Different Dietary Protein and PUFA Interventions Alter the Fatty Acid Concentrations, but Not the Meat Quality, of Porcine Muscle

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1 Nutrients 2012, 4, ; doi: /nu Article OPEN ACCESS nutrients ISSN Different Dietry Protein nd PUFA Interventions Alter the Ftty Acid Concentrtions, ut Not the Met Qulity, of Porcine Muscle Dirk Dnnenerger 1, *, Krin Nuernerg 1, Gerd Nuernerg 1 nd Antje Priepke Reserch Unit of Muscle Biology nd Growth nd Genetics nd Biometry, Leiniz Institute for Frm Animl Biology, Wilhelm-Sthl-Allee 2, Dummerstorf, Germny; E-Mils: knuerng@fn-dummerstorf.de (K.N.); gnuerng@fn-dummerstorf.de (G.N.) Institute of Animl Production, Stte Institute for Agriculture nd Fishing Reserch, Wilhelm-Sthl-Allee 2, Dummerstorf, Germny; E-Mil:.priepke@lf.mvnet.de * Author to whom correspondence should e ddressed; E-Mil: dnnenerger@fn-dummerstorf.de; Tel.: ; Fx: Received: 6 July 2012; in revised form: 8 August 2012 / Accepted: 28 August 2012 / Pulished: 5 Septemer 2012 Astrct: The present study investigted the effect of reduced protein diet in comintion with different vegetle oils (sunflower seed oil or linseed oil) on crcss trits, met qulity nd ftty cid profile in porcine muscle. Forty mle Lndrce pigs were llocted into four experimentl groups (ech n = 8) nd one control group (n = 8) t live weight of pproximtely 60 kg. The pigs were fed d liitum from 60 kg to 100 kg live weight nd restricted to 2.8 kg/dy until they reched 120 kg. In contrst to other studies, the intrmusculr ft content (IMF) did not increse in nimls of groups fed reduced protein diet nd vegetle oils. The IMF rnged etween 1.2% nd 1.4%. The growth performnce nd met qulity of the longissimus muscle ws not ffected y the diet, ut the verge dily gin (ADG) nd drip loss were ffected. The muscle ftty cid concentrtions were significntly ffected y the diet, resulting in higher n-3 FA concentrtions up to 113 mg/100 g muscle nd lower n-6/n-3 PUFA rtio for pigs fed linseed oil-contining high- nd reduced protein diets, compred to sunflower seed oil-contining diets. Keywords: reduced protein diet; linseed oil; sunflower oil; pig muscle; crcss trits; met qulity; ftty cids

2 Nutrients 2012, Introduction The mnipultion of the ftty cid composition of frm niml dipose tissues hs een of gret interest in recent yers due to n incresing demnd for the production of met with desirle nutritionl nd technologicl qulities [1]. In contrst, the risks ssocited with the consumption of red met to humn helth (e.g., cncer, dietes nd coronry hert disese) re currently controversil topic [2,3]. To reduce the risk of cncer, the World Cncer Reserch Fund report recommends limiting the consumption of red met to less thn 500 g per week [4]. The mjority of evidence for the ssocition of red met with cncer shows n increse in cncer risk for consumers with the highest level of red met consumption; however, the results of most studies hve not reched the level of sttisticl significnce [5]. Currently, the min strtegies for ltering the nutritionl profile of met re genetic selection nd/or dietry mnipultion. Selection for len growth nd ginst higher ck ft thickness hs een mjor gol of the pig industry. Dietry strtegies used to customize the ftty cid composition of pig ft hve proven very effective ecuse dietry ftty cids cn e incorported into pig muscle nd dipose tissues with few modifictions [6 8]. The intrmusculr ft (IMF) content of the pork is one importnt trit tht influences met qulity chrcteristics, such s met tenderness, juiciness, flvor nd tste [1]. The role of IMF is of prticulr interest in pigs ecuse genetic selection for len pigs hs reduced its level to elow 1% IMF, compred with 2% 4% IMF in pig muscle fifty yers go. Severl studies hve suggested fvorle reltionship etween IMF nd met tenderness nd juiciness nd recommended tht minimum level of IMF is needed to mximize met tenderness nd consequently increse consumer cceptnce [1,9]. Selected monounsturted ftty cids (MUFAs) nd polyunsturted ftty cids (PUFAs) hve numer of helth enefits. The mjority of the helth enefits hve een ssocited with n-3 PUFAs [10]. Severl studies hve investigted the effects of dietry PUFA (18:3n-3, linolenic cid; 18:2n-6, linoleic cid) source, minly linseed, rpeseed or sunflower supplements, on pig performnce nd the ftty cid