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Maintaining continuity of nutrient intake after weaning. I. Review of pre-weaning strategies

Maintaining continuity of nutrient intake after weaning. I. Review of pre-weaning strategies Maintaining continuity of nutrient intake after weaning. I. Review of pre-weaning strategies †,1 † † † Madie R. Wensley , Mike D. Tokach , Jason C. Woodworth , Robert D. Goodband , ‡ † || Jordan T. Gebhardt , Joel M. DeRouchey , and Denny McKilligan Department of Animal Sciences and Industry, College of Agriculture, Manhattan, KS 66506-0201, USA; Department of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine Kansas State University, || Manhattan, KS 66506-0201, USA; and TechMix Inc., Stewart, MN 55385, USA ABSTRACT: Weaning is a crucial phase of swine Supplemental milk replacer has also been shown production marked by a multitude of biological to elicit a positive response in preweaning growth and environmental stressors, which have a signifi- performance, which may help to reduce pre- cant impact on immediate postweaning behavior weaning mortality. While socialization and milk and feed intake (FI). During this time, the pig- replacer are acknowledged to ease the weaning let’s gastrointestinal (GI) system is also under- transition, these strategies have not been widely going extensive epithelial, immune, and nervous adopted due to labor and application challenges. system development. In this review, our objective Additionally, the cost of milk replacer and logis- is to describe the different preweaning strategies tics of retrofitting farrowing houses to accommo- that can be used to minimize nutrient intake dis- date litter socialization have limited adaptation. ruption and improve FI in the immediate post- Further exploration of maternal nutrition strat- weaning period. Reducing nutrient disruption egies, particularly fetal imprinting, is needed to postweaning can be accomplished through the better understand the implications of perinatal implementation of management and nutritional learning. Other areas for future research include, strategies. Research consistently demonstrates combining environmental enrichment with feed- that weaning older, more developmentally mature ing strategies, such as large destructible pellets or pigs helps prevent many of the adverse GI effects play feeders, as well as determining at what time associated with weaning stress. Providing creep point producers should start socializing pigs be- feed to pigs during lactation is another reliable fore weaning. While more research is needed to strategy that has been shown to increase imme- develop strategic preweaning management pro- diate postweaning FI by acclimating pigs to solid grams, many of the strategies presented in this feed prior to weaning. Likewise, socialization by review provide opportunities for producers to allowing pigs to mix before weaning improves so- minimize nutrient intake disruption by prevent- cial skills, minimizing mixing stress, and aggres- ing feed neophobia, reducing stress, and easing sion-related injury immediately postweaning. the wean pig transition. Key words: feed intake, nutrient disruption, preweaning, pig © The Author(s) 2021. 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- NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial 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. 2021.5:1-12 doi: 10.1093/tas/txab021 Corresponding author: wensleym@ksu.edu Received November 20, 2020. Accepted February 2, 2021. 1 Wensley et al. INTRODUCTION on the sow to supply more nutrients, both in utero and during lactation, which has led to an increased Weaning is a stressful event in a pig’s life, marked proportion of light birth weight pigs (≤1 kg). Data by maternal and littermate separation, dietary and collected from 965 litters indicated that this pro- environmental changes, in addition to co-mingling portion increased from 7% to 23% of total pigs and social hierarchy establishment (Moeser et  al., born as litter size increased from ≤ 11 to ≥ 16 pigs, 2007a). In the wild, pigs are gradually weaned with 17% of light birth weight pigs dying within around 12 weeks of age, whereas pigs reared in the first 24 h after farrowing (Quiniou et al., 2002). modern U.S.  production systems are weaned be- In more recent years, Feldpausch et al. (2019) ob- tween 2.5 and 4 weeks of age (Moeser et al., 2017), served that 43% of total preweaning mortalities oc- an outcome determined by lactation space, pig curred amongst the light birth weight population. o fl w, and disease status. The period preweaning is In addition, Craig et al. (2017) observed that in gilt characterized by exogenous and endogenous fac- progeny, pigs were weaned and marketed at lighter tors that act to limit immune activation until 2.5–4 weights than sow progeny, with significantly in- weeks of age, at which time there is a reduction creased mortality rates. Differences in gilt progeny in maternal immunity and an increase in piglet birth weights and subsequent growth is attributed lymphocyte development and Peyer’s patches ma- to developmental delays associated with decreased turity (Moeser et  al., 2017). During this time, the organ weights, restricted colostrum digestion, piglet’s gastrointestinal (GI) system is also under- and lower serum IgG concentrations (Craig et al., going extensive epithelial, immune and nervous 2019). These data indicate an opportunity for pro- system development. This emphasizes the need for ducers to implement nutritional and management a sanitary environment to achieve long-term mat- programs prior to weaning to better prepare pigs uration of the immune system. However, this crit- for the changes in FI and growth rate postweaning. ical window of maturation is often interrupted by Therefore, the present review will focus on different the weaning transition, which can have detrimental preweaning strategies to minimize nutrient intake effects on gut health, nutrient utilization, and dis- disruption and improve FI in the immediate (7 d) ease resistance (Moeser et al., 2017). Furthermore, postweaning period. the combination of stressors that occur at weaning has a significant impact on immediate postweaning PREWEANING STRATEGIES TO INCREASE behavior and feed intake (FI; Pluske, 2016). FEED INTAKE AFTER WEANING It is well established that stress plays a pivotal role in intestinal barrier breakdown (Hart and Kamm, 2002; Kelly et  al., 2015). Exploration of Maternal Nutrition the gut-brain axis has revealed the impacts of stress on the biochemical signaling that occurs between Lucas et  al. (1991; derived from Davies and the GI tract and central nervous system (Hart and Norman, 2002) defined programming as the physio- Kamm, 2002), suggesting an interactive relation- logical “setting” by an early stimulus or insult at ship between the microbiome, intestinal barrier, a “sensitive” period, resulting in long-term con- and enteric nervous and mucosal immune systems sequences for function. Fetal programming is the (Yu et al., 2012; Kelly et al., 2015). Stress stimuli ac- foundation for fetal growth and development and is tivate the hypothalamic–pituitary–adrenal (HPA) influenced by maternal uterine conditions that are axis, the body’s central stress response mechanism. often categorized into nutritive and non-nutritive Activation of this pathway is characterized by in- factors (Johnston et al., 2008). These conditions in- creased corticotropin release factor (CRF) activity, clude uterine capacity, gestational stress from the mast cell (MC) degranulation, and increased gut environment, maternal under and over nutrition, permeability (Hart and Kamm, 2002). Continuous and placental nutrient transport. These conditions activation of this stress response system can have impact postnatal growth and development, HPA detrimental effects on the protective, metabolic, activity, intestinal morphology, and offspring life- structural, and immune functions of the gut co- time reproductive performance (Johnston et  al., inciding with persistent inflammation, decreased 2008; Ji et al., 2017). The final weeks leading to par - nutrient utilization, and poor growth performance turition are well documented as the most sensitive (Hart and Kamm, 2002; Yu et al., 2012). stage for fetal programming (Ji et al., 2017). In addition to weaning stressors, genetic se- Nutritional strategies to influence uterine lection for large litter sizes has increased demands conditions have been suggested throughout the Translate basic science to industry innovation Pre-weaning effects on postweaning intake literature. It is understood that vitamin and mineral gain of piglets in the immediate postweaning period nutrition, glucose transport, and growth hormone (Oostindjer et al., 2010; Blavi et al., 2016), and de- circulation play crucial roles in fetal growth and crease time to initial FI (Oostindjer et  al., 2011). development (Johnston et  al., 2008). Specifically, Interestingly, when given a choice between feed l -glutamine supplementation during gestation has with or without flavor after weaning, previous ex- demonstrated encouraging physiological and devel- posure did not affect flavor preference (Oostindjer opmental benefits, ameliorating intrauterine growth et al., 2010; Figueroa et al., 2013); however, flavor retardation in gilt progeny (Wu et  al., 2011) and learning did reduce aggressive tendencies following increasing the average birth weight of multiparous nursery placement (Fuentes et al., 2010; Oostindjer sow progeny (Zhu et al., 2018). Dietary glutamine et al., 2010, 2011). This suggests that flavor learning in lactating sow diets has also been shown to en- in pigs works through a reduction of weaning stress hance glutamine concentrations in milk, increasing rather than flavor preference, which may reduce piglet growth and survival (Wu et al., 2011). While feed neophobia at weaning. glutamine appears to have beneficial effects, limited While many of these strategies appear prom- research has prevented widespread adaptation. ising, few have gained industry-wide application as Glutamine is also not approved for feeding in all lo- a result of limited research. Additionally, the eco- cations globally. Furthermore, Zhang et  al. (2017) nomics of implementing these strategies on the farm reviewed the effects of branched-chain amino acid is not well understood. Therefore, further research (BCAA) supplementation in sow diets. Collectively, is needed in the area of sow nutrition to better the data demonstrate that BCAAs stimulate mam- understand its influence on fetal programming, as mary epithelial cell growth, increase the percentage to develop more practical approaches to improving of milk protein, and increases glutamine, glutamate, maternal uterine conditions and imprinting on sub- and aspartate concentrations in the milk. Among sequent offspring behavior and long-term growth all BCAA, leucine plays a vital role in mTOR performance. pathway activation, enhancing blastocyte devel- opment and embryo implantation, as well as fetal Management Strategies protein synthesis. Supplementing sow diets with BCAA remains promising, however, more research Cross fostering and split-suckling.  