Effects of supplementing organic microminerals and methionine with or without limiting growth during the rearing phase of replacement gilts on lameness, growth, and body composition1 Lluís Fabà,†, Josep Gasa,† Mike D. Tokach,‡ Evelia Varella,|| and David Solà-Oriol† Animal Nutrition and Welfare Service, Department of Animal and Food Science, Universitat Autònoma de † Barcelona, Bellaterra 08193, Spain; ‡Department of Animal Sciences and Industry, Kansas State University, Manhattan, KS 66506-0201; and ||Tecnología & Vitaminas S.L., Alforja 43365, Spain ABSTRACT: Previous research suggested that and were offered ad libitum. Low Lys did not lameness in growing pigs could be reduced using affect feed intake but rather reduced average feeding strategies, such as limiting growth rate daily gain (ADG) by 6.35% and the final BW by and supplementing trace minerals (TM) and (or) 3.80% compared with standard Lys (P < 0.001). methionine (Met). The present study evaluates Low Lys reduced ADG (P < 0.001) and gain:feed effects of 1) TM and Met and 2) limiting total (P = 0.012) during phase I but not during phase lysine (Lys) during the rearing phase (90 d) of II. Lameness prevalence was 7.92% during rear- gilts (as a means to limit growth rate) on lame- ing and increased with time (P < 0.001). Final ness, performance, and sow claw health and pro- BW (151 kg) and ADG (989 g) were similar (P ductivity (to first parity). Gilts (n = 240; 58.0 ± > 0.05) whether gilts displayed lameness or not. 11.1 kg body weight [BW]) were blocked, distrib- Lameness was low in severity and not affected by uted into pens of 10 gilts, and pens were allo- dietary factors. However, TM- plus Met-fed gilts cated to a 2 × 2 factorial arrangement. Factors were 19.2 kg heavier (P = 0.016) than were con- were: 1) control or TM plus Met, which provided trol at lameness detection. On the sow farm, there additional 10, 20, and 50 mg/kg of chelated cop- was no evidence for differences in lameness or per, manganese, and zinc, respectively (0.1%, claw lesions among previous dietary treatments. Aplomotec Plus, Tecnología & Vitaminas, S.L.; In conclusion, lameness prevalence during the Alforja, Spain), and a 1.01 Met:Lys ratio and rearing phase was similar, independent of TM 2) standard Lys was formulated to meet growth plus Met supplement, low Lys, or the interaction. requirements or low Lys to 19% below growth Insufficient reduction of ADG and low severity requirements. Feeding was provided through in lameness may have limited the potential of die- two phases, first between 119 and 163 d of age tary treatments. Moreover, a greater deficiency (phase I) and the second between 163 and 209 d of Lys would be needed to achieve the degree of of age (phase II). Diets had 2.43 and 2.31 Mcal growth reduction previously reported to lessen net energy/kg for phases I and II, respectively, lameness through feed restriction. Key words: growth, lameness, lysine, minerals, pigs © The Author(s) 2019. Published by Oxford University Press on behalf of the American Society of Animal Science. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-com- mercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Transl. Anim. Sci. 2019.3:717–730 doi: 10.1093/tas/txz038 717 718 Fabà et al. The authors thank the graduate students for their help, techni- This study was supported by the Centre for the Develop- 1 cal support received from the SNIBA staff and, also, the farm ment of Industrial Technology (Spanish Innovation Agency, owners for the opportunity to work in their facilities. Ministry of Industry Tourism and Trade), Madrid, Spain; 2 Corresponding author: Lluis.Faba@uab.cat Project IDI-20150749. Appreciation is expressed to Tecnología Received December 4, 2018. & Vitaminas S.L. for providing the feed and microminerals. Accepted April 15, 2019. INTRODUCTION claws of gilts entering into production, using two different strategies in a factorial approach: 1) sup- Lameness is a persistent problem and a welfare plementing organic TM and Met and 2) reducing concern in the swine industry (Kilbride et al., 2009; ADG by lowering dietary Lys by 19%. Pluym et al., 2013) as a primary reason for gilt failure (Engblom et al., 2008; Jensen et al., 2010). MATERIAL AND METHODS Disorders such as osteochondrosis (OC, a defec- tive endochondral ossification) and claw lesions are Animal Care and Use important causes of lameness (Yazdi et al., 2000; de Koning et al., 2015). Lameness includes a high The animals used were produced and housed in cost per lame sow, estimated at up to $180 in the commercial swine facilities in northern Spain (Lleida). United States (Deen et al., 2008) and between $330 A rearing facility provided gilts to two sow sites with and $380 in Finland (Niemi et al., 2017). similar performance and management conditions. In a previous study, lameness was reduced when The Ethical Committee on Animal Experimentation supplementing organic trace minerals (TM) copper (CEEAH) at the Universitat Autònoma de Barcelona (Cu), manganese (Mn), and zinc (Zn) in combina- reviewed and approved the procedures and protocols tion or not with high methionine (Met) such as a for this experiment according to the guidelines of the 1.02 Met:lysine (Lys) ratio (Fabà et al., 2018). In European Union (Directive 2010/63/EU). a subsample study, TM also increased tibia break- age force, bone density, and metacarpal weight and Experimental Design, Housing, and Dietary ash content (Fabà et al., 2019). Similarly, Frantz Treatments et al. (2008) reported effects of Cu–Mn and com- bined Met and threonine to reduce OC scores. TM, Maternal-line gilts (n = 240; DanAvl Dania acknowledged as being necessary in the keratiniza- Hybrid line, Landrace × Yorkshire; DanBred tion and horn production process (van Riet et al., International; Sant Cugat del Vallés, Spain) acquired 2013), improve claw health (Varagka et al., 2016). from a breeding production company were used in Nonetheless, extended research supports that a 90-d experiment. Gilts of 15 to 17 wk of age and other factors such as genotype, feed composition, 58.0 ± 11.1 kg of body weight (BW) were individu- average daily gain (ADG), housing conditions, ally identified with ear tags, weighed, and blocked and mechanical stress interact and influence OC, into pens of 10. Pens (0.90 m2/gilt; 60% slatted and claw health, and therefore lameness (Nakano and 40% solid floor) were randomly allocated to one of Aherne 1988; Heinonen et al., 2013; Pluym et al., four dietary treatments in a 2 × 2 factorial arrange- 2013; de Koning et al., 2014a, 2014b; Quinn et al., ment, the main factors being: 1) TM and Met levels 2015; Le et al., 2016). and 2) Lys concentration. The TM and Met levels Fast growth rate has become controversial for were control as 10, 40, and 110 mg/kg Cu, Mn, and increasing OC and lameness in pigs (Busch and Zn, respectively, and of inorganic sources and 0.31 Wachmann 2011; Quinn et al., 2015; de Koning to 0.39 Met:Lys ratio or TM plus Met, which pro- et al., 2014b) or not (Ytrehus et al., 2004a, 2004b, vided the diet with an additional 10, 20, and 50 mg/ 2007; Tóth et al., 2016). Therefore, intentionally lim- kg of chelated Cu, Mn, and Zn, respectively (0.1%, iting ADG may have a positive effect on lameness. Aplomotec Plus, Tecnología & Vitaminas, S.L.; Previous studies mainly used feed restriction (Quinn Alforja, Spain), and a 1.01 Met:Lys ratio. Lys lev- et al., 2015; de Koning et al., 2014b); however, growth els were standard Lys, which provided 165 g crude rate could be modulated by altering amino acid den- protein (CP)/kg with 10.0 g Lys/kg between 119 and sity (Rozeboom and Johnston, 2007; Díaz et al., 163 d of age (phase I) and 140 g CP/kg with 8.0 g 2017), which would be a more practical approach. Lys/kg between 163 and 209 d of age (phase II) or The present objective is to evaluate replace- low Lys with 155 g CP/kg CP with 8.1 g Lys/kg in ment