composition of pig tissues. It is known tht feeding linseed diet increses the content of n-3 PUFA nd decreses the n-6/n-3 PUFA rtio in ll tissues, wheres feeding sunflower seed diet leds to n increse in the n-6 PUFA contents [11,12]. An increse in the tissue n-3 PUFA hs een oserved under these conditions nd hs een correlted with the direct incorportion of dietry PUFA into pig tissues [7]. Animl nutrition hs mjor impct on ft qulity nd composition; for exmple, protein or lysine-deficient diets re known to increse the IMF contents in pigs. Severl studies hve shown tht the IMF content in pigs cn e incresed without incresing ck ft deposition y feeding pigs low protein diets during the growing or finishing phse. This might e due to tissue-specific ctivtion of the expression of lipogenic enzymes y the reduced protein diet [13 15]. The present study investigted the effects of feeding reduced protein diets in comintion with different vegetle oils on crcss trits, met qulity nd ftty cid profile in porcine muscle. To dte, feeding reduced protein diets in comintion with different vegetle oils to pigs hs not een investigted. Bsed on the current knowledge, we hypothesized tht the reduced protein diet in comintion with linseed or sunflower seed oil would led to n increse in the IMF content in porcine muscle without detrimentl effects on met qulity.

3 Nutrients 2012, Experimentl Section 2.1. Experimentl Design Forty mle Lndrce pigs (cstrtes) were used in the diet experiment. The nimls were llocted into five feeding groups (ech n = 8) t live weight of pproximtely 60 kg (Tle 1). The pigs were fed d liitum from 60 kg to 100 kg live weight nd restricted to 2.8 kg/dy until 120 kg. The nimls in the experimentl groups (1 4) were fed two different levels of protein nd two different types of vegetle oil. The nimls in the control group were fed regulr diet without plnt oil supplementtion. The chemicl nd ftty cid compositions of the diets of the five groups high protein diet with sunflower seed oil (HPD-SO), high protein diet with linseed oil (HPD-LO), reduced protein diet with sunflower seed oil (RPD-SO), reduced protein diet with linseed oil (RPD-LO) nd control (CON) re presented in Tle 2. The HPD ws formulted to contin n verge of 19.5% crude protein, nd the RPD ws formulted to contin n verge of 15.5% crude protein. Sunflower seed oil (lipids high in linoleic cid, 18:2n-6) ws used in the HPD-SO nd RPD-SO diet groups, nd linseed oil (lipids high in linolenic cid, 18:3n-3) ws used in the HPD-LO nd RPD-LO diet groups s ft sources (Tle 2). The diets contined the sme level of metolizle energy (ME), pproximtely 13.6 MJ/kg. Thus, the energy/mino cid rtio ws lower in the RPD groups. Acquisition of feed intke ws performed for ech single niml. The pigs were weighed once per week during the diet experiment. The pig experiment ws crried out t the fcilities of the University of Rostock, Fculty of Agriculturl nd Environmentl Sciences. All experiments were conducted simultneously to void sesonl effects etween the different feeding groups. All diet composition components were nlyzed efore the eginning of the experiment s sis for the finl diet clcultions. Diet smples were tken twice during the experiment nd the chemicl nd ftty cid compositions were nlyzed y certificted lortory (LUFA Rostock) ccording to VDLUFA guidelines. The results of the diet nlyses re presented in Tle 2. All nimls were slughtered t trget live weight of 120 kg in the ttoir of the Leiniz Institute for Frm Animl Biology in Dummerstorf (Germny). The slughter nd dressing procedures were performed in ccordnce with EU specifictions. Immeditely fter slughtering, tissue smples were collected from the right side of the crcss. Longissimus muscles used for the nlysis of met qulity nd ftty cid concentrtions were tken from the 13th/14th ri nd stored t 80 C until nlysis. Tle 1. Experimentl design nd diet composition of the feeding groups. Group 1 (HPD-SO) Group 2 (HPD-LO) Group 3 (RPD-SO) Group 4 (RPD-LO) Numer (n) High protein diet High protein Reduced protein Reduced protein Feeding with sunflower diet with diet with sunflower diet with linseed seed oil linseed oil seed oil oil Group 5 (CON) Control Diet Composition * Brley Whet Soyen mel Rye Mize