Cross- is needed in this area. Other interventions have re- fostering and split-suckling are management strat- ported that supplementing sow lactation diets with egies widely used throughout the swine industry as a fatty acids (FA) influence the transfer of n−3 and means to increase preweaning growth and survival. n−6 polyunsaturated fatty acids (PUFA) from the The process by which these strategies are carried sow milk to the piglet (Lauridsen, 2020). Uptake out varies widely across production systems (Baxter of these FA into the piglets enteric tissues may im- et al., 2013); however, there is a consensus that age, pact gut health and function, while also providing birth order, litter size, and body weight (BW) play immune system support. In a review by Rosero critical roles in the success of implementing these et al. (2016), supplemental FA also showed a con- strategies. sistent improvement in litter growth. Piglet survival Cross-fostering is the relocation of piglets from however was less consistent and was therefore not their biological mother to a foster sow in an at- reported. The authors concluded maximum sow re- tempt to equalize litter size and reduce mortality. It productive efficiency can be achieved by providing is well-recognized that fostering piglets is time-sen- a minimum dietary intake of 10 g/d of α-linolenic sitive. Ideally, fostering should take place 12–24  h acid and 125 g/d of linoleic acid. Additionally, many after birth which allows piglets sufficient colostrum studies evaluating the effects of PUFA in sow diets intake from their birth sow, while also preventing have shown improved intestinal glucose absorp- the disruption of teat hierarchy establishment tion, FA concentrations, and tissue glycogen stores (Heim et al., 2012; Baxter et al., 2013). When there in piglets (Jarocka-Cyrta et al., 1998; Gabler et al., is a risk that sows colostrum production will not 2007; Boudry et al., 2009). Perinatal flavor learning meet piglets needs (> 200 g), fostering should occur is another interesting concept. Research shows that earlier (Alexopoulos et al., 2018). Observations at young animals can learn flavors from the maternal the time of milk let down throughout lactation sug- diet that appear in the amniotic fluid and mother’s gest that the number of fights associated with suck- milk (Oostindjer et al., 2010). Prenatal exposure to ling tend to be lower in biologically related litters flavors in addition to flavors in the maternal diet compared to cross-fostered litters; however, this after birth have been shown to increase FI and BW does not impact the number of successful nursing Translate basic science to industry innovation Wensley et al. episodes and the subsequent growth and survival of opportunities for pigs to receive colostrum, which fostered pigs (Heim et al., 2012). Huting et al. (2017) should provide greater immunity and promote utilized light and heavy birth weight pigs and as- healthy growth (Alexopoulos et al., 2018). sessed the impact of mixed- verses uniform-weight Intermittent suckling and socialization.  litters through cross-fostering. Not surprisingly, Intermittent suckling (IS) is a strategy that lightweight piglets reared in uniform litters had is long-established but not commonly used heavier weaning weights and fewer removals than throughout the swine industry due to labor impli- those reared in mixed litters. Conversely, heavier cations. Intermittent suckling is a form of gradual birth weight piglets performed better and had weaning where piglets are removed from the sow fewer removals in mixed litters. Both of these re- for a period of time each day. This simulates the sponses are related to the piglet’s ability to compete progressive maternal separation that occurs dur- for a more productive anterior teat. These results ing natural weaning. Turpin et  al. (2016a,b; 2017) are in agreement with Deen and Bilkei (2004) who conducted three trials evaluating the effects of IS observed greater mortality in low birth weight pigs on postweaning behavior and performance. Litters reared with high birth weight littermates. More im- exposed to IS 7 d prior to weaning had decreased portantly, however, was the impact of litter size. preweaning mortality compared to conventionally Low birth weight pigs fostered into larger litters, weaned litters (Turpin et  al., 2016a). Interestingly, regardless of littermate BW, missed more nursing 3 d after weaning IS groups had a negative average episodes and had increased mortality compared daily gain (ADG) in contrast to conventionally to those fostered into smaller litters. Furthermore, weaned groups; however, gain recovered and sur- piglets fostered into older litters had significantly passed that of the conventionally weaned group by reduced suckling activity compared to piglets fos- d 7. Turpin et al. (2016b) also observed that com- tered into younger litters (Pajžlar and Skok, 2019). bining IS with a 35 d wean age improved the post- Taken together, small piglets should be fostered weaning adaptation period, evident by increased into litters of other small pigs (Alexopoulos et al., FI and ADG through d 12 postweaning. No dif- 2018). When this is not feasible, litter size should ference was observed when combining IS with a be reduced by the removal of larger pigs. There is 28 d wean age relative to the control group. Lastly, some data that suggest cross-fostering may also IS with comingling non-littermate piglets before impact long-term growth and survival; however, weaning, in combination with grouping familiar the results are inconsistent and seem to be more pigs together after weaning, improved performance closely related to piglet birth weight (Baxter et al., in an additive manner, resulting in increased FI and 2013; Huting et  al., 2017). When done correctly, decreased expression of manipulative behavior im- cross-fostering allows producers to equalize litter mediately postweaning (Turpin et  al., 2017). This size, which should reduce teat competition and give highlights the impact of familiarity on growth per- piglets more opportunity to consume milk. formance and the potential benefit of preweaning Limited research has been conducted to deter- socialization on social skill development. mine the best approach for split-suckling. Morton Hötzel et al. (2004) demonstrated that modern et  al. (2019) conducted a study evaluating two rearing systems have a significant impact on the split-suckling methods, temporarily removing ei- development of piglet behavior. Compared to pig- ther the heaviest six pigs in the litter or the first half lets reared in farrowing stalls, piglets reared in out- of the piglets born. It was concluded that while door systems exhibit less social interaction with the both birth weight and order are important for sow and fewer nursing episodes, which appears to preweaning growth and survival, the two interact encourage earlier solid feed consumption during differently. Birth weight was closely related to col- lactation and reduce manipulative social behav- ostrum intake, compared to birth order which was iors after weaning. Research conducted to mimic observed to affect immunocrit levels. Furthermore, outdoor rearing systems by removing the bar- Donovan and Dritz (2000) demonstrated that while rier between two adjacent farrowing pens and al- split-suckling decreased variation in ADG of pigs lowing pigs to mix has shown a similar response from birth to weaning, this response was only sig- in reducing agonistic behavior and lesion scores nificant for pigs in large litters (≥9 pigs). These stud- (North and Stewart, 2000; Hessel et  al., 2006). ies were conducted during the preweaning period, Other studies have found that mixing pigs dur- therefore the implications of split-suckling strategy ing lactation increases preweaning play behavior, on postweaning nutrient intake and performance reduces BW loss at weaning, and improves post- is unknown; however, split-suckling creates more weaning growth rates (North and Stewart, 2000; Translate basic science to industry innovation Pre-weaning effects on postweaning intake Hessel et  al., 2006; Salazar et  al., 2018). D’Eath to an Escherichia coli challenge, these immune re- (2005) also observed that socialized pigs were able sponses were suppressed and exacerbated intestinal to more quickly form stable dominance hierarchies injury was observed (McLamb et  al., 2013). This when faced with unfamiliar pigs compared to pre- suggests stress-induced MC activation is different viously unsocialized pigs. These data demonstrate than pathogenic, and that stress compromises gut the importance of socialization prior to weaning as integrity, altering innate immune responses to sub- a strategy to minimize mixing stress and better pre- sequent health challenges. Interestingly, the E. coli pare pigs for weaning. Despite these added bene- challenge reduced growth rates in pigs weaned at 16 fits, early mixing strategies have not been widely d, whereas growth was not affected in pigs weaned adopted in practical operations. The logistics and at 20 d of age; however, feed intake was similar be- cost of retrofitting farrowing houses to accommo- tween wean age groups. This data further demon- date litter socialization, in addition to the potential strates the importance of weaning an older, more disease spread when comingling litters have pre- biologically mature pig. vented application. However, as interest in this area Further research investigating early weaning increases, more research is needed to fully under- and its impact on gut integrity revealed that pigs stand the effects of early mixing on postweaning FI weaned at 15 d of age developed chronic, relapsing and growth performance. diarrhea, with a more severe clinical response ob- Wean age.  