gilt diets on lameness, body composition, per- phase I and 140 g CP/kg with 6.5 g Lys/kg in phase formance, and carryover effects on lameness and II. A total of six pen replicates per treatment were Translate basic science to industry innovation Microminerals and Met with limited Lys 719 Table 1. Composition of the experimental diets (phases I and II) offered to growing gilts (as-fed basis), % Phase I (119–163 d of age) Phase II (164–209 d) Control TM plus Met Control TM plus Met Ingredient, kg Standard Low Lys Standard Low Lys Standard Low Lys Standard Low Lys Corn 20.4 23.8 19.8 22.6 16.5 16.6 15.0 15.6 Wheat 25.0 25.0 25.0 25.0 25.0 25.0 25.0 25.0 Barley 25.0 24.8 24.8 25.0 25.0 25.0 25.0 25.0 Wheat middlings – – – – 6.00 6.00 5.95 6.00 Soybean meal 15.6 13.8 15.8 13.6 7.00 7.55 7.05 7.70 Sunflower meal 6.00 5.65 6.00 6.00 7.00 7.00 7.00 7.00 Bakery byproduct – – – – 9.15 8.90 10.0 9.25 Fat 2.90 2.45 2.85 2.50 0.30 0.30 0.30 0.30 Calcium carbonate 1.08 1.10 1.06 1.03 1.60 1.60 1.54 1.55 Dicalcium phosphate 1.35 1.38 1.35 1.38 1.01 0.98 1.00 0.99 Salt 0.40 0.40 0.40 0.40 0.40 0.40 0.40 0.40 Met 0.13 – 0.84 0.63 – – 0.63 0.45 hydroxy analogue L-Lys HCl 0.50 0.23 0.50 0.24 0.48 0.18 0.48 0.17 L-threonine 0.09 – 0.09 – 0.06 – 0.06 – L-tryptophan 0.03 – 0.03 – – – – – Premix 1 0.40 0.40 0.40 0.40 0.40 0.40 0.40 0.40 Premix TM2 – – 0.10 0.10 – – 0.10 0.10 Calculated composition, % Net Energy, kcal kg-1 2,425 2,425 2,425 2,425 2,310 2,310 2,310 2,310 Crude protein 16.5 15.5 16.5 15.5 14.0 14.0 14.0 14.0 Total Lys 1.00 0.81 1.00 0.81 0.80 0.65 0.80 0.65 Total Met 0.39 0.28 1.02 0.82 0.25 0.25 0.80 0.64 Met:Lys 0.39 0.35 1.02 1.01 0.31 0.38 1.01 0.98 SID3 Lys 0.90 0.72 0.90 0.72 0.70 0.56 0.70 0.56 SID Met 0.36 0.24 0.99 0.79 0.22 0.23 0.77 0.61 SID Met + cysteine 0.65 0.52 1.28 1.07 0.49 0.49 1.03 0.88 SID tryptophan 0.21 0.17 0.21 0.17 0.15 0.15 0.15 0.15 SID threonine 0.58 0.48 0.58 0.47 0.46 0.41 0.46 0.41 Calcium, % 0.90 0.91 0.91 0.90 1.02 1.01 1.01 1.02 Phosphorus, % 0.59 0.59 0.59 0.59 0.57 0.57 0.57 0.57 1 Vitamin–minerals premix provided per kg of feed: vitamin B2, 3.5 mg; vitamin B12, 0.035 mg; nicotinamide, 20 mg; folic acid, 1.25 mg; vitamin D3, 2,000 IU; vitamin A, 10,000 IU; vitamin E, 30 mg; vitamin K3, 1 mg; vitamin B1, 1 mg; vitamin B6, 2.4 mg; D-calcium pantothenate, 14 mg; biotin, 0.125 mg; choline chloride, 400 mg; Fe (from FeSO4.H2O), 120 mg; I (from Ca(IO3)2), 0.5 mg; Cu (from CuSO4·5H2O), 10 mg; Mn (from MnO2), 40 mg; Zn (from ZnO2), 110 mg; Se (from Na2SeO3), 0.4 mg; phytase EC 3.1.3.26, 1,500 FTU; and butylhydroxytoluene, 25 mg. 2 Vitamin–minerals premix provided per kg of feed: 10, 20, and 50 mg/kg of chelated cooper, manganese, and zinc, respectively (Aplomotec Plus, Tecnología & Vitaminas, S.L., Alforja, Spain). 3 Standard ileal digestible; calculated using SID coefficients for the various ingredients obtained from the NRC (2012). used. Feed was provided ad libitum and in pelleted blocks were equally divided into two similar desti- form using a single-space dry feeder in each pen. nation farms. Details of the farms’ management and Also, gilts had free access to fresh water provided characteristics were previously described by Fabà through drinking nipples. The entire rearing was et al. (2018). Briefly, the sow farms had a similar divided into two feed phases of 44 and 46 d, with inventory (1700–1800 sows) and were in the same diets containing 2,425 and 2,310 kcal net energy region (20 km) and integrative company and fed (NE)/kg, respectively (Table 1). For each experimen- by the same feed mill. Equivalent feed and routines tal period, feeds were formulated to meet or exceed were provided. Gilts were penned (5–8 gilts/pen) for nutrient requirements (FEDNA, 2013) and accord- 30 d in a quarantine-adaptation barn (4 × 3 m; 40% ing to the genetics recommendations (Tybirk, 2015), solid floor and 60% concrete slatted floor). Then, except for Lys. gilts were placed in crates for a minimum of 2 wk In the overall rearing phase, six gilts died and before service after at least the second detected heat. four had nonviable leg conformation. Therefore, the After confirming gestation (28 d), gilts and sows remaining 230 gilts across dietary treatments and were moved to group housing pens of 70 females (1.5 Translate basic science to industry innovation 720 Fabà et al. m2/female; 30% solid floor and 70% concrete slatted observer. The gait scoring was a subjective meth- floor) with an electronic feeding system (EFS). The odology adapted from Welfare Qualitys (2009) and concrete slatted floor areas had 80-mm wide beams Mustonen et al. (2011) as: not lame (0); moderate and a 20-mm opening between beams. difficulties with gilts having reluctance to move and The first diet in the sow farm was the phase II reduced walking speed or some difficulties with control (standard Lys), which was provided for 30 exercise including slightly shortened stride to obvi- d to all gilts and offered ad libitum. Subsequently, ous limp (1), and, severe difficulties with gilts being gestation feed formulated to 2,200 kcal NE/kg, and minimum weight bearing to incapable of standing 5.7 g/kg standardized ileal digestible (SID) Lys was (2). The evaluation was performed allowing the gilt provided. From service to 28 d of gestation, feed to advance and freely explore a familiar (two train- was individually adjusted according to the body ings) corridor that was well illuminated (daylight composition score (2.2 to 3.2 kg/d). After confirmed plus led lamps) without obstacles ahead. Also, gilts gestation, the feeding level was 2.2 kg/d for gilts and were classified as lame (obvious limping) or not a range between 2.3 and 2.5 kg/d in multiparous lame (no limping), and within the lame category sows depending on the body composition score. In whether or not they were severe (barely bearing the lactation room, sows received 2 kg/d of lacta- weight on the affected limb) for binomial analysis. tion feed (2,340 kcal NE/kg and 9.3 g/kg SID Lys) On the sow farm, gait score and lameness were until farrowing day, and from the day after onward, evaluated by the same observer at three different feed was progressively increased to ad libitum. times: 1) before first service; 2) at day 109 of gesta- tion, and 3) at weaning. Lameness evaluation was Performance and Body Composition Measurements performed during a 2-min observation by walking (6–10 m) on a solid floor corridor (moving females Measurements of BW, backfat (BF), and loin to the insemination line at first service and at wean- depth were individually collected every 3 wk (days ing) or a 2-min observation inside the group-hous- 119, 141, 164, 184, and 209 of age). The BF and loin ing pens in gestation. depth were always collected by the same trained per- son at point P2 (6 cm from the midline and the last Claw Lesions rib level) using an ultrasound scanner (AV-3000V Digital Handheld Electronic B Ultrasound In the farrowing room, females were evaluated Scanner, AMBISEA Technology Corp., Ltd; Hong for claw lesions following the protocol previously Kong, China). Feed intake was measured by pen on reported by Fabà et al. (2018). Briefly, the lesions a weekly basis. The ADG, average daily feed intake evaluated were: toe dewclaws; heel sole overgrowth (ADFI), and gain:feed ratio (G:F) were calculated and cracks; white line; hoof wall cracks; long hoofs; by pen for each feeding phase and overall. Similarly, and asymmetry between digit claws. The score grades SID Lys intake per kg BW gain was also calculated were: 0 = none, 1 = mild moderate (without affecting by phases using formulated feed composition. the integrity of the claw), and 2 = severe (affecting On the sow farm, BW was measured at first the integrity of the claw, including gait difficulties service and BF was collected at service, before far- or indicating clinical signs of pain). The assessment rowing, and at weaning. Productive