4 Nutrients 2012, Tle 1. Cont. Fier mixture Fttening Supplement Linseed oil Sunflower oil Lysine * Percent sed on originl mtter Methods Tle 2. Results of chemicl- nd ftty cid composition nlyses of the diets. Group 1 (HPD-SO) Group 2 (HPD-LO) Group 3 (RPD-SO) Group 4 (RPD-LO) Group 5 (CON) Chemicl Composition * Dry mtter Crude protein Crude ft Crude fier Crude sh Strch ME (MJ/kg) Amino Acids * Lysine Methionine Cysteine Threonine Ftty Acids 14: : : :1cis :2n :3n * Percent sed on originl mtter; proportion of totl ftty cids Met Qulity Prmeters The ph vlues of the longissimus muscle smples were mesured t 45 min nd 24 h post mortem y sting ph-str CPU (Mtthäus, Eenried, Germny) into the left crcss side t the 7th/9th ri. The color of the longissimus muscle smples ws mesured t 24 h using Minolt CR 200 (Minolt GmH, Ahrensurg, Germny) with triplicte mesurements from freshly cut surfce using the prmeters L* (rightness), * (redness) nd * (yellowness). The drip loss procedure hs een descried previously [16]. For the determintion of Wrner-Brtzler sher force (WBSF), one section of longissimus muscle (2.54 cm) ws pcked in trnsprent foil 24 h fter slughter, nd then cooked in wter th t 80 C for 1 h to n internl temperture of 70 C. After cooling for 60 min t room temperture, 3 4 cores (12.7 mm) were cut from the steks prllel to the muscle fier orienttion. The WBSF ws mesured with the Texture Anlyser (Ahnseck) using Wrner-Brtzler lde (2.8 mm wide) [17]. The intrmusculr ft content (IMF) of the longissimus muscle smples were nlyzed

5 Nutrients 2012, using FoodScn Met Anlyser (FOSS Anlytic, Hillerod, Denmrk). The mesurements were sed on ner infrred (NIR) trnsmission nd covered 16 mesurement points. The results re the verge of 16 mesurements. The IMF contents were expressed s g/100 g muscle Ftty Acid Anlysis Smples of M. longissimus were thwed t 4 C. After homogeniztion (Ultr Turrx, IKA, Stufen, Germny; T25, 3 15 s, 12,000 rpm) nd the ddition of the ftty cid C19:0 s n internl stndrd, the totl lipids were extrcted in duplicte using chloroform/methnol (2:1, v/v) t room temperture. The detiled smple preprtion procedure hs een descried previously [7]. Briefly, ll of the solvents contined of tert-utylhydroxytoluene (BHT) to prevent the oxidtion of PUFAs. The finl lipid extrcts were redissolved in 300 µl of toluene, nd 25 mg liquot ws used for methyl ester preprtion. Sodium methoxide in methnol ws dded to the smples, which were shken in 60 C wter th for 10 min. Susequently, 1 ml of 14% oron trifluoride (BF 3 ) in methnol ws dded to the mixture, which ws then shken for n dditionl 10 min t 60 C. Finlly, the solvent contining the FAMEs ws reduced to dryness under n oxygen-free nitrogen strem, nd the FAMEs were resuspended in 100 µl of n-hexne nd stored t 18 C until use for gs chromtogrphy (GC) nlysis. The ftty cid nlysis of the muscle lipids ws performed using cpillry GC with CP-Sil 88 CB column (100 m 0.25 mm, Chrompck-Vrin, Lke Forest, CA, USA) tht ws instlled in PerkinElmer gs chromtogrph Autosys XL with flme ioniztion detector (PerkinElmer Instruments, Shelton, CT, USA). The detiled GC conditions were recently descried [18]. Hydrogen ws used s the crrier gs t flow rte of 1 ml/min. The split rtio ws 1:20, nd the injector nd detector were set t 260 C nd 280 C, respectively Sttisticl Anlysis The effects of the reduced protein diets nd vegetles oils were estimted y one-wy nlysis of vrince with fixed fctor group (group 1 to 5) using the GLM procedure of the SAS softwre system (SAS Systems, Relese 9.2, SAS Institute Inc., Cry, NC, USA). The lest squres mens (LSMs) nd the stndrd errors (SEM) of the LSMs re given in the tles. All post hoc tests were performed t significnce level of p 0.05 using the Tukey-Krmer correction for multiple tests. 3. Results nd Discussion The results of growth performnce nd crcss trit mesurements of mle Lndrce pigs re presented in Tle 3. The verge dily gin (ADG) ws not ffected y the experimentl diets; however, the control group (CON) exhiited lower ADG compred with experimentl groups. The verge dily feed intke (ADFI) ws not ffected y the diet. These results re consistent with recent studies investigting the effects of dietry protein level on growth performnce nd crcss trits in crossred pigs [13,14]. Furthermore, the crcss trits, e.g., ck ft, muscle re nd liver nd elly ft weights, were not influenced y the different experimentl diets, except the hot crcss weight (Tle 3).