Emerging evidence indicates that served in females (Pohl et  al., 2017). Others have early life adversities lead to the early onset and shown that these clinical (Medland et  al., 2016) greater severity of intestinal disorders (Gresse and pathophysiological (Smith et  al., 2010) re- et al., 2017; Pohl et al., 2017). In humans, early-life sponses can persist into later life, which supports stressors have been linked to irritable bowel syn- the observations by Main et  al. (2004) where they drome and depression (Kelly et al., 2015). Moeser reported improved wean-to-finish performance as et  al. (2007a) evaluated the effects of weaning wean age increased from 12 to 21 d of age. Despite age-induced stress on intestinal dysfunction in there being no difference in lifetime performance pigs 24 h postweaning. Compared to age-matched, when analyzed on a common age, Faccin et  al. unweaned littermates, pigs weaned at 19 d of age (2020) observed that as wean age increased up to exhibited increased serum and peripheral CRF, a 25 d, belly nosing behavior, immediate postweaning stress peptide hormone that is released in response body weight loss, and nursery removal rates were to HPA axis stimuli. This neuroendocrine survival reduced. As a result, BW sold per pig weaned in- mechanism is responsible for bringing the body creased with weaning age, which is in support of back to homeostasis after a stress event (Moeser the Main et al. (2004) study. et  al., 2017). Additionally, HPA helps to regu- The immediate postweaning impacts of wean late many body processes, including digestion and age have also been studied. van der Meulen et  al. the immune system, thus playing a central role in (2010) observed that increasing wean age from 4 gut health. This response was supported by using to 7 wk of age improved postweaning FI and gain chamber analysis of jejunal tissue, which showed immediately after weaning. Furthermore, Pluske reduced tight junction integrity, increased intestinal et al. (2003) reported GI underdevelopment in permeability, and net ion transport, all of which pigs weaned at either 2  wk of age or lighter body suggest the role of CRF in intestinal permeability. weight, regardless of age. Underdevelopment was In a follow-up trial, Moeser et al. (2007b) evaluated marked by lighter GI organs and accessory organ the effects of stress in delayed weaning. Compared weights, as well as lower specific maltase, glucoam- to pigs weaned at d 19, pigs weaned at d 28 exhib- ylose, and pancreatic enzyme activity. Similarly, ited decreased CRF-recpetor1 expression, an indi- when pigs were divided into young (<32.4 wean cator of CRF concentrations. Furthermore, pigs age) versus old (>35.9 wean age) groups at a weaned at d 28 displayed decreased tryptase activity, common wean date, higher mortality rates were ob- a marker of MC activation. Tryptase, along with served in young (9.1%) compared to old pigs (5.0%; pro-inflammatory compounds (serotonin/5-hydrox- Huting et  al., 2019). However, when divided into ytryptamine and histamine) are released from MC light verses heavy groups, no statistical differences in response to immune stimuli. Under normal con- were detected. Huting et  al. (2019) also observed ditions, these mediators are designed to increase in- that increasing wean age and feeding allowance in testinal secretion and inflammation to rid the body the nursery benefited light weaned pigs compared of invading pathogens (Yu et  al., 2012). However, to heavy weaned pigs. Regardless of BW though, when pigs weaned at 16 d of age were subjected Main et  al. (2004) reported that feeding program Translate basic science to industry innovation Wensley et al. complexity in the nursery phase did not impact weaning stress (Xiang et  al., 2020). Furthermore, wean-to-finish performance. the transfer of feces from a healthy donor to a dis- These data suggest that weaning older, more de- eased recipient may offer the opportunity to alter velopmentally mature pigs helps prevent many of the GI microbiota and reduce morbidity and mor- the clinical, pathophysiological, and economic con- tality in health challenge herds (Niederwerder et al., sequences associated with stress. 2018). While this strategy appears to have more relevance in human health, it does provide insight on specific bacteria or probiotics that may be used Nutrient Intake to create a more symbiotic microflora environment Topsoil.  Aside from a more natural weaning in the pig. Nevertheless, more research is needed to process, outdoor rearing systems offer more phys- understand the interaction between the gut micro- ical and social environmental interactions for biota and the development of immune cells (Xiang young pigs (Lau et al., 2015). Specifically, early ex- et al., 2020). posure to topsoil during lactation has been shown Creep feeding.  Offering creep feed prewean- to accelerate gut microbiota maturation in wean- ing is believed to ease the weaning transition by ling pigs (Vo et  al., 2017). In modern indoor sys- improving feed intake in the immediate postwean- tems, piglets do not have access to topsoil, therefore ing period. At first introduction, familiarization reducing their microbial load exposure. This may of solid feed is an exploratory behavior; however, be associated with immune deficiencies and poorer as pigs begin to mature, creep feed consumption lifetime health. is largely driven by nutrient demand (Pajor et  al., Exposure to topsoil 4 d postfarrow until weaning 1991). It has also been suggested that piglets with resulted in lower weaning weights compared to lit- insufficient milk intake or those with low BW will ters that were not exposed to topsoil (Tsai et  al., compensate by increasing solid feed consumption 2016). However, during the nursery period, pigs (Pajor et al., 1991; Fraser et al., 1994; Huting et al., provided topsoil during lactation had increased 2017). Recent data by Middelkoop et al. (2019) are FI and ADG. Subsequent FI during the grow-fin- in agreement, demonstrating that piglets reared on ish period was also increased with a tendency for a restrict-fed sows and provided creep feed had in- 4.6  kg heavier market weight. Furthermore, when creased creep FI and percentage of eaters at weaning challenged with lipopolysaccharide on d 56, pigs compared to piglets reared on full-fed sows. English provided topsoil preweaning had an improved im- et  al. (1980; derived from Pluske et  al., 2018) sug- mune response, represented by increased plasma gest that piglets should consume, on average, 600 g IL1α concentration (Tsai et  al., 2016). Vo et  al. of creep feed before weaning to better prepare them (2017) demonstrated that this response can be at- for solid feed. Consequently, Pluske et al. (2018) in- tributed to abundant Prevotella and short-chain dicated that the level of creep feed intake needed to fatty acid-producing taxa when pigs are exposed completely alleviate the postweaning growth check to soil early in life. Furthermore, because the soil is not achievable considering wean age less than contains plant-derived carbohydrates and fibers it 28 days. Several others have reported relatively low is also believed that early transfer of these com- creep FI up until the last week prior to weaning at pounds in the colon can prepare the piglet GI tract 28 d of age (Pajor et al., 1991; Fraser et al., 1994; for solid food, preventing reductions in postwean- Bruininx et  al., 2002), with FI having minimal ef- ing FI and BW gain (Vo et  al., 2017). Similar to fects on preweaning BW gain. These studies have outdoor rearing, these data suggest that exposure also determined that creep feed consumption on of naïve pigs to the soil during lactation may help an individual pig and within litter basis is highly to develop a more functional immune response, variable. which may provide subsequent health and perform- While quantity and variability in total creep ance benefits. More research however is needed to consumption are important considerations, the better understand the microbial implications of true value of creep feeding is found in the devel- topsoil exposure on the piglet GI tract. Likewise, opment of eaters, pigs that actually consume creep fecal microbiota transplantation (FMT) has gained feed. Bruininx et al. (2002) observed that pigs des- attention in regulating gut microbial colonization. ignated as eaters had improved FI and ADG in Exogenous FMT has been shown to improve the the immediate postweaning period compared to growth performance, intestinal barrier function, non-eaters. Furthermore, eaters required less time and innate immune system of piglets (Hu et  al., from weaning to the initial consumption of dry 2018), so as to potentially alleviate the damage of feed. This was evident by the number of visits to the Translate basic science to industry innovation Pre-weaning effects on postweaning intake feeder during which feed consumption was higher impact BW at weaning, the authors did observe for eaters than non-eaters. The authors suggest that pigs who had received more complex diets dur- that familiarity with solid feed at weaning may be ing lactation continued to eat more postweaning the result of pigs focusing more on FI and less on and exhibited reduced BW loss immediately after exploratory behavior of the pen. In an attempt to weaning. Furthermore, pigs fed high complexity understand the impact of feeding duration on the creep feed had improved growth performance in proportion of eaters, Sulabo et al. (2010b) reported the postweaning period (Fraser et  al., 1994; Pajor 10% more pigs designated as eaters when increas- et al., 2002; Yan et al., 2011) compared with those ing the duration in which creep feed was offered that had received a simple creep feed diet. Cabrera from 6 to 13 d. Likewise, creep feeder design plays et al. (2013) noted that pigs who received glutamine an important role in maximizing the proportion supplementation in creep feed and throughout a of eaters, as well as managing creep feed wastage. 