data were also included all claws and both outer and inner digits. recorded for the first parity. The reproductive per- Overall, only few (n = 5) lesions were classified as formance included the number of total born, born severe, and final analysis was for complete prev- alive, stillborn, and weaned piglets. The breeding alence independent of severity. The toe dewclaw, performances recorded were returning to service and white line, and hoof wall crack are lesions associated weaning-to-estrus interval. Also, removal reasons with horn properties and influenced after supple- and the date were recorded. Removals classified as menting organic TM (Varagka et al., 2016). Those reproductive disorder included not displaying a first lesions were also grouped as hoof lesions, including estrus, abortion, or consecutive repeating estrus. all females that had at least one of the three lesions. Lameness and Gait Score Statistical Analysis During rearing, lameness and gait score were The statistical procedures were performed using evaluated by studying walking pattern on a hard, SAS v9.4 (SAS Inst. Inc.; Cary, NC). The experi- solid floor for a distance of 6 m at an average mental unit was the gilt for lameness, claw lesions, age of 119, 141, 164, 184, and 209 d by the same and number of piglets, whereas the pen (10 gilts) Translate basic science to industry innovation Microminerals and Met with limited Lys 721 was the unit for BW, BF, loin depth, ADG, ADFI, Feeding low Lys did not affect ADFI but rather Lys intake per kg of BW gain, and G:F ratio. The reduced overall ADG (P < 0.001) by 6.35% and different variables were evaluated for normality and final BW (P < 0.001) by 3.80%, compared with homoscedasticity by using the Shapiro–Wilk and standard Lys (Table 2). According to the different Levene’s test and examining the normal plot (PROC feed phases, gilts fed low Lys had a lowered ADG UNIVARIATE). For all parametric analysis, the (P < 0.001) and G:F ratio (P = 0.012) between 119 Tukey–Kramer adjustment was used to determine and 163 d but not from 163 to 209 d. There was no significant (P < 0.05) and marginal (P < 0.10) dif- evidence of main effects due to TM plus Met sup- ferences among dietary treatments. plements on gilt ADG, ADFI, or G:F. Throughout The BW, loin depth, BF, and lameness occur- the growing phase, gilts fed low Lys had a lower rence over the experimental time were analyzed BW than with standard Lys (P < 0.05). However, an using repeated-measures models, including die- interaction at day 184 showed that gilts fed TM plus tary treatment and time (days of experimental Met and low Lys were 2.8 kg heavier (SE = 1.796; study) as fixed effects and block as a random effect P = 0.034) than were control gilts fed low Lys, not using mixed-model methods (PROC GLIMMIX). different than control gilts fed the standard Lys but Additionally, ADG was analyzed using repeat- lighter (P = 0.034) than gilts fed TM plus Met and ed-measures with lameness and time as fixed effects standard Lys. and block and pen as the random effects. In this The BF was not different amongst dietary treat- case, it was analyzed separately for the dietary sup- ments until the end of rearing. Then, an interaction plements strategy and the limited Lys strategy due to occurred where gilts fed control and low Lys had the low incidence of lameness (PROC GLIMMIX). reduced (P = 0.049) BF as compared with the gilts Furthermore, phase and overall ADG, ADFI, Lys fed TM plus Met with low Lys and the control with intake per BW gain, and G:F were analyzed using standard Lys, with TM plus Met with standard Lys the general linear model (PROC GLM). being intermediate. Interactions for loin depth were Sow farm measurements of BW, BF, and sow pro- observed with some inconsistency but seemed to ductivity were analyzed using the general linear model align with those of BW at 184 d. Gilts fed low Lys (PROC GLM). Claw lesions, grouped hoof lesions, without supplements (control) had lower loin depth and lameness occurrence at different times were ana- than with standard Lys (P < 0.02), whilst low Lys lyzed with a Binomial model (PROC GENMOD). supplemented was intermediate at 163 and 184 d of Fisher’s Exact test was used for testing removal rea- age (Table 2). Differently, at the end of rearing (day sons (PROC FREQ). The main fixed effects included 209 of age), gilts fed TM plus Met with low Lys had dietary treatment and sow farm. Reproductive per- a lower loin depth than with standard Lys in con- formances of females classified as lame (eventually trol, with others being not different. More clearly, displayed lameness) or not lame (never displayed at 163 and 184 d of age, gilts fed low Lys diets had lameness) on the sow farm were analyzed using a non- a reduced loin depth when compared with gilts fed parametric Binomial model (PROC GENMOD). standard Lys (P = 0.05). Results from the lameness assessments are RESULTS presented in Table 3. During the rearing period, lameness prevalence was 7.92% and appeared in a Limiting dietary Lys reduced growth; however, CI between 119.6 and 139.5 kg of BW. The propor- neither such reduction, nor the dietary supplemen- tion of lameness at a given moment increased with tation of TM and Met or the combination of the time and BW (P < 0.001). The final BW and overall slower growth and dietary supplements were capable ADG were not different (P > 0.05) when compar- of reducing lameness prevalence compared with the ing gilts that eventually undergo lameness (988 g control, although age and BW at lameness detection and 150.1 kg, respectively) and those that never had were higher on gilts supplemented with TM and signs of lameness (990 g and 151.2 kg, respectively). Met than on the control gilts. Results are presented Lameness prevalence was not different among first for performance and lameness during rearing dietary treatments. However, lame gilts fed the TM and second for the measurements in the sow farm. plus Met diets were 19.2 kg heavier (SE = 5.04, P = 0.016) and 17.9 d older (SE = 5.17, P = 0.034) Rearing at lameness detection when compared with con- trol-fed lame gilts. Figure 1 presents ADG by phases Overall performance showed no interactions and for gilts fed TM plus Met that were classified as between limited Lys and dietary supplements. lame (a gilt that eventually undergoes lameness) or Translate basic science to industry innovation 722 Fabà et al. Table 2. Effects of organic TM plus Met and lowering Lys dietary treatments provided (90 d) to rearing gilts on performance and body composition Control1 TM plus Met1 P-value Standard Lys2 Low Lys2 Standard Lys2 Low Lys2 SEM Min Met Lys MinMet × Lys Body weight, kg 119 d 58.3 58.1 58.2 57.8 1.796 0.813 0.889 0.940 141 d 87.2x 84.1y 87.2x 85.2xy 0.685 0.047 0.091 163 d 112.1 106.2 112.5 108.0 0.543 <0.001 0.491 184 d 132.7ab 126.1c 134.5a 129.9b 0.030 <0.001 0.034 209 d 153.9 146.9 154.3 149.6 0.189 <0.001 0.141 Backfat depth, mm 119 d 7.19 7.33 7.04 7.36 0.353 0.805 0.352 0.695 141 d 9.04 9.32 9.04 9.58 0.640 0.145 0.173 163 d 11.2 10.8 11.1 11.5 0.429 0.953 0.348 184 d 12.9 12.7 13.0 13.3 0.270 0.945 0.407 209 d 15.0a 14.2b 14.3ab 14.9a 0.998 0.603 0.049 Loin depth, mm 119 d 30.1 30.4 29.4 29.9 0.742 0.605 0.628 0.242 141 d 39.9 39.5 39.9 39.6 0.452 0.271 0.729 163 d 49.5a 48.9b 50.2ab 49.2ab 0.939 0.036 0.019 184 d 62.8a 59.7b 64.1a 61.1ab 0.074 <0.001 <0.01 209 d 67.7a 66.3ab 66.4ab 65.3b 0.129 0.106 0.030 Average daily gain, g 119–163 d 1,220 1,090 1,225 1,133 17.5 0.172 <0.001 0.275 163–209 d 907 875 908 900 41.5 0.751 0.635 0.781 Overall 1,018 944 1,028 972 23.4 0.439 0.011 0.705 Average daily feed intake, g 119–163 d 3,055 2,953 3,040 3,001 51.2 0.761 0.183 0.554 163–209 d 3,403 3,263 3,393 3,245 103 0.892 0.179 0.968 Overall 3,238 3,204 3,215 3,220 98.8 0.887 0.971 0.885 Gain:feed ratio 119–163 d 0.40 0.37 0.40 0.38 0.010 0.609 0.012 0.807 163–209 d 0.27 0.27 0.27 0.28 0.011 0.834 0.727 0.727 Overall 0.32 0.30 0.32 0.30 0.013 0.173 0.905 0.999 1 Control, basal diet and TM plus Met (MinMet), with additional 10, 20, and 50 mg/kg of chelated cooper, manganese, and zinc, respectively (0.1%, Aplomotec Plus, Tecnología & Vitaminas, S.L., Alforja, Spain), and increased Met:Lys ratio as 1.01. 