6 Nutrients 2012, Tle 3. Growth performnce nd crcss trits of Lndrce pigs fed different diets. Group 1 Group 2 Group 3 Group 4 Group 5 (HPD-SO) (HPD-LO) (RPD-SO) (RPD-LO) (CON) Signific. LSM SEM LSM SEM LSM SEM LSM SEM LSM SEM (n = 8) (n = 8) (n = 8) (n = 8) (n = 8) Strt weight (kg) Live weight t slughter (kg) <0.001 ADG (g) <0.001 ADFI (g) Hot crcss weight, left (kg), , , Hot crcss weight, right (kg) <0.001 Liver weight (kg) Belly weight (kg) Bck ft (mm) Muscle re (cm 2 ) Different smll letters (, ) denote significnt effect of diet groups (p 0.05); ADG: verge dily gin; ADFI: verge dily feed intke. Selected met qulity prmeters of the longissimus muscles of pigs re presented in Tle 4. A numer of studies hve demonstrted tht IMF nd sucutneous ft content might e mnipulted independently through dietry mens. For exmple, feeding low protein diet increses the level of IMF with much smller effects or no effects on sucutneous ft content in pigs [9,13,14]. Indequte dietry protein nd/or lysine limit protein synthesis nd increse the mount of energy ville for ft deposition, resulting in higher IMF. In contrst, the IMF level in the Lndrce pigs of the present study ws not ffected y the reduced protein level or y the use of linseed or sunflower seed oil in the diet. The IMF content rnged etween 1.2% nd 1.4% (Tle 4). One possile explntion for unffected IMF contents could e the smller difference of protein level in the diets (19.4% 19.6% HPD) vs. 15.0% 15.7% in the RPD groups compred with other studies (10% 13% low protein vs. 18% 23% for the high protein diet) [13,14]. No significnt effects were oserved etween the different diets for muscle color (L*, *, nd *), consistent with the results of recent studies y Alonso et l. [9] nd Guo et l. [14]. However, one other study detected higher L*, * nd * color vlues in the longissimus muscles of pigs fed low protein diets due to higher IMF contents nd higher concentrtions of 12:0 nd 14:0 in the muscle, which mkes the IMF less trnslucent nd leds to greter color sturtion [19]. Neither reduced protein level nor dietry vegetle oil supplementtion ffected sher force (WBSF), ph vlue or cooking loss of the longissimus muscle (Tle 4). Our results indicte tht the pigs of ll diet groups were in good condition pre-slughter, resulting in norml ph development with tendency towrd etter wter holding chrcteristics in the muscles of HPD-LO pigs (lower drip loss). The lck of significnt differences in IMF contents etween the dietry tretments cn contriute to the similr sher forces mesured in the longissimus muscle (Tle 4). Additionlly, comprle muscle sher force seems to e reflection of uniform growth nd development pttern, indicting similr sizes of muscle fiers nd IMF contents.