6-week nursery phase tended to have improved FG. Sulabo et al. (2010a) observed that although feeder This response was also observed in pigs that re- type did not impact preweaning BW, piglets that re- ceived either no creep or a controlling creep feed in ceived creep from a rotary feeder with hopper had the preweaning period and were later weaned onto reduced feed disappearance and increased number a glutamine supplemented diet. Intestinal histology of eaters than those provided creep in a pan feeder measures concluded that glutamine supplemented or rotary feeder without hopper. Moreover, the pigs had increased villous height and cell prolifer- number of times feeders were filled compared to ation, similar to pigs who were weaned at a later a rotary feeder with no hopper and pan feeder was age. Research evaluating flavored creep feed has reduced to once every 12  h. This indicates that demonstrated that adding flavor has no influence workers getting piglets up while filling feeders did on total creep intake or the proportion of eaters not encourage pigs to consume more feed. Play (Sulabo et al., 2008); however, pigs exposed to fla- feeders, or conventional rotary feeders with canvas vored creep feed tended to have improved FI im- cloth, braided cotton ropes, and PVC spiral tubes mediately postweaning and increased gain when attached on the inside bottom of the feeder, have fed complex starter diets supplemented with the also been shown to elicit exploratory behavior, at- same flavor. tracting more pigs to creep feed (Middelkoop et al., Several factors should be considered when 2019). This response followed pigs through the im- implementing a creep feeding program, including mediate postweaning period where increased FI the duration of feeding, feeder design, pellet size, and growth were observed. The authors suggested and diet complexity. It is expected that pigs may lose that providing creep feed in play feeders prior to weight immediately postweaning; however, these weaning may develop a positive association be- data indicate that the growth check associated with tween solid feed and object play, stimulating greater weaning can be reduced by acclimating pigs to feed feed consumption. In contrast, research has shown during the suckling period. Providing creep feed to that the pellet size in the suckling period has no nursing pigs weaned at older ages (> approximately effect on the number of pigs designated as eaters. 25 days) may also have the opportunity to improve However, van den Brand et al. (2014) observed that weaning weights (Tokach et  al., 2020). Taken col- feeding large pellets during lactation increased FI lectively, providing creep feed for 2−3 days prior to and BW gain after weaning. The authors attributed weaning is often satisfactory to observe the benefits this response to greater pellet consumption in early in postweaning performance (Tokach et al., 2020). lactation. Additionally, feeding a large pellet diam- Water consumption and liquid milk replacer.  eter has been reported to reduce preweaning mor- Water access and intake of piglets in the first days tality (Clark et al., 2015). after farrowing is often assumed to be of little Research has also looked at increasing the diet relevance. Fraser et  al. (1988) speculated that pig- complexity of creep feed to offer additional growth lets who are not receiving enough milk from the performance benefits. Results in the preweaning sow may be at risk of dehydration. In agreement, period indicate that increasing the diet complexity the authors observed that litters of pigs with low (Fraser et  al., 1994) or energy density (Yan et  al., growth during the first 4 d after farrowing used 2011) of creep feed has little effect on BW gain more water than faster gaining litters. This suggests prior to weaning. Conversely, Pajor et al. (2002) re- that pigs may correct for low milk intake by com- ported that pigs offered a complex diet consumed pensating with increased water intake (Fraser et al., 50% more solid feed before weaning compared 1988). Other trials looking at water dispenser de- to pigs provided a simple diet. While this did not sign have demonstrated that when water is visible in Translate basic science to industry innovation Wensley et al. either an open bowl or cup, compared to a nipple or help improve weaning weights, decrease prewean- push-lever dispenser, discovery time is significantly ing mortality, and increase FI postweaning. reduced (Phillips and Fraser, 1991). Furthermore, bite nipples can be modified to reduce discovery Gaps in Knowledge time by adding either a chain to the valve lever or oor fl -mounting the nipple at an upward angle so Reducing nutrient disruption postweaning can that it’s eye level with the pig (Phillips and Fraser, be accomplished through further exploration of 2001). This data provides insight into dispenser sys- multiple preweaning strategies that may be best tems that may be more advantageous to provide implemented in combination to prevent feed neo- nutrition supplements, such as milk replacer, to phobia, reduce stress, and improve the weaning preweaned pigs. transition. Areas where further research would be van Oostrum et al. (2016) evaluated the effects particularly beneficial include: of supplementing milk replacer before or after • Maternal nutrition: Gestation and lactation feed- weaning. The authors observed that pigs provided ing programs to influence piglet growth and de- milk replacer preweaning had improved FI during velopment (colostrum supply, BCAA, glutam- the first week postweaning compared to those sup- ine, and essential fatty acid concentrations). plemented with milk replacer after weaning. During • Fetal imprinting: Gestation and lactation feeding the preweaning period, several studies have reported programs designed to reduce stress in the imme- that pigs supplemented with milk replacer were diate postweaning period by providing pigs with heavier at weaning (Novotni-Dankó et  al., 2015; familiar olfactory stimuli. de Greeff et al., 2016), with a more pronounced re- • Sow management: When sow management tri- sponse observed in heavy birth weight pigs (Wolter als (i.e., split suckling, cross-fostering, etc.) are et  al., 2002). Furthermore, pigs that received milk conducted, often piglets are not followed down- replacer from birth to weaning had significantly stream into the nursery. Research instead focuses reduced preweaning mortality (Novotni-Dankó primarily on weaning weight. The question then et al., 2015). Nutrient-dense complex milk replacer becomes, does improving weaning weight, trans- has also elicited increased concentrations of meta- late to improved postweaning performance? bolic fermentation products and expression of • Socialization: In socialization studies, pigs are cell proliferation in the crypts along the piglet GI often not regrouped at weaning with pigs they tract, which may explain the performance response had previously been socialized with before wean- (de Greeff et  al., 2016). Alternatively, research in ing. This suggests an opportunity to assess the the last decade has demonstrated that bovine col- effects of postweaning placement strategies in ostrum may be a beneficial substitute for milk re- combination with preweaning socialization on placer because of its high immunoglobulin levels latency to feed and potentially BW loss after (de Lange et al., 2010). Piglets supplemented with weaning. At what time point should we start bovine colostrum had reduced E. coli colonization mixing pigs before weaning? in the intestine, similar to the colonization seen in • Environmental enrichment: Combining enrich- suckling litters (Sugiharto et  al., 2015). Likewise, ment with feeding strategies, such as large, de- the ileal microbiota population of pigs offered bo- structible pellets or play feeders on feed con- vine colostrum more closely resembled sow-reared sumption after weaning. piglets compared to those that received milk re- • Creep feeding: Providing lactation feed on far- placer (Poulsen et  al., 2017). Despite these bene- rowing stall mats prior to weaning as a strategy fits, milk replacer is not widely used throughout to familiarize pigs with solid feed. the industry due to increased labor and hygiene • Topsoil or other bacteria source: Influence of bac- challenges. Additionally, the added cost of milk re- teria exposure on the gut microbial population, placer has prevented further application. piglet performance, and health. While current data on water supplementation for suckling pigs is limited, previous research has demonstrated the importance of preventing dehy- CONCLUSION dration in piglets. This is particularly important as litter size increases and sows milk yield remains rela- Weaning is an important phase of swine pro- tively constant. These data also demonstrate that duction marked by some of the most profound providing milk replacer to pigs prior to weaning stressors. It is during this time period that pigs ex- offers an additional source of nutrients that may hibit low voluntary FI, much of which stems from Translate basic science to industry innovation Pre-weaning effects on postweaning intake Baxter, E. M., K. M. D. Rutherfored, R. B. D’Eath, G. Arnott, their physiological response to stress and the be- S.  P.  Turner, P.  Sandøe, V.A.  Moustsen, F.  Thorup, havioral mechanisms that follow, therefore prevent S.  A.  Edwards, and A.  B.  Lawrence. 2013. The wel- weanling pigs from searching out and consuming fare implications of large litter size in the domestic feed. Several factors are known to influence nu- pig II: management factors. Anim. Welf. 22:2019–238. trient intake after weaning including: doi:10.7120/09627286.22.2.219 Blavi,  L., D.  Solà-Oriol, J.  J.  Mallo, and J.  F.  Pérez. 