim). fctors for digestive development nd metolic requirements (Hrtmnn et l., 1989). However, little is known out the digestion of nutrients from the colostrum of ny species. Colostrum consumption hs een estimted to pproximtely 5 to 7% of the piglet's BW during the first h of nursing (Frser nd Rushen, 1992) nd its nursing frequency progressively increses during the initil 24 h postntlly (Vrley et l., 1987). After the neworn piglet egins to nurse, the gstrointestinl trct immeditely exhiits profound physiologicl chnges, including rpid growth nd differentition (Smith nd Jrvis, 1978). Colostrum ingestion further enhnces protein synthesis in the skeleton, crdic muscle, rin, nd the jejunum of piglets (Friorotto et l., 2000). Regulrity of nursing nd sustntil glucogenic ctivity y consuming colostrum is necessry for the neworn piglets to mintin these functions (Lepine et l., 1991) /$ see front mtter 2008 Elsevier B.V. All rights reserved. doi: /j.livsci

2 C. Lin et l. / Livestock Science 121 (2009) Although the functions of colostrum hve een extensively studied (Simmen et l., 1990; Burrin et l., 1994; Dunshe nd vn Brneveld, 2003) nd reviewed(hmosh, 1998; Plyford et l., 2000; Sngild, 2003), the iovilility nd digestiility of nutrients in this specil food hs not een studied in neontes. Determintion of the digestiility of mino cids in colostrum will provide informtion out the mount of ech mino cid ville from colostrum to the neonte. Requirement of individul mino cids cn e ccurtely estimted considering digestile mino cid contents rther thn totl mino cid contents. Therefore, the ojective of this study ws to determine the digestiility of proteins in porcine colostrum when fed to neontl pigs. Considering limited fermenttion in neontl hind gut (Swords et l., 1993) nd infesiility of ilel cnnultion of neontl pigs within short recovery period, totl trck digestiility ws mesured to provide meningful vlues. 2. Mterils nd methods 2.1. Chemicls HPLC-grde solvents were procured from Fisher Scientific (Fir Lwn, NJ). Unless indicted, ll other chemicls were purchsed from Sigm Chemicl (St. Louis, MO) Colostrum A quntity of colostrum (30 to 40 ml/sow) ws mnully milked from pproximtely 400 sows (Yorkshire Lndrce, Duroc, nd Yorkshire) within 12 h postprtum fter n i.m. injection of oxytocin (20 IU) t the Swine Reserch Frm of The Ohio Stte University. Sows hd een fed corn soyen mel diets tht met or exceeded NRC nutrient requirements (NRC, 1998). Colostrum ws frozen upon collection t 20 C until the entire tch ws collected (13 L) nd then it ws shipped to Texs Tech University. Freezing colostrum ws previously shown to e one of the preferred methods to preserve its nturl stte (Mvromichlis et l., 2001). Prior to feeding the neworn piglet, colostrum ws thwed in wrm wter th t 37 C, pooled, nd thoroughly mixed in lrge plstic continer with chromium oxide (0.25% DM) dded s n indigestile externl indictor Animls nd smple collection All experimentl procedures using nimls were pproved y the College Animl Cre committee t The Ohio Stte University nd the Texs Tech University Institutionl Animl Use nd Cre Committee. Twelve, 1-d-old mle neworn piglets (C-22 PIC Bor) with n verge initil BW of 1.57±0.07 kg were selected from 3 litters (4 pigs/litter), kept in n environmentlly controlled uilding nd individully housed in metolism crtes ( m) exceeding recommended spce llownce for nursing pigs (FASS, 1999). Het lmps were provided to mintin pen temperture t 35 C. Piglets were fed 6 mels/ d (0730, 1030, 1330, 1630, 1930, nd 2230) during the 3-d experimentl period y providing 40 ml/mel for d 1 (240 ml/d, 150 ml/kg BW), 55 ml/mel for d 2 (330 ml/d, 210 ml/kg BW), nd 70 ml/mel for d 3 (420 ml/d, 270 ml/kg BW). Dily colostrum llownce ws greter thn Frser nd Rushen (1992) nd less thn relistic recommendtion (280 ml/kg BW) y Le Dividich et l. (1994). The ctul colostrum intke ws recorded dily considering the mount wsted. Colostrum ws hnd-fed using y milk ottles (Cler View, Nurser 5 