2 Standard Lys provided 165 crude protein (CP)/kg with 10.0 g Lys/kg between 119 and 163 d of age and 140 g CP/kg with 8.0 g Lys/kg between 164 to 209 d of age; or low Lys, set first to 155 g CP/kg with 8.1 g Lys/kg and second phase to 140 g CP/kg with 6.5 g Lys/kg. a,b Values within a row with different superscripts differ significantly at P < 0.05. x,y Values within a row with different superscripts trend at P < 0.10. never lame (a gilt that never had signs of lameness). lowered (P < 0.001) ADG as compared with stand- Between 163 and 184 d of age, ADG increased ard Lys for never-lame gilts; however, lame gilts (P < 0.01) for a mineral-plus-Met strategy (lame were intermediate for both standard and low Lys. or never lame) as compared with a control strategy Finishing the rearing phase (184 to 209 d of age), of never-lame gilts, while control-lame gilts were lame gilts fed standard Lys tended to have reduced intermediate. Late in growth (184 to 209 d of age), (P = 0.097) ADG compared with never-lame gilts lame gilts had reduced (P = 0.015) ADG within the on both standard Lys and low Lys diets; neverthe- control fed gilts, but gilts from TM plus Met were less, lame gilts on low Lys were intermediate. intermediate for both lame and never-lame gilts. The same assessment of ADG and lameness, but Sow Farm for a Lys dietary strategy, is presented in Figure 2. Between 113 and 141 d of age, lame gilts fed the Lameness on the sow farm increased to 17.4% low Lys and never-lame gilts fed standard Lys had at first service, then decreased to 11.3% at the greater ADG than never-lame females fed low Lys end of gestation, increasing to 15.2% at weaning. (P = 0.001). From 141 to 163 d of age, low Lys There was no evidence of differences for lameness Translate basic science to industry innovation Microminerals and Met with limited Lys 723 Table 3. Effects of TM plus Met and lowering Lys dietary treatments provided (90 d) to rearing gilts (from 58.0 ± 11.1 kg to 151 ± 14.1 kg of BW) on lameness during rearing and sow productive phases Control1 TM plus Met1 P-value Standard Lys2 Low Lys2 Standard Lys2 Low Lys2 SEM Min Met Lys MinMet × Lys Gilts, n 59 58 56 57 BW at lameness, kg 120.2 119.8 134.2 144.4 7.75 0.016 0.515 0.456 Age at lameness, d 173.8 175.8 185.3 198.2 6.92 0.034 0.346 0.462 Lameness, % During rearing3 6.67 8.33 10.0 6.67 19.530 0.775 0.834 0.456 Early gestation4 15.5 22.6 14.1 17.6 14.98 0.587 0.309 0.746 Late gestation5 15.6 12.1 7.10 10.6 17.76 0.246 0.859 0.421 Lactation6 17.1 19.1 8.88 15.8 16.04 0.211 0.304 0.503 Overall 20.5 32.8 19.6 24.0 13.49 0.447 0.532 0.625 Gait score, 0–2 During rearing 0.15 0.13 0.15 0.15 0.052 0.854 0.789 0.152 Early gestation 0.22 0.29 0.19 0.18 0.124 0.272 0.763 0.486 Late gestation 0.19 0.17 0.09 0.12 0.057 0.140 0.742 0.587 Lactation 0.24 0.26 0.11 0.21 0.096 0.108 0.222 0.344 Overall 0.19 0.23 0.14 0.15 0.046 0.284 0.681 0.871 Severity, % During rearing – – – – – – – – Early gestation 39.1 31.2 21.5 7.76 16.40 0.185 0.439 0.792 Late gestation 24.4 54.3 25.0 16.7 21.26 0.364 0.956 0.630 Lactation 47.0 67.7 42.9 32.8 22.90 0.410 0.607 0.793 Overall 66.7 53.8 46.1 38.8 17.01 0.360 0.716 0.534 All severe cases, % 13.7 17.3 8.88 10.6 21.80 0.726 0.449 0.449 1 Control, basal diet and TM plus Met (MinMet), with additional 10, 20, and 50 mg/kg of chelated cooper, manganese, and zinc, respectively (0.1%; Aplomotec Plus, Tecnología & Vitaminas, S.L., Alforja, Spain) and increased Met:Lys ratio as 1.01. 2 Standard Lys provided 165 CP/kg with 10.0 g Lys/kg between 119 and 163 d of age and 140 g CP/kg with 8.0 g Lys/kg between 164 to 209 d of age; or low Lys, set first to 155 g CP/kg with 8.1 g Lys/kg and second phase to 140 g CP/kg with 6.5 g Lys/kg. 3 During the rearing phase, lameness was evaluated for 60 gilts per dietary treatment; for other measurements, it is indicated in the table. 4 Evaluated at service and at 28 d of gestation. 5 Evaluated at 109 d of gestation. 6 Evaluated at weaning. Figure 1. ADG according to different age phases for control (gray) or dietary supplemented1 (black) gilts, comparing between females that never showed lameness (n = 230) and gilts that eventually became lame (n = 19) during rearing. 1Control, basal diet and TM plus Met (MinMet), with additional 10, 20, and 50 mg/kg of chelated cooper, manganese, and zinc, respectively (0.1%, Aplomotec Plus, Tecnología & Vitaminas, S.L., Alforja, Spain), and increased Met:Lys ratio as 1.01. a,bDifferent superscripts differ significantly at P < 0.05 within 119 and 141 d ADG. e,fDifferent superscripts differ significantly at P < 0.05 within 141 and 163 d ADG. m,nDifferent superscripts differ significantly at P < 0.05 within 163 and 184 d ADG. x,yDifferent superscripts differ significantly at P < 0.05 within 184 and 209 d ADG. Translate basic science to industry innovation 724 Fabà et al. Figure 2. ADG according to the different age phases for gilts fed standard (gray) or low Lys1 (black), comparing between females that never showed lameness (n = 230) and gilts that eventually became lame (n = 19) during rearing. 1Standard (Std) Lys provided 165 CP/kg with 10.0 g Lys/ kg between 119 and 163 d of age and 140 g CP/kg with 8.0 g Lys/kg between 164 and 209 d of age; or low Lys, set first to 155 g CP/kg with 8.1 g Lys/ kg and second phase to 140 g CP/kg with 6.5 g Lys/kg. a,bDifferent superscripts differ significantly at P < 0.05 within 119 and 141 d ADG. e,fDifferent superscripts differ significantly at P < 0.05 within 141 and 163 d ADG. m,nDifferent superscripts differ significantly at P < 0.05 within 163 and 184 d ADG. x,yDifferent superscripts differ marginally at P < 0.10 within 184 and 209 d ADG. Table 4. Effects of organic TM plus Met and lowering Lys dietary treatments provided (90 d) to rearing gilts (from 58.0 ± 11.1 kg to 151 ± 14.1 kg of BW) on first parity performance Control1 TM plus Met1 P-value Standard Lys2 Low Lys2 Standard Lys2 Low Lys2 SEM MinMet Lys MinMet × Lys Gilts, n 59 58 56 57 Service BW, kg 181.3 180.3 184.4 179.1 2.66 0.721 0.228 0.430 BF, mm 15.6 15.8 15.9 15.0 0.47 0.700 0.537 0.188 Farrowing BF, mm 14.4 13.8 14.4 14.9 0.46 0.206 0.936 0.195 Rate, % 91.4 82.6 87.8 89.5 4.39 0.373 0.669 0.212 Total born, n 17.3 17.4 17.4 16.4 0.59 0.403 0.351 0.332 Liveborn, n 15.6xy 16.3x 16.2x 15.2y 0.58 0.627 0.740 0.091 Stillborn, % 9.3 7.03 5.18 7.68 1.62 0.264 0.933 0.125 Weaning BF, mm 12.5 11.7 12.1 12.8 0.42 0.370 0.984 0.091 Weaned, n 14.2 14.4 13.3 14.0 0.55 0.208 0.371 0.672 Days to estrus 6.60 5.92 6.84 8.75 1.54 0.660 0.294 0.401 x,y Values within a row with different superscripts trend at P < 0.10. 1 Control, basal diet and TM plus Met (MinMet), with additional 10, 20, and 50 mg/kg of chelated cooper, manganese, and zinc, respectively (0.1%, Aplomotec Plus, Tecnología & Vitaminas, S.L., Alforja, Spain) and increased Met:Lys ratio as 1.01. 