2016. • Wean age: Weaning older, more developmentally Anethol, cinnamaldehyde, and eugenol inclusion in feed mature pigs helps prevent many of the adverse affects postweaning performance and feeding behavior effects of weaning associated stressors. of piglets. J. Anim. Sci. 94:5262–5271. doi:10.2527/ jas.2016-0760 • Cross-fostering and split-suckling: While there is Boudry, G., V . Douard, J. Mourot, J. P. Lallès, and I. Le Huërou- limited research on the effects of these manage- Luron. 2009. Linseed oil in the maternal diet during ges- ment strategies immediately after weaning, it is tation and lactation modifies fatty acid composition, understood that providing greater opportunities mucosal architecture, and mast cell regulation of the ileal for pigs to nurse prior to weaning should im- barrier in piglets. J. Nutr. 139:1110–1117. doi:10.3945/ jn.108.102640 prove nutrient intake and weaning BW, creating van  den  Brand,  H., D.  Wamsteeker, M.  Oostindjer, a more robust pig for the postweaning period. L. C. M. van Enckevort, A. F. B. van der Poel, B. Kemp, • Socialization: Allowing pigs to mix prior to and J.  E.  Bolhuis. 2014. Effects of pellet diameter dur- weaning improves social skills and encourages ing and after lactation on feed intake of piglets pre- and play behavior, minimizing mixing stress and in- postweaning. J. Anim. Sci. 92:4145–4153. doi: 10.2527/ jury from aggression immediately postweaning. jas2014-7408 Bruininx, E. M. A. M., G. P. Binnendijk, C. M. C. van der Peet- • Creep feeding: Providing creep feed to pigs dur- Schwering, J.  W.  Schrama, L.  A.  den  Hartog, H.  Everts, ing lactation encourages exploratory behavior and A. C. Beynen. 2002. Effect of creep feed consumption and familiarizes pigs with solid feed before wean- on individual feed intake characteristics and perfroamcne ing, increasing immediate postweaning FI. of group-housed weanling pigs. J. Anim. Sci. 80:1413– ◦ Water supplementation in combination with 1418. doi:10.2527/2002.8061413x Cabrera,  R.  A., J.  L.  Usry, C.  Arrellano, E.  T.  Nogueira, creep feed may help pigs learn the difference M. Kutschenko, A. J. Moeser, and J. Odle. 2013. Effects of between hunger and thirst prior to weaning. creep feeding and supplemental glutamine or glutamine • Milk supplementation: Provides an additional plus glutamate (Aminogut) on pre- and post-weaning source of nutrients that may help to reduce pre- growth performance and intestinal health of piglets. J. weaning mortality, particularly in the lightweight Anim. Sci. Biotechnol. 4:29. doi:10.1186/2049-1891-4-29 pig population. 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Pathophysiol. 3:27–43. doi: 10.4291/wjgp. promise selected measures of piglet welfare and stress. v3.i1.27 Animals. 6:24. doi:10.3390/ani6030024 Zhang, S., X. Zeng, M. Ren, X. Mao, and S. Qiao. 2017. Novel Turpin, D. L., P. Langendijk, T. Chen, D. Lines, and J. R. Pluske. metabolic and physiological functions of branched chain 2016b. Intermittent suckling in combination with an older amino acids: a review. J. Anim. Sci. Biotechnol. 8:10. weaning age improves growth, feed intake and aspects doi:10.1186/s40104-016-0139-z of gastrointestinal tract carbohydrate absorption in pigs Zhu, Y., T. Li, S. Huang, W. Wang, Z. Dai, C. Feng, G. Wu, and after weaning. Animals. 6:66. doi:10.3390/ani6110066 J.  Wang. 2018. Maternal l -glutamine supplementation Turpin,  D.  L., P.  Langendijk, K.  Plush, and J.  R.  Pluske. during late gestation alleviates intrauterine growth restric- 2017. Intermittent suckling with or without co-mingling tion-induced intestinal dysfunction in piglets. Amino of non-littermate piglets before weaning improves piglet Acids 50:1289–1299. doi:10.1007/s00726-018-2608-5 Translate basic science to industry innovation http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Translational Animal Science Oxford University Press

Maintaining continuity of nutrient intake after weaning. I. Review of pre-weaning strategies

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Maintaining continuity of nutrient intake after weaning. I. Review of pre-weaning strategies †,1 † † † Madie R. Wensley , Mike D. Tokach , Jason C. Woodworth , Robert D. Goodband , ‡ † || Jordan T. Gebhardt , Joel M. DeRouchey , and Denny McKilligan Department of Animal Sciences and Industry, College of Agriculture, Manhattan, KS 66506-0201, USA; Department of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine Kansas State University, || Manhattan, KS 66506-0201, USA; and TechMix Inc., Stewart, MN 55385, USA ABSTRACT: Weaning is a crucial phase of swine Supplemental milk replacer has also been shown production marked by a multitude of biological to elicit a positive response in preweaning growth and environmental stressors, which have a signifi- performance, which may help to reduce pre- cant impact on immediate postweaning behavior weaning mortality. While socialization and milk and feed intake (FI). During this time, the pig- replacer are acknowledged to ease the weaning let’s gastrointestinal (GI) system is also under- transition, these strategies have not been widely going extensive epithelial, immune, and nervous adopted due to labor and application challenges. system development. In this review, our objective Additionally, the cost of milk replacer and logis- is to describe the different preweaning strategies tics of retrofitting farrowing houses to accommo- that can be used to minimize nutrient intake dis- date litter socialization have limited adaptation. ruption and improve FI in the immediate post- Further exploration of maternal nutrition strat- weaning period. Reducing nutrient disruption egies, particularly fetal imprinting, is needed to postweaning can be accomplished through the better understand the implications of perinatal implementation of management and nutritional learning. Other areas for future research include, strategies. Research consistently demonstrates combining environmental enrichment with feed- that weaning older, more developmentally mature ing strategies, such as large destructible pellets or pigs helps prevent many of the adverse GI effects play feeders, as well as determining at what time associated with weaning stress. Providing creep point producers should start socializing pigs be- feed to pigs during lactation is another reliable fore weaning. While more research is needed to strategy that has been shown to increase imme- develop strategic preweaning management pro- diate postweaning FI by acclimating pigs to solid grams, many of the strategies presented in this feed prior to weaning. Likewise, socialization by review provide opportunities for producers to allowing pigs to mix before weaning improves so- minimize nutrient intake disruption by prevent- cial skills, minimizing mixing stress, and aggres- ing feed neophobia, reducing stress, and easing sion-related injury immediately postweaning. the wean pig transition. Key words: feed intake, nutrient disruption, preweaning, pig © The Author(s) 2021. 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- NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial 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. 2021.5:1-12 doi: 10.1093/tas/txab021 Corresponding author: wensleym@ksu.edu Received November 20, 2020. Accepted February 2, 2021. 1 Wensley et al. INTRODUCTION on the sow to supply more nutrients, both in utero and during lactation, which has led to an increased Weaning is a stressful event in a pig’s life, marked proportion of light birth weight pigs (≤1 kg). Data by maternal and littermate separation, dietary and collected from 965 litters indicated that this pro- environmental changes, in addition to co-mingling portion increased from 7% to 23% of total pigs and social hierarchy establishment (Moeser et  al., born as litter size increased from ≤ 11 to ≥ 16 pigs, 2007a). In the wild, pigs are gradually weaned with 17% of light birth weight pigs dying within around 12 weeks of age, whereas pigs reared in the first 24 h after farrowing (Quiniou et al., 2002). modern U.S.  production systems are weaned be- In more recent years, Feldpausch et al. (2019) ob- tween 2.5 and 4 weeks of age (Moeser et al., 2017), served that 43% of total preweaning mortalities oc- an outcome determined by lactation space, pig curred amongst the light birth weight population. o fl w, and disease status. The period preweaning is In addition, Craig et al. (2017) observed that in gilt characterized by exogenous and endogenous fac- progeny, pigs were weaned and marketed at lighter tors that act to limit immune activation until 2.5–4 weights than sow progeny, with significantly in- weeks of age, at which time there is a reduction creased mortality rates. Differences in gilt progeny in maternal immunity and an increase in piglet birth weights and subsequent growth is attributed lymphocyte development and Peyer’s patches ma- to developmental delays associated with decreased turity (Moeser et  al., 2017). During this time, the organ weights, restricted colostrum digestion, piglet’s gastrointestinal (GI) system is also under- and lower serum IgG concentrations (Craig et al., going extensive epithelial, immune and nervous 2019). These data indicate an opportunity for pro- system development. This emphasizes the need for ducers to implement nutritional and management a sanitary environment to achieve long-term mat- programs prior to weaning to better prepare pigs uration of the immune system. However, this crit- for the changes in FI and growth rate postweaning. ical window of maturation is often interrupted by Therefore, the present review will focus on different the weaning transition, which can have detrimental preweaning strategies to minimize nutrient intake effects on gut health, nutrient utilization, and dis- disruption and improve FI in the immediate (7 d) ease resistance (Moeser et al., 2017). Furthermore, postweaning period. the combination of stressors that occur at weaning has a significant impact on immediate postweaning PREWEANING STRATEGIES TO INCREASE behavior and feed intake (FI; Pluske, 2016). FEED INTAKE AFTER WEANING It is well established that stress plays a pivotal role in intestinal barrier breakdown (Hart and Kamm, 2002; Kelly et  al., 2015). Exploration of Maternal Nutrition the gut-brain axis has revealed the impacts of stress on the biochemical signaling that occurs between Lucas et  al. (1991; derived from Davies and the GI tract and central nervous system (Hart and Norman, 2002) defined programming as the physio- Kamm, 2002), suggesting an interactive relation- logical “setting” by an early stimulus or insult at ship between the microbiome, intestinal barrier, a “sensitive” period, resulting in long-term con- and enteric nervous and mucosal immune systems sequences for function. Fetal programming is the (Yu et al., 2012; Kelly et al., 2015). Stress stimuli ac- foundation for fetal growth and development and is tivate the hypothalamic–pituitary–adrenal (HPA) influenced by maternal uterine conditions that are axis, the body’s central stress response mechanism. often categorized into nutritive and non-nutritive Activation of this pathway is characterized by in- factors (Johnston et al., 2008). These conditions in- creased corticotropin release factor (CRF) activity, clude uterine capacity, gestational stress from the mast cell (MC) degranulation, and increased gut environment, maternal under and over nutrition, permeability (Hart and Kamm, 2002). Continuous and placental nutrient transport. These conditions activation of this stress response system can have impact postnatal growth and development, HPA detrimental effects on the protective, metabolic, activity, intestinal morphology, and offspring life- structural, and immune functions of the gut co- time reproductive performance (Johnston et  al., inciding with persistent inflammation, decreased 2008; Ji et al., 2017). The final weeks leading to par - nutrient utilization, and poor growth performance turition are well documented as the most sensitive (Hart and Kamm, 2002; Yu et al., 2012). stage for fetal programming (Ji et al., 2017). In addition to weaning stressors, genetic se- Nutritional strategies to influence uterine lection for large litter sizes has increased demands conditions have been suggested throughout the Translate basic science to industry innovation Pre-weaning effects on postweaning intake literature. It is understood that vitamin and mineral gain of piglets in the immediate postweaning period nutrition, glucose transport, and growth hormone (Oostindjer et al., 2010; Blavi et al., 2016), and de- circulation play crucial roles in fetal growth and crease time to initial FI (Oostindjer et  al., 2011). development (Johnston et  al., 2008). Specifically, Interestingly, when given a choice between feed l -glutamine supplementation during gestation has with or without flavor after weaning, previous ex- demonstrated encouraging physiological and devel- posure did not affect flavor preference (Oostindjer opmental benefits, ameliorating intrauterine growth et al., 2010; Figueroa et al., 2013); however, flavor retardation in gilt progeny (Wu et  al., 2011) and learning did reduce aggressive tendencies following increasing the average birth weight of multiparous nursery placement (Fuentes et al., 2010; Oostindjer sow progeny (Zhu et al., 2018). Dietary glutamine et al., 2010, 2011). This suggests that flavor learning in lactating sow diets has also been shown to en- in pigs works through a reduction of weaning stress hance glutamine concentrations in milk, increasing rather than flavor preference, which may reduce piglet growth and survival (Wu et al., 2011). While feed neophobia at weaning. glutamine appears to have beneficial effects, limited While many of these strategies appear prom- research has prevented widespread adaptation. ising, few have gained industry-wide application as Glutamine is also not approved for feeding in all lo- a result of limited research. Additionally, the eco- cations globally. Furthermore, Zhang et  al. (2017) nomics of implementing these strategies on the farm reviewed the effects of branched-chain amino acid is not well understood. Therefore, further research (BCAA) supplementation in sow diets. Collectively, is needed in the area of sow nutrition to better the data demonstrate that BCAAs stimulate mam- understand its influence on fetal programming, as mary epithelial cell growth, increase the percentage to develop more practical approaches to improving of milk protein, and increases glutamine, glutamate, maternal uterine conditions and imprinting on sub- and aspartate concentrations in the milk. Among sequent offspring behavior and long-term growth all BCAA, leucine plays a vital role in mTOR performance. pathway activation, enhancing blastocyte devel- opment and embryo implantation, as well as fetal Management Strategies protein synthesis. Supplementing sow diets with BCAA remains promising, however, more research Cross fostering and split-suckling.  Cross- is needed in this area. Other interventions have re- fostering and split-suckling are management strat- ported that supplementing sow lactation diets with egies widely used throughout the swine industry as a fatty acids (FA) influence the transfer of n−3 and means to increase preweaning growth and survival. n−6 polyunsaturated fatty acids (PUFA) from the The process by which these strategies are carried sow milk to the piglet (Lauridsen, 2020). Uptake out varies widely across production systems (Baxter of these FA into the piglets enteric tissues may im- et al., 2013); however, there is a consensus that age, pact gut health and function, while also providing birth order, litter size, and body weight (BW) play immune system support. In a review by Rosero critical roles in the success of implementing these et al. (2016), supplemental FA also showed a con- strategies. sistent improvement in litter growth. Piglet survival Cross-fostering is the relocation of piglets from however was less consistent and was therefore not their biological mother to a foster sow in an at- reported. The authors concluded maximum sow re- tempt to equalize litter size and reduce mortality. It productive efficiency can be achieved by providing is well-recognized that fostering piglets is time-sen- a minimum dietary intake of 10 g/d of α-linolenic sitive. Ideally, fostering should take place 12–24  h acid and 125 g/d of linoleic acid. Additionally, many after birth which allows piglets sufficient colostrum studies evaluating the effects of PUFA in sow diets intake from their birth sow, while also preventing have shown improved intestinal glucose absorp- the disruption of teat hierarchy establishment tion, FA concentrations, and tissue glycogen stores (Heim et al., 2012; Baxter et al., 2013). When there in piglets (Jarocka-Cyrta et al., 1998; Gabler et al., is a risk that sows colostrum production will not 2007; Boudry et al., 2009). Perinatal flavor learning meet piglets needs (> 200 g), fostering should occur is another interesting concept. Research shows that earlier (Alexopoulos et al., 2018). Observations at young animals can learn flavors from the maternal the time of milk let down throughout lactation sug- diet that appear in the amniotic fluid and mother’s gest that the number of fights associated with suck- milk (Oostindjer et al., 2010). Prenatal exposure to ling tend to be lower in biologically related litters flavors in addition to flavors in the maternal diet compared to cross-fostered litters; however, this after birth have been shown to increase FI and BW does not impact the number of successful nursing Translate basic science to industry innovation Wensley et al. episodes and the subsequent growth and survival of opportunities for pigs to receive colostrum, which fostered pigs (Heim et al., 2012). Huting et al. (2017) should provide greater immunity and promote utilized light and heavy birth weight pigs and as- healthy growth (Alexopoulos et al., 2018). sessed the impact of mixed- verses uniform-weight Intermittent suckling and socialization.  litters through cross-fostering. Not surprisingly, Intermittent suckling (IS) is a strategy that lightweight piglets reared in uniform litters had is long-established but not commonly used heavier weaning weights and fewer removals than throughout the swine industry due to labor impli- those reared in mixed litters. Conversely, heavier cations. Intermittent suckling is a form of gradual birth weight piglets performed better and had weaning where piglets are removed from the sow fewer removals in mixed litters. Both of these re- for a period of time each day. This simulates the sponses are related to the piglet’s ability to compete progressive maternal separation that occurs dur- for a more productive anterior teat. These results ing natural weaning. Turpin et  al. (2016a,b; 2017) are in agreement with Deen and Bilkei (2004) who conducted three trials evaluating the effects of IS observed greater mortality in low birth weight pigs on postweaning behavior and performance. Litters reared with high birth weight littermates. More im- exposed to IS 7 d prior to weaning had decreased portantly, however, was the impact of litter size. preweaning mortality compared to conventionally Low birth weight pigs fostered into larger litters, weaned litters (Turpin et  al., 2016a). Interestingly, regardless of littermate BW, missed more nursing 3 d after weaning IS groups had a negative average episodes and had increased mortality compared daily gain (ADG) in contrast to conventionally to those fostered into smaller litters. Furthermore, weaned groups; however, gain recovered and sur- piglets fostered into older litters had significantly passed that of the conventionally weaned group by reduced suckling activity compared to piglets fos- d 7. Turpin et al. (2016b) also observed that com- tered into younger litters (Pajžlar and Skok, 2019). bining IS with a 35 d wean age improved the post- Taken together, small piglets should be fostered weaning adaptation period, evident by increased into litters of other small pigs (Alexopoulos et al., FI and ADG through d 12 postweaning. No dif- 2018). When this is not feasible, litter size should ference was observed when combining IS with a be reduced by the removal of larger pigs. There is 28 d wean age relative to the control group. Lastly, some data that suggest