oz, Gerer, Prsippny, NJ), llowing ech pig to consume the llotted mount. Totl fecl collections contining the chromium green color were collected ech dy. Fecl collection ws terminted efore the fding of the green color. Fresh fecl smples were weighed, stored t 20 C, freeze-dried (Dur-Top Bulk Try Dryer, FTS System, Inc., Stone Ridge, NY), re-weighed, nd ground for further chemicl nlysis. Fecl smples from the 3-d collection period were pooled for ech pig. Blood smples were collected (5 ml) vi jugulr venipuncture 2 h fter feeding (0900 h) on d 3 with plsm seprted from whole lood for further chemicl nlysis. Blood smples were centrifuged t 1500 g for 15 min nd plsm ws otined. Pigs were fed milk replcer (Liqui-Wen, Milk Specilties, Dundee, IL) fter finishing the 3-d experimentl period Chemicl nlyses Fecl smples were freeze-dried nd dry mtter determined. Freeze-dried fecl smples were finely ground using commercil lender (Sunem Products Inc., Boc Rton, FL) with the smple stored t 4 C. The DM nd crude protein contents in colostrum nd fecl smples were determined y the desicction t 105 C for 4 h in drying oven nd y the comustion method using LECO (AOAC, 1995), respectively. Crude ft nd crude sh contents in colostrum were determined y Soxhlet extrction (AOAC, 1995) nd y comusting the smples in muffle furnce t 500 C for 8 h(aoac, 1995), respectively. The mino cid content of the colostrum, fecl smples, nd plsm ws nlyzed y HPLC involving pre-column derivtiztion with o-phthldildehyde s descried y Wu (1993) nd Wu et l. (1997) Immunogloulin G Totl concentrtion of the immunogloulin (Ig) G in colostrum nd plsm ws mesured y n indirect enzymelinked immunosorent ssy (ELISA) commercil kit specific for swine IgG (Bethyl Lortories Inc., Montgomery, TX). Plsm nd colostrum smples were diluted t 1:10,000 for the nlysis Clcultion nd sttisticl nlysis Digestiility of nutrients ws clculted y Eq. (1), DIG ðkþ ¼ ½ðNI NFÞ=NIŠ100 ð1þ where, DIG (%) is the pprent totl trct digestiility of nutrients, NI is the mount of nutrient ingested, nd NF is the mount of nutrient excreted in the feces. Becuse immunogloulins in colostrum re sored directly into enterocytes without digestion, term digestiility my not correctly represent the mount of dietry colostrl nutrients tht disppered from the

3 184 C. Lin et l. / Livestock Science 121 (2009) gut. Therefore, in this study, digestiility ws defined s the percentge of ingested colostrl nutrients tht were not recovered from the feces. Dt re expressed s mens±se. Ech piglet ws considered s experimentl unit in sttisticl nlysis, using Proc Mens of SASsoftwre(SASInst.,Inc.,Cry,NC).Proilityvlues0.05 were tken to indicte sttisticl significnce. 3. Results 3.1. The composition of nutrients nd IgG in colostrum The nutrient compositions of sow's colostrum re presented in Tle 1. It contined 21.9% DM, nd on DM sis, 21.9% crude ft, 68% CP, nd 0.91% crude sh. The most undnt mino cids were, in % of DM, Glu+Gln (7.8%), followed y Lys (6.6%) nd Pro (5.6%) (Tle 1). Arginine (2.1%) ws one of the lest undnt mino cids in porcine colostrum. Colostrl concentrtion of IgG ws 3.8 g/l (Tle 1) Animl growth performnce nd IgG levels in plsm Colostrum intke verged 330 ml/d etween d 1 nd 3 of ge (Tle 2). Piglets gined weight normlly during the 3-d feeding period, verging 140 g/d. The concentrtion of IgG in piglet plsm t 3 d of ge ws 3.4±0.3 g/l Concentrtions of mino cids in plsm At d 3, Gly (738.5 μmol/l) ws the most undnt mino cid in neworn pigs' plsm, followed y Vl (681.6 μmol/l), Pro (607.5 μmol/l), nd Gln (587.8 μmol/l). Concentrtion of Arg in plsm ws reltively low compred with Pro nd Gly. The metolites involved in the ure cycle, nmely citrulline, nd Orn, were lso reltively low (Tle 3) Concentrtions of mino cids in feces Fecl concentrtions of mino cids in neontl pigs re presented in Tle 4. The most undnt mino cid ws Lys (5.78% DM sis), followed y Glu + Gln (5.47% DM sis) nd Pro (4.07% DM sis). Concentrtions of CP nd totl Tle 2 Growth performnce of neontl pigs from d 1 