7 Nutrients 2012, Tle 4. Longissimus muscle qulity of Lndrce pigs fed different diets. Group 1 Group 2 Group 3 Group 4 Group 5 (HPD-SO) (HPD-LO) (RPD-SO) (RPD-LO) (CON) Signific. LSM SEM LSM SEM LSM SEM LSM SEM LSM SEM (n = 8) (n = 8) (n = 8) (n = 8) (n = 8) IMF (%) ph (45 min) ph (24 h) Color L* * * Drip loss (g/100 g) Cooking loss (g/100 g) Sher force (kg/cm 2 ) Different smll letters (, ) denote significnt effect of diet groups (p 0.05); IMF: intrmusculr ft. The effects of dietry PUFA supplements, minly linseed, rpeseed or sunflower seed oils, cke or seeds, on pig performnce nd ftty cid composition of tissues hve een investigted intensively. It is known tht feeding linseed diet increses the n-3 PUFA content nd decreses the n-6/n-3 ftty cid rtio in ll tissues, wheres feeding sunflower seed leds to n increse in the n-6 PUFA contents due to the direct incorportion of the dietry PUFA into pig tissues [7,11,20,21]. The single ftty cid concentrtions of the longissimus muscle in pigs re shown in Tle 5, nd the selected totl ftty cid concentrtions re presented in Figure 1. The muscle ftty cid concentrtions of the present study ppered to e significntly ffected y the diet, resulting in significntly higher n-3 FA concentrtions (up to 113 mg/100 g muscle) in linseed oil-contining high- nd reduced protein diets, compred to sunflower seed oil diets; only docoshexenoic cid (22:6n-3, DHA) ws not significntly incresed. In most of the previous studies, the use of n-3 PUFA-rich vegetle oils showed no or only smll effects on the intrmusculr DHA level [7,15,21,22]. Feeding linseed oil-contining HPD- nd RPD diets significntly decresed the concentrtion of single nd totl n-6 PUFA in longissimus muscle of pigs compred with the sunflower seed oil-contining fed groups nd the control group (Tle 5 nd Figure 1). Consequently, the high level of n-3 PUFAs, which re eneficil for humn nutrition, nd the lower level of n-6 PUFAs in pigs fed linseed oil-contining diets cused eneficilly low n-6/n-3 PUFA rtio in the muscle compred with sunflower seed oil contining diets nd the control diet. The n-6/n-3 PUFA rtio ws 1.8:1 in muscle of pigs fed linseed oil contining HPD- nd RPD diets, which corresponds to the n-6/n-3 PUFA rtio recommended y the Germn Nutrition Society ( 5:1) [23]. The concentrtions of single sturted nd totl sturted ftty cids (SFA) were not ffected y either the protein content or the type of oil supplement (Tle 5 nd Figure 1). Other studies showed tht feeding low protein diet with n incresed IMF level resulted in elevted concentrtions of 14:0, 16:0 nd totl SFAs, s reflection of the higher IMF contents [19]. Additionlly, oleic cid (18:1cis-9), the most undnt ftty cid in pig muscles, nd totl monounsturted ftty cids (MUFAs) were not ffected y the different dietry tretments.

8 mg/100g muscle Nutrients 2012, Tle 5. Ftty cid concentrtions (longissimus muscle, mg/100 g muscle) of Lndrce pigs fed different diets. Group 1 Group 2 Group 3 Group 4 Group 5 (HPD-SO) (HPD-LO) (RPD-SO) (RPD-LO) (CON) Signific. LSM SEM LSM SEM LSM SEM LSM SEM LSM SEM (n = 8) (n = 8) (n = 8) (n = 8) (n = 8) Sum FA : : : : : :1cis :1cis :2n , < :3n < :2n , ,c , < :3n , , < :3n < :4n < :5n < :4n < :5n < :6n Different smll letters (, ) denote significnt effect of diet groups (p 0.05). Figure 1. Totl ftty cid concentrtions (longissimus muscle) of Lndrce pigs fed different diets c d Group 1 (HPD-SO) Group 2 (HPD-LO) Group 3 (RPD-SO) Group 4 (RPD-LO) Group 5 (CON) N-6/n-3 PUFA rtio Totl SFA 1 Totl 2MUFA Totl 3PUFA Totl 4n-3 PUFA Totl 5n-6 PUFA Different smll letters (,, c, d ) denote significnt effect of diet groups (p 0.05); totl SFA: 10:0 + 11:0 + 12:0 + 13:0 + 14:0 + 15:0 + 16:0 + 17:0 + 18:0 + 20:0 + 21:0 + 22:0 + 23:0 + 24:0; totl MUFA: 14:1 + 15:1 + 16:1 + 17:1 + 18:1t + 18:1c9 + C18:1c11 + C22:1 + C24:1; totl PUFA: 18:2t + 18:2n :3n :4n :3n :4n :5n :1 + 22:4n :5n :6n-3 + c9,tr11cla + 18:3n :2n :3n :2n-6; totl n-3 PUFA: 20:3n :6n :5n :5n :4n :3n-3; totl n-6 PUFA: 22:2n :2n :3n :4n :3n :2n :4n-6.