cross-fostering may also IS with comingling non-littermate piglets before impact long-term growth and survival; however, weaning, in combination with grouping familiar the results are inconsistent and seem to be more pigs together after weaning, improved performance closely related to piglet birth weight (Baxter et al., in an additive manner, resulting in increased FI and 2013; Huting et  al., 2017). When done correctly, decreased expression of manipulative behavior im- cross-fostering allows producers to equalize litter mediately postweaning (Turpin et  al., 2017). This size, which should reduce teat competition and give highlights the impact of familiarity on growth per- piglets more opportunity to consume milk. formance and the potential benefit of preweaning Limited research has been conducted to deter- socialization on social skill development. mine the best approach for split-suckling. Morton Hötzel et al. (2004) demonstrated that modern et  al. (2019) conducted a study evaluating two rearing systems have a significant impact on the split-suckling methods, temporarily removing ei- development of piglet behavior. Compared to pig- ther the heaviest six pigs in the litter or the first half lets reared in farrowing stalls, piglets reared in out- of the piglets born. It was concluded that while door systems exhibit less social interaction with the both birth weight and order are important for sow and fewer nursing episodes, which appears to preweaning growth and survival, the two interact encourage earlier solid feed consumption during differently. Birth weight was closely related to col- lactation and reduce manipulative social behav- ostrum intake, compared to birth order which was iors after weaning. Research conducted to mimic observed to affect immunocrit levels. Furthermore, outdoor rearing systems by removing the bar- Donovan and Dritz (2000) demonstrated that while rier between two adjacent farrowing pens and al- split-suckling decreased variation in ADG of pigs lowing pigs to mix has shown a similar response from birth to weaning, this response was only sig- in reducing agonistic behavior and lesion scores nificant for pigs in large litters (≥9 pigs). These stud- (North and Stewart, 2000; Hessel et  al., 2006). ies were conducted during the preweaning period, Other studies have found that mixing pigs dur- therefore the implications of split-suckling strategy ing lactation increases preweaning play behavior, on postweaning nutrient intake and performance reduces BW loss at weaning, and improves post- is unknown; however, split-suckling creates more weaning growth rates (North and Stewart, 2000; Translate basic science to industry innovation Pre-weaning effects on postweaning intake Hessel et  al., 2006; Salazar et  al., 2018). D’Eath to an Escherichia coli challenge, these immune re- (2005) also observed that socialized pigs were able sponses were suppressed and exacerbated intestinal to more quickly form stable dominance hierarchies injury was observed (McLamb et  al., 2013). This when faced with unfamiliar pigs compared to pre- suggests stress-induced MC activation is different viously unsocialized pigs. These data demonstrate than pathogenic, and that stress compromises gut the importance of socialization prior to weaning as integrity, altering innate immune responses to sub- a strategy to minimize mixing stress and better pre- sequent health challenges. Interestingly, the E. coli pare pigs for weaning. Despite these added bene- challenge reduced growth rates in pigs weaned at 16 fits, early mixing strategies have not been widely d, whereas growth was not affected in pigs weaned adopted in practical operations. The logistics and at 20 d of age; however, feed intake was similar be- cost of retrofitting farrowing houses to accommo- tween wean age groups. This data further demon- date litter socialization, in addition to the potential strates the importance of weaning an older, more disease spread when comingling litters have pre- biologically mature pig. vented application. However, as interest in this area Further research investigating early weaning increases, more research is needed to fully under- and its impact on gut integrity revealed that pigs stand the effects of early mixing on postweaning FI weaned at 15 d of age developed chronic, relapsing and growth performance. diarrhea, with a more severe clinical response ob- Wean age.  Emerging evidence indicates that served in females (Pohl et  al., 2017). Others have early life adversities lead to the early onset and shown that these clinical (Medland et  al., 2016) greater severity of intestinal disorders (Gresse and pathophysiological (Smith et  al., 2010) re- et al., 2017; Pohl et al., 2017). In humans, early-life sponses can persist into later life, which supports stressors have been linked to irritable bowel syn- the observations by Main et  al. (2004) where they drome and depression (Kelly et al., 2015). Moeser reported improved wean-to-finish performance as et  al. (2007a) evaluated the effects of weaning wean age increased from 12 to 21 d of age. Despite age-induced stress on intestinal dysfunction in there being no difference in lifetime performance pigs 24 h postweaning. Compared to age-matched, when analyzed on a common age, Faccin et  al. unweaned littermates, pigs weaned at 19 d of age (2020) observed that as wean age increased up to exhibited increased serum and peripheral CRF, a 25 d, belly nosing behavior, immediate postweaning stress peptide hormone that is released in response body weight loss, and nursery removal rates were to HPA axis stimuli. This neuroendocrine survival reduced. As a result, BW sold per pig weaned in- mechanism is responsible for bringing the body creased with weaning age, which is in support of back to homeostasis after a stress event (Moeser the Main et al. (2004) study. et  al., 2017). Additionally, HPA helps to regu- The immediate postweaning impacts of wean late many body processes, including digestion and age have also been studied. van der Meulen et  al. the immune system, thus playing a central role in (2010) observed that increasing wean age from 4 gut health. This response was supported by using to 7 wk of age improved postweaning FI and gain chamber analysis of jejunal tissue, which showed immediately after weaning. Furthermore, Pluske reduced tight junction integrity, increased intestinal et al. (2003) reported GI underdevelopment in permeability, and net ion transport, all of which pigs weaned at either 2  wk of age or lighter body suggest the role of CRF in intestinal permeability. weight, regardless of age. Underdevelopment was In a follow-up trial, Moeser et al. (2007b) evaluated marked by lighter GI organs and accessory organ the effects of stress in delayed weaning. Compared weights, as well as lower specific maltase, glucoam- to pigs weaned at d 19, pigs weaned at d 28 exhib- ylose, and pancreatic enzyme activity. Similarly, ited decreased CRF-recpetor1 expression, an indi- when pigs were divided into young (<32.4 wean cator of CRF concentrations. Furthermore, pigs age) versus old (>35.9 wean age) groups at a weaned at d 28 displayed decreased tryptase activity, common wean date, higher mortality rates were ob- a marker of MC activation. Tryptase, along with served in young (9.1%) compared to old pigs (5.0%; pro-inflammatory compounds (serotonin/5-hydrox- Huting et  al., 2019). However, when divided into ytryptamine and histamine) are released from MC light verses heavy groups, no statistical differences in response to immune stimuli. Under normal con- were detected. Huting et  al. (2019) also observed ditions, these mediators are designed to increase in- that increasing wean age and feeding allowance in testinal secretion and inflammation to rid the body the nursery benefited light weaned pigs compared of invading pathogens (Yu et  al., 2012). However, to heavy weaned pigs. Regardless of BW though, when pigs weaned at 16 d of age were subjected Main et  al. (2004) reported that feeding program Translate basic science to industry innovation Wensley et al. complexity in the nursery phase did not impact weaning stress (Xiang et  al., 2020). Furthermore, wean-to-finish performance. the transfer of feces from a healthy donor to a dis- These data suggest that weaning older, more de- eased recipient may offer the opportunity to alter velopmentally mature pigs helps prevent many of the GI microbiota and reduce morbidity and mor- the clinical, pathophysiological, and economic con- tality in health challenge herds (Niederwerder et al., sequences associated with stress. 2018). While this strategy appears to have more relevance in human health, it does provide insight on specific bacteria or probiotics that may be used Nutrient Intake to create a more symbiotic microflora environment Topsoil.  Aside from a more natural weaning in the pig. Nevertheless, more research is needed to process, outdoor rearing systems offer more phys- understand the interaction between the gut micro- ical and social environmental interactions for biota and the development of immune cells (Xiang young pigs (Lau et al., 2015). Specifically, early ex- et al., 2020). posure to topsoil during lactation has been shown Creep feeding.  