to 3 of ge Age of piglets Body weight, g d ±67.7 d ±65.9 d ±64.8 Age of piglets Averge dily gin, g/d d 1 to ± 10.6 d 2 to ± 8.1 d 1 to ± 7.6 Dt re mens ±SE, n=12. mino cids were 52.3% nd 47.4% in fecl smples, respectively Digestiilities of protein nd DM in colostrum Apprent digestiilities of crude protein nd DM in colostrum were 96.9% nd 98.3%, respectively (Tle 5). Digestiilities of totl mino cids were 98.3%. Digestiilities of Glu plus Gln nd Gly were the highest (98.8%) nd lowest (97.9%), respectively, mong ll mino cids. 4. Discussion The present study demonstrtes tht there ws little recovery ( %) of dietry proteins nd mino cids in the feces of neontl pigs tht were fed porcine colostrum, suggesting tht nerly ll of these dietry components were sored into the smll intestine. Intct immunogloulins in colostrum re not ll hydrolyzed y the digestive proteses ut cn e sored directly into the enterocytes of neontl pigs in the first few dys of life efore gut closure (Lskowski et l., 1957; Smith, 1988). Therefore, these immunogloulin proteins in colostrum nd perhps totl proteins would hve greter digestiility vlues thn those in mture milk. The true digestiility vlues for Lys, Thr, nd Arg in mture milk for 17-d-old pigs were found to e 92.1, 84.3, Tle 1 Composition of porcine colostrum Item Men±SE Item Men±SE DM, % 21.9±0.1 Crude sh, % 0.91±0.05 Crude ft, % 21.92±1.83 CP, % 68.04±0.05 Immunogloulin G c, g/l 3.8±0.7 Amino cid,% Al 2.03 ±0.09 Lys 6.59±0.26 Arg 2.12±0.09 Met 1.05±0.06 Asp +Asn 3.81 ±0.31 Phe 2.03±0.15 Cys 0.73±0.01 Pro 5.63±0.09 Gly 1.96±0.09 Ser 2.74±0.12 Glu + Gln 7.80±0.50 Thr 2.67± 0.16 His 1.17±0.06 Trp 0.66 ± 0.01 Ile 1.86±0.13 Tyr 1.85±0.10 Leu 4.46 ±0.24 Vl 3.25±0.20 c Dt re mens±se, n=12. Colostrum ws collected within 12 h postprtum. DM sis. As-fed sis. Tle 3 Concentrtions of immunogloulin G nd mino cids in plsm of neontl pigs t d 3 of ge Item Men±SE Item Men±SE Immunogloulin G, g/l 3.4±0.3 Amino cid, µmol/l Al 464.2±39.7 Leu 331.2±24.2 Arg 231.8±24.0 Lys 246.1±24.5 Asn ± 13.4 Met 73.8 ±5.8 Asp 18.6±6.1 Orn 164.5±11.3 β-al 10.4±0.8 Phe ±9.5 Citrulline ± 9.2 Pro 607.5±27.6 Cys 261.3±19.0 Ser 243.1±28.1 Glu 84.7 ± 25.4 Turine 78.7 ±8.2 Gln 587.8±34.4 Thr 481.1±33.6 Gly ± 59.9 Trp 43.4 ±5.3 His 117.7±9.8 Tyr ±19.6 Ile 149.1±11.1 Vl 681.6±29.6 Dt re mens ±SE, n=12.

4 C. Lin et l. / Livestock Science 121 (2009) nd 90.4%, respectively (Mvromichlis et l., 2001), which were lower thn digestiility of mino cids in colostrum otined in this study. Considering tht the digestiility otined in this study ws n pprent vlue, the true digestiility of proteins nd DM in porcine colostrum would e essentilly 100%. Nutrient composition of sow's colostrum cn e influenced y severl fctors, including vrition mong sows, vrying disese sttus, genetic difference, dietry regimen, nd sow's ody ft content (Perrin, 1955; Goonertne et l., 1982; Zou et l., 1992; King et l., 1993; Jckson et l., 1995; Klver et l., 1981). In ddition, the techniques for collecting the colostrum from the vrious mmmry glnds could ffect the composition of colostrum or sow milks. Atwood nd Hrtmnn (1992) indicted n increse in the concentrtion of ft nd totl solids when the milk ws collected from glnds towrd the rer of the sow. These uthors collected milk smples immeditely fter the completion of suckling rther thn t the eginning of the next nturl let-down. Concentrtions of nutrients in colostrum collected from 400 sows in the present study were generlly similr to those of others (Cspó et l., 1996; Klos et l., 1987; Dvis et l., 1994; Wu et l., 1994; Kim nd Wu, 2004). Notly, the concentrtion of totl mino cids (peptide-ound nd free) in colostrum ws 52.4% of DM (Tle 1), tht ws similr to the vlue (51%) previously reported for colostrum otined t d 1 of lcttion (Wu et l., 1994) ut ws 94% greter thn tht for porcine mture milk (Kim nd Wu, 2004). In this, study, the difference etween CP nd true protein contents (68.0 nd 52.4%, respectively) my e prtly contriuted from the presence of high