2 Standard Lys provided 165 CP/kg with 10.0 g Lys/kg between 119 and 163 d of age and 140 g CP/kg with 8.0 g Lys/kg between 164 and 209 d of age; or low Lys, set first to 155 g CP/kg with 8.1 g Lys/kg and second phase to 140 g CP/kg with 6.5 g Lys/kg. prevalence and severity across dietary treatments, sows having a lower number of liveborn piglets productive phases, or overall (Table 3). (P = 0.091) than did control with low Lys and The results from first parity performance are mineral plus Met with standard Lys. A 17.5% presented in Table 4 and show no major carry- lameness rate at early gestation tended to increase over effects from dietary treatments provided the odds (1.12; CI = 1.251, 1.116; P = 0.060) during growth. Still, gilts fed TM plus Met with for reduced, total-born piglets (16.5 vs. 17.7) low Lys tended to be 16 d younger (SE = 3.63; and increased the odds (1.11; CI = 1.074, 1.00; P = 0.009) at first service than those fed TM plus P = 0.044) for reduced piglets born alive (14.8 Met with standard Lys. Additionally, the number vs. 16.0). Furthermore, an 11.4% lameness rate of liveborn piglets tended to show the same inter- from late gestation and 15.3% at weaning weakly action with gilts fed TM plus Met, with low Lys increased the odds (1.04; CI = 1.008, 1.077; Translate basic science to industry innovation Microminerals and Met with limited Lys 725 P = 0.015; and 1.03; CI = 1.001, 1.067; P = 0.040, and dewclaw) had a 23.3% prevalence. When com- respectively) for greater weaning-to-estrus inter- pared across dietary treatments, no differences were val days than nonlame females (13.1 vs. 6.17 and observed for any type of lesion. 11.1 vs. 6.21, respectively). The percentage of removals and removal reasons DISCUSSION during first parity are presented in Table 5. Thirty-one out of 230 females (13.5%) did not reach a second ges- In agreement with our expectations, the diets tation. Of these, 68.1% were sudden deaths, whereas with lower Lys reduced final BW (3.8%), but to a 19.4% were removed due to reproductive problems, lesser extent than that expected (10%). Conversely, 6.9% for lameness, and 5.6% for other reasons. Over neither this nor the supplement of TM plus Met the productive phases, 16.7% of those were in gesta- or both strategies together affected lameness prev- tion, 59.7% during lactation (all sudden deaths), and alence. The only effect aligned with our hypothesis 23.6% at weaning. Culling and mortality showed no might be a delay in lameness occurrence for the gilts evidence for differences across dietary treatments. supplemented with TM plus Met. However, removals due to reproductive reasons The lack of a clear ADG effect on lameness tended to be less frequent amongst gilts fed with a was, to some extent, not surprising since a positive low Lys strategy (6.25%) than control Lys (33.3%; relationship between ADG and lameness was not P = 0.083). Additionally, an interaction occurred with detected in our previous study (Fabà et al., 2018) gilts fed TM plus Met and low Lys, tending (P < 0.10) and because the relationship between ADG and OC to have the highest incidence of sudden-death remov- is somewhat inconsistent (Orth et al., 1999; Ytrehus als and total removals in lactation. et al., 2007; Olstad et al., 2015). Nevertheless, young females (113 to 141 d of age) that eventually Claw Health became lame had greater ADG than never-lame gilts under low Lys (Figure 2). This may suggest an Incidence of claw lesions among dietary treat- initial greater potential for growth associated with ments was evaluated for 87.8% of the females, lameness, although caution must be taken due to and results are presented in Table 6. Of all sows the low number of observations. Some research sup- evaluated, 52.4% had at least one claw lesion, ports restrictive growth via dietary strategies (i.e., whereas 24.8% of them had two lesions or more. low energy, low Lys, and/or feed restriction) with Heel lesions were the most common claw lesions a positive effect on reducing OC (Reiland, 1975; (27.0%, both overgrowth and heel cracks). This was Goedegebuure et al., 1980; Koning et al., 2014b) followed by lesions of asymmetry (16.1%), hoof and lameness (Quinn et al., 2015), whereas other wall cracks (10.9%), white line (7.83%), broken or studies do not support such effects (Grøndalen, missing dewclaws (4.78%), and long hoofs (3.49%). 1974; Nakano et al., 1984, Woodard et al., 1987, The grouped hoof lesions (wall cracks, white line, Carlson et al.,1988). Busch and Wachmann (2011) Table 5. Effects of organic TM plus Met lowering Lys dietary treatments provided (90 d) to rearing gilts (from 58.0 ± 11.1 kg to 151 kg ± 14.1 kg of body weight) on removal reasons during the first parity Control1 TM plus Met1 P-value Standard Lys2 Low Lys2 Standard Lys2 Low Lys2 SEM MinMet Lys MinMet × Lys Gilts culled, n 6 9 9 7 Removals, % 10.2 15.5 16.1 12.3 4.59 0.847 0.999 0.758 Sudden death, % 50.0 77.8 44.4 100 18.60 0.999 0.736 0.069 Reproductive, % 33.3 11.1 33.3 0.0 10.60 0.685 0.083 0.365 Lameness, % 16.7 11.1 0.0 0.0 10.62 0.226 0.990 0.554 Others, % 0.0 22.2 22.2 0.0 9.90 0.484 0.226 0.232 Phases Gestation, % 33.3 11.1 22.2 0.0 15.73 0.654 0.172 0.488 Lactation, % 50.0 44.4 44.4 100 19.26 0.285 0.285 0.074 Postweaning, % 16.7 44.4 33.3 0.0 17.60 0.433 0.999 0.219 1 Control, basal diet and TM plus Met (MinMet), with additional 10, 20, and 50 mg/kg of chelated cooper, manganese, and zinc, respectively (0.1%, Aplomotec Plus, Tecnología & Vitaminas, S.L., Alforja, Spain), and increased Met:Lys ratio as 1.01. 2 Standard Lys provided 165 CP/kg with 10.0 g Lys/kg between 119 and 163 d of age and 140 g CP/kg with 8.0 g Lys/kg between 164 and 209 d of age; or low Lys, set first to 155 g CP/kg with 8.1 g Lys/kg and second phase to 140 g CP/kg with 6.5 g Lys/kg. Translate basic science to industry innovation 726 Fabà et al. associated fast ADG with an increasing risk of OC, to 142 d of age and of 0.65%, 0.70%, and 0.76%, whilst others did not (Ytrehus et al., 2004a, 2004b; respectively, from 143 to 212 d of age. Hence, our Tóth et al., 2016), suggesting that other factors treatments provided similar Lys to their low Lys (i.e., genetics, age, or even location) are likely more and high Lys levels (Table 1). However, present important. For example, van Grevenhof et al. (2012) diets (with wheat, barley, corn, soybean meal, sun- observed an inconsistent association between ADG flower meal, and wheat byproducts) contained 2.3– and OC amongst joints. In their study, heavier gilts 2.4 Mcal/kg NE and were lower than the 2.5–2.9 had more lesions in the elbow, but lighter females Mcal/kg NE in high Lys diets (corn-soybean based) had more in femoropatellar joints. of Díaz et al. (2017). Higher Lys:energy ratio herein Inherited traits associate OC with fast growth might result in a relatively high feed and Lys intake (Grøndalen and Vangen, 1974; Jørgensen and than the previous study because a lower energy Andersen, 2000; Kadarmideen et al., 2004; density will increase feed intake (NRC, 2012; Li Aasmundstad et al., 2013), however, if the associa- and Patience, 2017). As calculated, gilts in standard tion between fast growth with OC is related to joint Lys consumed 25 g SID Lys/kg gain whereas low overload or simply a genetic correlation for the Lys consumed 19 g SID Lys/kg gain up to 163 d of pathology is less clear. Indeed, it was earlier noted age. According to Shelton et al. (2011), this would that physiological biomechanical forces would be be near or slightly below sufficiency and might have sufficient to affect the OC outcome (Ytrehus et al., been insufficient. This is especially noted as a lack 2007; Etterlin et al., 2014; Olstad et al., 2015); of Lys deficiency, and hence, lack of ADG reduc- meanwhile, the initial vascular disruption cause of tion between 163 and 209 d of age for the low Lys OC still needs to be elucidated (Olstad et al., 2015). treatment. This indicates that present genetics is not A great degree of reduction may be required to limited with 21 g Lys daily per kg of gain between lessen OC via weight load reduction, and, perhaps, 163 and 209 d of age but slightly limited with 19 g the present lowering was insufficient as low Lys only Lys daily intake per kg of gain between 119 and 163 reduced final BW by 3.8%. Quinn et al. (2015), via d. Altogether, high intake even with low Lys den- feed restriction, found that reducing final BW by sity in the diet, could explain the moderate but not 7.30% was associated with less lameness and OC. de severe reduction of BW and the lack of ADG dif- Koning et al. (2014b) found that gilts fed ad libitum ferences