9 Nutrients 2012, Conclusions In contrst to our hypothesis, reduced protein diet in comintion with linseed or sunflower oil did not led to n increse in the IMF content of the longissimus muscle of mle Lndrce pigs. However, diets supplemented with linseed oil llow the production of pork met with high n-3 ftty cid content nd low n-6/n-3 PUFA rtio, which is eneficil for humn nutrition. Additionlly, feeding pigs reduced protein diet in comintion with linseed or sunflower oil hd no detrimentl effects on muscle met qulity. Acknowledgments The uthors wish to thnk B. Jentz, M. Dhm, U. Bretschneider nd H. Peters of the Deprtment of Muscle Biology nd Growth who collorted in the smple preprtion, HRGC nd met qulity mesurements. Conflicts of Interest The uthors declre no conflicts of interest. References 1. Wood, J.D.; Enser, M.; Fisher, A.V.; Nute, G.R.; Sherd, P.R.; Richrdson, R.I.; Hughes, S.I.; Whittington, F.M. Ft deposition, ftty cid composition nd met qulity: A review. Met Sci. 2008, 78, Corpet, D.E. Red met nd colon cncer: Should we ecome vegetrins, or cn we mke met sfer? Met Sci. 2011, 89, Fretts, A.M.; Howrd, B.V.; McKnight, B.; Duncn, G.E.; Beresford, S.A.A.; Mete, M.; Eilt-Adr, S.; Zhng, Y.; Siscovick, D.S. Associtions of processed met nd unprocessed red met intke with incident dietes: The strong hert fmily study. Am. J. Clin. Nutr. 2012, 95, World Cncer Reserch Fund, Americn Institute for Cncer Reserch. Policy nd Action for Cncer Prevention; WCRF nd AICR: Wshington, DC, USA, Wyness, L.; Weichselum, E.; O Connor, A.; Willims, E.B.; Rilex, H.; Stnner, S. Red met in the diet: An updte. Nutr. Bull. 2010, 36, Durn-Montge, P.; Relini, C.E.; Brroet, A.C.; Lizrdo, R.G.; Esteve-Grci, E. De novo ftty cid synthesis nd lnce of ftty cids of pigs fed different ft sources. Livest. Sci. 2010, 132, Nuernerg, K.; Nuernerg, G.; Dnnenerger, D. Effect of extruded linseed on growth nd lipids of muscle nd ck ft in pigs. Fleischwirtschft 2011, 91, Sootk, W.; Flis, M.; Antoszkiewicz, Z.; Lipinski, K.; Zdunczyk, Z. Effect of ot y-product ntioxidnts nd vitmin E on the oxidtive stility of pork from pigs fed diets supplemented with linseed oil. Arch. Amin. Nutr. 2012, 66, Alonso, A.; Cmpo, M.M.; Provincil, L.; Roncles, P.; Beltrn, J.A. Effect of protein level in commercil diets on pork met qulity. Met Sci. 2010, 85, Clder, P.C.; Dngour, A.D.; Diekmn, C.; Eilnder, A.; Koletzko, B.; Meijer, G.W.; Mozffrin, D.; Niinikoski, H.; Osendrp, S.J.; Pietinen, P.; et l. Essentil fts for future helth. Proceedings of the 9th Unilever Nutrition Symposium, My Eur. J. Clin. Nutr. 2010, 64, S1 S13.

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