concentrtions of oth ure (6 to 8 mmol/l) nd mmoni (1.6 to 2.0 mmol/l) in sow's colostrum (Wu et l., 1994). Content of rginine in colostrum ws 2.1% which is 32% of lysine content nd this is similr to Mteo et l. (2008) nd Wu et l. (2004). Arginine from colostrum nd milk of sows is not sufficient to meet the requirement of rginine for neontl nd nursing piglets (Dvis et l., 1997; Wu, 1998). Dietry supplementtion of 0.4% L-rginine to sl milk formul contining 0.67% rginine (totl of 1.07% rginine with supplementtion) improved the growth nd generl helth of those young piglets compred to pigs fed sl milk formul without L- rginine supplementtion (Kim nd Wu, 2004). Requirement of individul mino cids cn e ccurtely estimted Tle 4 Fecl composition of dry mtter nd mino cids in neontl pigs from d 1 to 3 of ge Item Men±SE Item Men±SE Amount excreted, g s-is 10.3±1.0 DM, % 75.1±6.4 CP2, % 52.3±3.7 Amino cid,% Al 2.29±0.13 Lys 5.78±0.33 Arg 2.28±0.14 Met 0.95±0.05 Asp +Asn 3.71±0.19 Phe 2.17±0.11 Cys 0.67± 0.03 Pro 4.07± 0.16 Glu + Gln 5.47±0.28 Ser 2.76±0.23 Gly 2.40±0.15 Thr 2.74±0.21 His 0.93±0.05 Trp 0.58±0.04 Ile 1.85±0.07 Tyr 2.06±0.14 Leu 3.77± 0.20 Vl 2.88±0.36 Dt re mens ±SE, n=12. DM sis. Tle 5 Apprent digestiility (%) of dry mtter nd mino cids in porcine colostrum y neontl pigs Item Men±SE Items Men±SE DM 98.3±0.2 CP 96.9 ±0.4 Amino cid Al 98.1±0.4 Lys 98.5 ±0.3 Arg 98.3±0.3 Met 98.5 ±0.2 Asp +Asn 98.1±0.3 Phe 98.1±0.3 Cys 98.4±0.3 Pro 98.7 ±0.2 Glu + Glu 98.8±0.2 Ser 98.2 ±0.6 Gly 97.9±0.4 Thr 98.2 ±0.4 His 98.6±0.2 Trp 98.3 ±0.2 Ile 98.3±0.3 Vl 98.5 ±0.4 Leu 98.5±0.3 Dt re mens ±SE, n=12. DM sis. considering digestile mino cid contents rther thn totl mino cid contents. Totl trct digest ws used to determine the nutrient digestiility in the present study ecuse we desired to conduct the study with neontl pigs. Ilel digest otined from surgiclly fitted T-cnnul t the terminl ileum cn e used to determine the ccurte nutrient digestiility y excluding potentil effects of cecl nd colonl fermenttion. However, surgicl cnnultion of neontl pigs would not e suitle for the ojective of the present study ecuse of the prolonged durtion period for the recovery nd incresed ge upon recovery. The colon in neworn pig is considered sterile t irth, ut gut microorgnisms cn egin coloniztion in the lrge intestine within 12 h of irth (Swords et l., 1993). Wlker et l. (1989) demonstrted tht crohydrte fermenttion occurs in the gut of preterm humn infnts. Edwrd et l. (2002) reported tht short-chin ftty cid concentrtion produced in meconium y rest-fed humn infnt ws very low t out 10% of dult level, indicting limited hind gut fermenttion y infnts. Using 1- to 3-d-old neontl pigs, the digestiility vlues otined in the present study could e ffected y colonl fermenttion, ut this is likely miniml due to the limited fermenttion in the hind gut of neontl pigs t 1- to 3 d of ge (Swords et l., 1993). In our study, verge colostrl IgG intke until 10 h of d 3 ws 2.43 g considering 0.64 L of colostrum intke nd 3.8 g/l IgG concentrtion in colostrum, wheres systemic IgG content ws 0.61 g sed on n ssumption tht the volume of lood in pig ody is 0.18 L (10% of 1.84 kg BW on d 3, Linderkmp et l., 1980) nd plsm IgG concentrtion is 3.4 g/l. Therefore, in this study, the percentge of sored porcine IgG ws 25.2%. Considering possiility of IgG turnover or ctolism, it cn e speculted tht t lest 25% of colostrl IgG ws successfully sored s n intct form during the first 3 d of life. Jensen et l. (2001) demonstrted tht the percentge of sored porcine IgG ws 22.6%. In conclusion, nerly ll of the proteins nd mino cids in porcine colostrum were sored y the smll intestine of neontl pigs. The high digestiility of non-immunogloulin proteins from colostrum is consistent with its enormous nutritionl importnce for the survivl, growth nd development of the gut, s well s whole ody growth nd development. Findings from this study with piglets provided new

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