in the second feed phase. A greater degree between 4 and 26 wk of age (final BW 132 kg) had of limiting dietary Lys or ratio to energy would be higher odds of OC than did those fed ad libitum needed to properly test the hypothesis herein. from 4 to 10 wk and then restricted from 10 to 26 wk Interactions for BW at day 184 and loin depth (reduced 16% BW). These authors also reported that at days 163 and 184 occurred, as values were initially restricting (4–10 wk) followed by ad libitum greater for gilts fed control Lys and TM plus Met feeding (10–26 wk; reduced 3.0% BW) increased than for gilts fed control and low Lys. The impor- odds of OC when compared with initially feeding ad tance of such interactions is minor since differences libitum (4–10 wk) followed by restriction (10–26 wk; were small. The reason behind the interactions is reduced 16% BW) or restricted throughout (reduced unknown. High dietary Met could support catabo- 19% BW). Assuming that slower ADG can minimize lism for some amino acids if control with low Lys lameness, the ADG reduction in the present study is was deficient, but other deficiencies are not expected notable less than that in the previous studies where with the present diets. Otherwise, supportive prop- benefits were reported and may be insufficient. erties to the immune system attributed to Met, In agreement with previous works, lowered Lys or an antioxidant effect, may have enhanced gilt (Cia et al., 1998; Díaz et al., 2017) or Lys and CP growth under Lys deficiency (Brosnan et al., 2006; (Li et al., 2018) in the diet reduced growth and loin Li et al., 2007). In fact, despite extensive research, area and (or) depth. Nonetheless, these authors the impacts of additives and environmental condi- reported greater BW reductions (7% to 12%) than tions on amino acid requirements remain poorly that herein (3.80%). Indeed, the target was to defined in practical diets (NRC, 2012). reduce final BW by nearly 10%, which according Providing extra TM plus Met did not reduce to the above-mentioned literature is that reported lameness prevalence though its occurrence seemed with the potential to reduce lameness and lame- to be delayed. Furthermore, lame gilts in control ness risk factors (OC). In a similar study, although diets tended to have lower ADG than never-lame focused on puberty, Díaz et al. (2017) used differ- gilts by the end of rearing, whereas lame gilts fed ing total Lys concentrations (low, medium, or high) TM plus Met were intermediate, suggesting little of 0.81%, 0.90%, and 0.99%, respectively, from 100 or null intervention. These results contrast with Translate basic science to industry innovation Microminerals and Met with limited Lys 727 our previous study where identical supplementa- be confirmed, a lower severity of lameness in the tion of TM and Met, in combination or separately, present study may explain the lack of more con- reduced lameness. Likewise, in the subsample study, sistent effects. TM alone enhanced bone strength and density and, When entering into the sow herd, lameness combined with Met, improved the OC lesions score prevalence doubled in our studies. This highlights (Fabà et al., 2019). the high susceptibility of young females (Pluym Over the years, bone and joint development were et al., 2013). Lameness is important and was asso- studied to enhance bone health and reduce lame- ciated with lowered prolificacy and an increased ness; however, controversy is commonly reported weaning-to-estrus interval. It could be that the among intervening factors. Deficiencies in TM such increased stress-under-lameness condition in early as Zn, Cu, and Mn (Ott and Asquith, 1995; Shaw gestation impairs reproductive function. Similarly, et al., 2006; Veum et al., 2009) and amino acid Met Anil et al. (2009) reported reduced liveborn piglets (Huang et al., 2014), used herein, would negatively for lame sows. Furthermore, lameness may affect influence bone development. Conversely, the use sow mobility in lactation (Anil et al., 2009; Pluym of TM above requirements is noted as noneffective et al., 2013) and reduce feed intake, which would (Orth, 1999; Creech et al., 2004; Gowanlock et al., compromise the state of reserves at weaning and 2013; Tóth et al., 2016) or with limited benefits on the interval to estrus. Still, this cannot be confirmed bone metabolism (Liu et al., 2016) and bones and from the present data. Entering into the sow farm joint lesions (Frantz et al., 2008; Quinn et al., 2015; was a challenge associated to an increased lame- Fabà et al., 2019). Similarly, benefits have been doc- ness similarly for all dietary treatments. Therefore, umented with Met (Frantz et al., 2008; Ouattara our previous (Fabà et al., 2018) and present data et al., 2016). The present results and published suggest that dietary supplements do not act as a data maintain controversy and do not support carryover measure to reduce lameness and claw a clear benefit from TM supplement on growing problems. Different facilities, wider slat void, floor pigs’ lameness. Using similar TM and levels to this type, social conflicts from management (i.e., move- study (all above NRC, 2012), Tóth et al. (2016) eval- ments, animal flow, density, remixing), or train- uated inorganic sources with additional organic ing for the electronic feeding system were all new ones (150 + 50 g/kg Zn, 50 + 20 mg/kg Cu, and factors also known to increase lameness and claw 16.5 + 10 mg/kg Mn). Results showed no improve- lesions (Pluym et al., 2011; Li and Gonyou, 2013; ments in OC either early (12 wk) or later (24 wk) in Olsson et al., 2016). Still, if lameness prevalence the pigs’ life. Further, only few severe cases of OC (3 were to be reduced through TM during rearing, out of 200) were detected at 24 wk of age. To discuss this would enhance latter productivity (Fabà et al., such results and the difference between our present 2018). Data do not negate that TM supplements and former study, lameness severity may be key. In in sows may reduce lameness via improving claw fact, whereas in the previous study the control gilts horn properties as previously reported (Varagka had a lameness prevalence of 14.8%, in the present, et al., 2016); probably, a continued supplement may lameness prevalence in control gilts was 6.67%. provide a better approach. Otherwise, the change Lameness during the rearing period (7.92%) may be too severe a challenge to find a response. was similar to that in our previous study (7.75%; These data indicate that lameness should be first Fabà et al., 2018), although, herein it was not addressed through management and environment, associated with performance loss. Lame gilts in especially for young sows. our previous study had reduced ADG (90 g) and In conclusion, during the rearing phase and final BW (7.0 kg) compared with never-lame gilts. under the present conditions, the organic TM (Cu, Such effects on performance would indicate high Mn, and Zn) and Met supplements, or the standard severity (Weary et al., 2009; Munsterhjelm et al., and low Lys, or combined treatments did not affect 2015), while absence of performance differences prevalence of lameness. The absence of performance between lame and never-lame gilts in the present loss in lame gilts and low gait scores suggests low study suggests low severity. These differences were lameness severity during rearing, which may have unexpected because facilities, genetics, and the limited dietary treatment potential. Nonetheless, observer were the same as in our previous study. sow herd lameness was associated with increased A different breeder multiplier may partly explain odds for reduced liveborn piglets and an increased differences because OC is inheritable, and more weaning-to-estrus interval. The dietary treatments concentrated within populations (Aasmundstad during rearing did not improve sow lameness and et al., 2013; Le et al., 2016). Although it cannot claw health at first parity but prevalence increased Translate basic science to industry innovation 728 Fabà et al. dramatically, likely due to management and envi- confined housing on joint health in a herd of fattening pigs. ronmental factors. The present low Lys reduced BMC Vet. Res. 10:208. doi:10.1186/s12917-014-0208-5 Ewers, B. J., D. Dvoracek-Driksna, M. W. Orth, and growth to a lesser extent as compared with previous R. C. Haut. 2001. The extent of matrix damage and chon- studies that documented reduced OC and lameness drocyte death in mechanically traumatized articular carti- via feed restriction. A greater deficiency of Lys lage explants depends on rate of loading. J. Orthop. Res. than that herein would be needed to further test the 19:779–784. doi:10.1016/S0736-0266(01)00006-7 potential of the present hypothesis. Fabà, L., J. Gasa, M. D. Tokach, E. Varella, and D. Solà-Oriol. 2018. Effects of supplementing organic microminerals and methionine during the rearing phase of replacement gilts on lameness, growth, and body composition. J. Anim. LITERATURE CITED Sci. 96:3274–3287. doi:10.1093/jas/sky195 Aasmundstad, T., J. Kongsro, M. Wetten, N. I. Dolvik, and Fabà, L., J. Gasa, M. D. Tokach, M. Font-i-Furnols, O. Vangen. 2013. Osteochondrosis in pigs diagnosed with E. Vilarrasa, and D. Solà-Oriol. 2019. Effects of addi- computed tomography: heritabilities and genetic corre- tional organic microminerals and methionine on carcass lations to weight gain in specific age intervals. Animal composition, gait score, bone characteristics, and osteo- 7:1576–1582. doi:10.1017/S1751731113001158 chondrosis in replacement gilts of different growth rate. Anil, S. S., L. Anil, and J. Deen. 2009. Effect of lameness on Anim. Feed Sci. Technol. (in press). sow longevity. J. Am. Vet. Med. Assoc. 235:734–738. FEDNA. 2013. Necesidades nutricionales para Ganado por- doi:10.2460/javma.235.6.734 cino. 2th ed. Madrid (Spain): Fundación Española para el Brosnan, J. T., and M. E. Brosnan. 2006. The sulfur-containing Desarollo de la Nutrición Animal. amino acids: an overview. J. Nutr. 136(6 Suppl):1636S– Frantz, N. Z., G. A. Andrews, M. D. Tokach, J. L. Nelssen, R. D. 1640S. doi:10.1093/jn/136.6.1636S Goodband, J. M. Derouchey, and S. S. Dritz. 2008. Effect Busch, M. E., and H. Wachmann. 2011. Osteochondrosis of of dietary nutrients on osteochondrosis lesions and car- the elbow joint in finishing pigs from three herds: associa- tilage properties in pigs. Am. J. Vet. Res. 69:617–624. tions among different types of joint changes and between doi:10.2460/ajvr.69.5.617 osteochondrosis and growth rate. Vet. J. 188:197–203. Goedegebuure, S. A., H. J. Häni, P. C. van der Valk, and doi:10.1016/j.tvjl.2010.03.021 P. G. van der Wal. 1980. Osteochondrosis in six breeds of Carlson, C. S., H. D. Hilley, D. J. Meuten, J. M. Hagan, and slaughter pigs. Vet. Q. 2:28–41. doi:10.1080/01652176.19 R. L. Moser. 1988. Effect of reduced growth rate on the 80.9693755 prevalence and severity of osteochondrosis in gilts. Am. van Grevenhof, E. M., H. C. M. Heuven, P. R. van Weeren, J. Vet. Res. 49:396–402. and P. Bijma. 2012. The relationship between growth Celi, P., A.J. Cowieson, F. Fru-Nji, R.E. Steinert, A.M. Kluenter, and osteochondrosis in specific joints in pigs. Livest. Sci. and V. Verlhac. 2017. Gastrointestinal functionality in 143(1):85–90. doi:10.1016/j.livsci.2011.09.002 animal nutrition and health: new opportunities for sus- Grøndalen, T. 1974. Leg weakness in pigs. I. Incidence and tainable animal production. Anim. Feed Sci. Technol. relationship to skeletal lesions, feed level, protein and min- 234:88–100. doi:10.1016/j.anifeedsci.2017.09.012 eral supply, exercise and exterior conformation. Acta Vet Cia, M. C., S. A. Edwards, V. L. Glasgow, M. Shanks, and H. Scand.15:555–73. Fraser. 1998. Modification of body composition by alter- Grøndalen, T., and O. Vangen 1974. Osteochondrosis and ing the dietary lysine to energy ratio during rearing and arthrosis in pigs. V. A comparison of the incidence in three the effect on reproductive performance of gilts. Anim. Sci. different lines of the Norwegian Landrace breed. Acta Vet 66:457–463. Scand. 15:61–79. Creech, B. L., J. W. Spears, W. L. Flowers, G. M. Hill, K. E. Gowanlock, D. W., D. C. Mahan, J. S. Jolliff, S. J. Moeller, and Lloyd, T. A. Armstrong, and T. E. Engle. 2004. Effect of G. M. Hill. 2013. Evaluating the NRC levels of Cu, Fe, dietary trace mineral concentration and source (inorganic Mn, and Zn using organic and inorganic mineral sources vs. Chelated) on performance, mineral status, and fecal for grower-finisher swine. J. Anim. Sci. 91:5680–5686. mineral excretion in pigs from weaning through finishing. doi:10.2527/jas2013-6608 J. Anim. Sci. 82:2140–2147. doi:10.2527/2004.8272140x Heinonen, M., O. Peltoniemi, and A. Valros. 2013. Impact Deen, J., S. S. Anil, L. Anil, and S. Baidoo. 2008. Lameness of lameness and claw lesions in cows on health and overview and awareness: implications for welfare, hous- production. Livest. Sci. 156:64–70. doi:10.1016/j. ing, performance and economics. Asten/Sterksel (The livsci.2013.06.012 Netherlands): FeetFirstTM Symp. Sow Lameness. Huang, T. H., J. L. Lewis, H. S. Lin, L. T. Kuo, S. W. Mao, Y. S. Díaz, J. A. C., J. L. Vallet, R. D. Boyd, C. A. Lents, T. J. Tai, M. S. Chang, G. P. Ables, C. E. Perrone, and Prince, A. E. DeDecker, C. E. Phillips, G. Foxcroft, and R. S. Yang. 2014. A methionine-restricted diet and endur- K. J. Stalder. 2017. Effect of feeding three lysine to energy ance exercise decrease bone mass and extrinsic strength diets on growth, body composition and age at puberty but increase intrinsic strength in growing male rats. J. in replacement gilts. Anim. Reprod. Sci. 184:1–10. Nutr. 144:621–630. doi:10.3945/jn.113.187922 doi:10.1016/j.anireprosci.2017.06.007. Jensen, T. B., M. K. Bonde, A. G. Kongsted, N. Toft, and Engblom, L., L. Eliasson-Selling, N. Lundeheim, K. Belák, K. J. T. Sørensen. 2010. The interrelationships between clinical Andersson, and A. M. Dalin. 2008. Post mortem findings in signs and their effect on involuntary culling among preg- sows and gilts euthanised or found dead in a large swedish nant sows in group-housing systems. Animal 4:1922–1928. herd. Acta Vet. Scand. 50:25. doi:10.1186/1751-0147-50-25 doi:10.1017/S1751731110001102 Etterlin, P. E., B. Ytrehus, N. Lundeheim, E. Heldmer, J. Jørgensen, B., and S. Andersen. 2000. Genetic parameters for Österberg, and S. Ekman. 2014. Effects of free-range and osteochondrosis in Danish Landrace and Yorkshire boars Translate basic science to industry innovation Microminerals and Met with limited Lys 729 and correlations with leg weakness and production traits. Nakano T., F. X. Aherne, J. J. Brennan, and J. R. Thompson. Anim. Sci. 71:427–434. doi:10.1017/S1357729800055442 1984. Effect of growth rate on the incidence of osteochon- Kadarmideen, H. N., D. Schwörer, H. Ilahi, M. Malek, and drosis in growing swine. Can J. Anim. Sci. 64:139–146. A. Hofer. 2004. Genetics of osteochondral disease and its doi:10.4141/cjas84-017 relationship with meat quality and quantity, growth, and Niemi, J. K., P. Bergman, S. Ovaska, M. -L. Sevón-Aimonen, feed conversion traits in pigs. J. Anim. Sci. 82:3118–3127. and M. Heinonen. 2017. Modeling the costs of postpar- doi:10.2527/2004.82113118x tum dysgalactia syndrome and locomotory disorders on KilBride, A. L., C. E. Gillman, and L. E. Green. 2009. A cross sow productivity and replacement. Front. Vet. Sci. 4:1–12. sectional study of the prevalence, risk factors and popu- doi:10.3389/fvets.2017.00181. lation attributable fractions for limb and body lesions in NRC. 2012. Nutrient requirements of swine. 11th rev. ed. lactating sows on commercial farms in England. BMC Washington (DC): National Academies of Press. Vet. Res. 5:30. doi:10.1186/1746-6148-5-30 Olsson, A. C., J. Svendsen, J. Botermans, and C. Bergsten. de Koning, D. B., E. M. van Grevenhof, B. F. Laurenssen, P. R. 2016. An experimental model for studying claw lesions in van Weeren, W. Hazeleger, and B. Kemp. 2014a. The influ- growing female pigs. Livest. Sci. 184:58–63. doi:10.1016/j. ence of floor type before and after 10 weeks of age on oste- livsci.2015.12.005 ochondrosis in growing gilts. J. Anim. Sci. 92:3338–3347. Olstad, K., S. Ekman, and C. S. Carlson. 2015. An update doi:10.2527/jas.2014-7902 on the pathogenesis of osteochondrosis. Vet Pathol de Koning, D. B., E. M. van Grevenhof, B. F. Laurenssen, P. R. 52(5):785–802. doi:10.1177/0300985815588778 van Weeren, W. Hazeleger, and B. Kemp. 2014b. The influ- Orth, M. W. 1999. The regulation of growth plate car- ence of dietary restriction before and after 10 weeks of tilage turnover. J. Anim. Sci. 77(Suppl 2):183–189. age on osteochondrosis in growing gilts. J. Anim. Sci. doi:10.2527/1999.77suppl_2183x 91:5167–5176. doi:10.2527/jas.2013-6591 Ott, E. A., and R. L. Asquith. 1995. Trace mineral supple- de Koning, D. B., E. M. van Grevenhof, B. F. Laurenssen, W. mentation of yearling horses. J. Anim. Sci. 73:466–471. Hazeleger, and B. Kemp. 2015. Associations of conforma- doi:10.1016/S0737-0806(06)81884-8 tion and locomotive characteristics in growing gilts with Ouattara, A., D. Cooke, R. Gopalakrishnan, T. H. Huang, and osteochondrosis at slaughter. J. Anim. Sci. 93:93–106. G. P. Ables. 2016. Methionine restriction alters bone mor- doi:10.2527/jas.2014-8366 phology and affects osteoblast differentiation. Bone Rep. Le, T. H., P. Madsen, N. Lundeheim, K. Nilsson, and 5:33–42. doi:10.1016/j.bonr.2016.02.002 E. Norberg. 2016. Genetic association between leg confor- Pluym, L. M., S. Hoorebeke, A. Lopez, and R. Jeroen. 2011. mation in young pigs and sow longevity. J. Anim. Breed. Prevalence and risk factors of lameness and claw lesions Genet. 133:283–290. doi:10.1111/jbg.12193 in two types of group housing for pregnant sows. Vet. Li, Y. Z., and H. W. Gonyou. 2013. Comparison of manage- Med. 56:101–109. doi:10.17221/3159-VETMED. ment options for sows kept in pens with electronic feed- Pluym, L. M., A. Nuffel, S. Weyenberg, and D. Maes. 2013. ing stations. Can. J. Anim. Sci. 93:445–452. doi:10.4141/ Prevalence of lameness and claw lesions during different cjas2013-044 stages in the reproductive cycle of sows and the impact on Li, Y. H., F. N. Li, Y. H. Duan, Q. P. Guo, C. Y. Wen, reproduction results. Animal. 7:1174–1181. doi:10.1017/ W. L. Wang, X. G. Huang, Y. L. Yin. 2018. Low-protein S1751731113000232 diet improves meat quality of growing and finishing pigs Quinn, A. J., L. E. Green, P. G. Lawlor, and L. A. Boyle. 2015. through changing lipid metabolism, fiber characteristics, The effect of feeding a diet formulated for developing and free amino acid profile of the muscle. J. Anim. Sci. gilts between 70kg and ~140kg on lameness indicators 8:3221–3232. doi:10.1093/jas/sky116 and carcass traits. Livest. Sci. 174:87–95. doi:10.1016/j. Li, Q., and J. F. Patience. 2017. Factors involved in the regu- livsci.2014.12.016 lation of feed and energy intake of pigs. Anim. Feed Sci. Reiland, S. 1975. Osteochondrosis in the pig [PhD thesis]. Technol. 233:22–33. doi:10.1016/j.anifeedsci.2016.01.001 Stockholm (Sweden): The Royal Veterinary College. Li, P., Y. L. Yin, D. Li, S. W. Kim, and G. Wu. 2007. Amino van Riet, M. M. J., S. Millet, M. Aluwé, and G. P. J. Janssens. acids and immune function. Br. J. Nutr. 98:237–252. 2013. Impact of nutrition on lameness and claw doi:10.1017/S000711450769936X health in sows. Livest. Sci. 156:24–35. doi:10.1016/j. Liu, B., P. Xiong, N. Chen, J. He, G. Lin, Y. Xue, W. Li, and livsci.2013.06.005 D. Yu. 2016. Effects of replacing of inorganic trace miner- Shaw, D. T., D. W. Rozeboom, G. M. Hill, M. W. Orth, D. S. als by organically bound trace minerals on growth perfor- Rosenstein, and J. E. Link. 2006. Impact of supplement mance, tissue mineral status, and fecal mineral excretion withdrawal and wheat middling inclusion on bone metab- in commercial grower-finisher pigs. Biol. Trace Elem. Res. olism, bone strength, and the incidence of bone fractures 173:316–324. doi:10.1007/s12011-016-0658-7 occurring at slaughter in pigs. J. Anim. Sci. 84:1138–1146. Munsterhjelm, C., M. Heinonen, and A. Valros. 2015. Effects doi:10.2527/2006.8451138x of clinical lameness and tail biting lesions on voluntary Shelton, N. W., M. D. Tokach, S. S. Dritz, R. D. Goodband, feed intake in growing pigs. Livest. Sci. 181:210–219. J. L. Nelssen, and J. M. DeRouchey. 2011. Effects of doi:10.1016/j.livsci.2015.09.003 increasing dietary standardized ileal digestible lysine for Mustonen, K., E. Ala-Kurikka, T. Orro, O. Peltoniemi, M. gilts grown in a commercial finishing environment. J. Raekallio, O. Vainio, and M. Heinonen. 2011. Oral ketopro- Anim. Sci. 89:3587–3595. doi:10.2527/jas.2010–3030 fen is effective in the treatment of non-infectious lameness Tybirk, P. E. R. 2015. Nutrient recommendations for pigs in in sows. Vet. J. 190:55–59. doi:10.1016/j.tvjl.2010.09.017 Denmark. 17th ed. Copenhague (DK): SEGES-VSP Nakano, T., and F. X. Aherne. 1988. Involvement of trauma Danis Pig Res. Cent.. in the pathogenesis of osteochondritis dissecans in swine. Tóth, F., J. L. Torrison, L. Harper, D. Bussieres, M. E. Can. J. Vet. Res. 52:154–155. Wilson, T. D. Crenshaw, and C. S. Carlson. 2016. Translate basic science to industry innovation 730 Fabà et al. Osteochondrosis prevalence and severity at 12 and 24 Woodard, J. C., H. N. Becker, and P. W. Poulos, Jr. 1987. weeks of age in commercial pigs with and without organ- Effect of diet on longitudinal bone growth and oste- ic-complexed trace mineral supplementation. J. Anim. Sci. ochondrosis in swine. Vet. Pathol. 24:109–117. 94:3817–3825. doi:10.2527/jas.2015-9950 doi:10.1177/030098588702400202 Varagka, N., M. Lisgara, V. Skampardonis, V. Psychas, and Yazdi, M. H., N. Lundeheim, L. Rydhmer, E. Ringmar- L. Leontides. 2016. Partial substitution, with their che- Cederberg, and K. Johansson. 2000. Survival of Swedish lated complexes, of the inorganic zinc, copper and man- Landrace and Yorkshire sows in relation to osteochon- ganese in sow diets reduced the laminitic lesions in the drosis: a genetic study. Anim. Sci. 71:1–9. doi:10.1017/ claws and improved the morphometric characteristics of S1357729800054849 the hoof horn of sows from three greek herds. Porcine Ytrehus, B., C. S. Carlson, and S. Ekman. 2007. Etiology and Health Manag. 2:26. doi:10.1186/s40813-016-0040-3 pathogenesis of osteochondrosis. Vet. Pathol. 44:429–448. Veum, T. L., D. R. Ledoux, M. C. Shannon, and V. Raboy. doi:10.1354/vp.44-4-429 2009. Effect of graded levels of iron, zinc, and copper sup- Ytrehus, B., C. S. Carlson, N. Lundeheim, L. Mathisen, F. P. plementation in diets with low-phytate or normal barley Reinholt, J. Teige, and S. Ekman. 2004a. Vascularisation on growth performance, bone characteristics, hematocrit and osteochondrosis of the epiphyseal growth cartilage of volume, and zinc and copper balance of young swine. J. the distal femur in pigs–development with age, growth rate, Anim. Sci. 87:2625–2634. doi:10.2527/ jas.2008-1604 weight and joint shape. Bone. 34:454–465. doi:10.1016/j. Weary, D. M., J. M. Huzzey, and M. A. von Keyserlingk. bone.2003.07.011. 2009. Board-invited review: using behavior to predict and Ytrehus, B., E. Grindflek, J. Teige, E. Stubsjøen, T. identify ill health in animals. J. Anim. Sci. 87:770–777. Grøndalen, C. S. Carlson, and S. Ekman. 2004b. The doi:10.2527/jas.2008-1297 effect of parentage on the prevalence, severity and Welfare Qualitys. 2009. Welfare quality assessment protocol location of lesions of osteochondrosis in swine. J. for pigs (sows and piglets, growing and finishing pigs). Vet. Med. A. Physiol. Pathol. Clin. Med. 51:188–195. Lelystad (The Netherlands): Welfare Quality Consortium. doi:10.1111/j.1439-0442.2004.00621.x Translate basic science to industry innovation