Offering creep feed prewean- to accelerate gut microbiota maturation in wean- ing is believed to ease the weaning transition by ling pigs (Vo et  al., 2017). In modern indoor sys- improving feed intake in the immediate postwean- tems, piglets do not have access to topsoil, therefore ing period. At first introduction, familiarization reducing their microbial load exposure. This may of solid feed is an exploratory behavior; however, be associated with immune deficiencies and poorer as pigs begin to mature, creep feed consumption lifetime health. is largely driven by nutrient demand (Pajor et  al., Exposure to topsoil 4 d postfarrow until weaning 1991). It has also been suggested that piglets with resulted in lower weaning weights compared to lit- insufficient milk intake or those with low BW will ters that were not exposed to topsoil (Tsai et  al., compensate by increasing solid feed consumption 2016). However, during the nursery period, pigs (Pajor et al., 1991; Fraser et al., 1994; Huting et al., provided topsoil during lactation had increased 2017). Recent data by Middelkoop et al. (2019) are FI and ADG. Subsequent FI during the grow-fin- in agreement, demonstrating that piglets reared on ish period was also increased with a tendency for a restrict-fed sows and provided creep feed had in- 4.6  kg heavier market weight. Furthermore, when creased creep FI and percentage of eaters at weaning challenged with lipopolysaccharide on d 56, pigs compared to piglets reared on full-fed sows. English provided topsoil preweaning had an improved im- et  al. (1980; derived from Pluske et  al., 2018) sug- mune response, represented by increased plasma gest that piglets should consume, on average, 600 g IL1α concentration (Tsai et  al., 2016). Vo et  al. of creep feed before weaning to better prepare them (2017) demonstrated that this response can be at- for solid feed. Consequently, Pluske et al. (2018) in- tributed to abundant Prevotella and short-chain dicated that the level of creep feed intake needed to fatty acid-producing taxa when pigs are exposed completely alleviate the postweaning growth check to soil early in life. Furthermore, because the soil is not achievable considering wean age less than contains plant-derived carbohydrates and fibers it 28 days. Several others have reported relatively low is also believed that early transfer of these com- creep FI up until the last week prior to weaning at pounds in the colon can prepare the piglet GI tract 28 d of age (Pajor et al., 1991; Fraser et al., 1994; for solid food, preventing reductions in postwean- Bruininx et  al., 2002), with FI having minimal ef- ing FI and BW gain (Vo et  al., 2017). Similar to fects on preweaning BW gain. These studies have outdoor rearing, these data suggest that exposure also determined that creep feed consumption on of naïve pigs to the soil during lactation may help an individual pig and within litter basis is highly to develop a more functional immune response, variable. which may provide subsequent health and perform- While quantity and variability in total creep ance benefits. More research however is needed to consumption are important considerations, the better understand the microbial implications of true value of creep feeding is found in the devel- topsoil exposure on the piglet GI tract. Likewise, opment of eaters, pigs that actually consume creep fecal microbiota transplantation (FMT) has gained feed. Bruininx et al. (2002) observed that pigs des- attention in regulating gut microbial colonization. ignated as eaters had improved FI and ADG in Exogenous FMT has been shown to improve the the immediate postweaning period compared to growth performance, intestinal barrier function, non-eaters. Furthermore, eaters required less time and innate immune system of piglets (Hu et  al., from weaning to the initial consumption of dry 2018), so as to potentially alleviate the damage of feed. This was evident by the number of visits to the Translate basic science to industry innovation Pre-weaning effects on postweaning intake feeder during which feed consumption was higher impact BW at weaning, the authors did observe for eaters than non-eaters. The authors suggest that pigs who had received more complex diets dur- that familiarity with solid feed at weaning may be ing lactation continued to eat more postweaning the result of pigs focusing more on FI and less on and exhibited reduced BW loss immediately after exploratory behavior of the pen. In an attempt to weaning. Furthermore, pigs fed high complexity understand the impact of feeding duration on the creep feed had improved growth performance in proportion of eaters, Sulabo et al. (2010b) reported the postweaning period (Fraser et  al., 1994; Pajor 10% more pigs designated as eaters when increas- et al., 2002; Yan et al., 2011) compared with those ing the duration in which creep feed was offered that had received a simple creep feed diet. Cabrera from 6 to 13 d. Likewise, creep feeder design plays et al. (2013) noted that pigs who received glutamine an important role in maximizing the proportion supplementation in creep feed and throughout a of eaters, as well as managing creep feed wastage. 6-week nursery phase tended to have improved FG. Sulabo et al. (2010a) observed that although feeder This response was also observed in pigs that re- type did not impact preweaning BW, piglets that re- ceived either no creep or a controlling creep feed in ceived creep from a rotary feeder with hopper had the preweaning period and were later weaned onto reduced feed disappearance and increased number a glutamine supplemented diet. Intestinal histology of eaters than those provided creep in a pan feeder measures concluded that glutamine supplemented or rotary feeder without hopper. Moreover, the pigs had increased villous height and cell prolifer- number of times feeders were filled compared to ation, similar to pigs who were weaned at a later a rotary feeder with no hopper and pan feeder was age. Research evaluating flavored creep feed has reduced to once every 12  h. This indicates that demonstrated that adding flavor has no influence workers getting piglets up while filling feeders did on total creep intake or the proportion of eaters not encourage pigs to consume more feed. Play (Sulabo et al., 2008); however, pigs exposed to fla- feeders, or conventional rotary feeders with canvas vored creep feed tended to have improved FI im- cloth, braided cotton ropes, and PVC spiral tubes mediately postweaning and increased gain when attached on the inside bottom of the feeder, have fed complex starter diets supplemented with the also been shown to elicit exploratory behavior, at- same flavor. tracting more pigs to creep feed (Middelkoop et al., Several factors should be considered when 2019). This response followed pigs through the im- implementing a creep feeding program, including mediate postweaning period where increased FI the duration of feeding, feeder design, pellet size, and growth were observed. The authors suggested and diet complexity. It is expected that pigs may lose that providing creep feed in play feeders prior to weight immediately postweaning; however, these weaning may develop a positive association be- data indicate that the growth check associated with tween solid feed and object play, stimulating greater weaning can be reduced by acclimating pigs to feed feed consumption. In contrast, research has shown during the suckling period. Providing creep feed to that the pellet size in the suckling period has no nursing pigs weaned at older ages (> approximately effect on the number of pigs designated as eaters. 25 days) may also have the opportunity to improve However, van den Brand et al. (2014) observed that weaning weights (Tokach et  al., 2020). Taken col- feeding large pellets during lactation increased FI lectively, providing creep feed for 2−3 days prior to and BW gain after weaning. The authors attributed weaning is often satisfactory to observe the benefits this response to greater pellet consumption in early in postweaning performance (Tokach et al., 2020). lactation. Additionally, feeding a large pellet diam- Water consumption and liquid milk replacer.  eter has been reported to reduce preweaning mor- Water access and intake of piglets in the first days tality (Clark et al., 2015). after farrowing is often assumed to be of little Research has also looked at increasing the diet relevance. Fraser et  al. (1988) speculated that pig- complexity of creep feed to offer additional growth lets who are not receiving enough milk from the performance benefits. Results in the preweaning sow may be at risk of dehydration. In agreement, period indicate that increasing the diet complexity the authors observed that litters of pigs with low (Fraser et  al., 1994) or energy density (Yan et  al., growth during the first 4 d after farrowing used 2011) of creep feed has little effect on BW gain more water than faster gaining litters. This suggests prior to weaning. Conversely, Pajor et al. (2002) re- that pigs may correct for low milk intake by com- ported that pigs offered a complex diet consumed pensating with increased water intake (Fraser et al., 50% more solid feed before weaning compared 1988). Other trials looking at water dispenser de- to pigs provided a simple diet. While this did not sign have demonstrated that when water is visible in Translate basic science to industry innovation Wensley et al. either an open bowl or cup, compared to a nipple or help improve weaning weights, decrease prewean- push-lever dispenser, discovery time is significantly ing mortality, and increase FI postweaning. reduced (Phillips and Fraser, 1991). Furthermore, bite nipples can be modified to reduce discovery Gaps in Knowledge time by adding either a chain to the valve lever or oor fl -mounting the nipple at an upward angle so Reducing nutrient disruption postweaning can that it’s eye level with the pig (Phillips and Fraser, be accomplished through further exploration of 2001). This data provides insight into dispenser sys- multiple preweaning strategies that may be best tems that may be more advantageous to provide implemented in combination to prevent feed neo- nutrition supplements, such as milk replacer, to phobia, reduce stress, and improve the weaning preweaned pigs. transition. Areas where further research would be van Oostrum et al. (2016) evaluated the effects particularly beneficial include: of supplementing milk replacer before or after • Maternal nutrition: Gestation and lactation feed- weaning. The authors observed that pigs provided ing programs to influence piglet growth and de- milk replacer preweaning had improved FI during velopment (colostrum supply, BCAA, glutam- the first week postweaning compared to those sup- ine, and essential fatty acid concentrations). plemented with milk replacer after weaning. During • Fetal imprinting: Gestation and lactation feeding the preweaning period, several studies have reported programs designed to reduce stress in the imme- that pigs supplemented with milk replacer were diate postweaning period by providing pigs with heavier at weaning (Novotni-Dankó et  al., 2015; familiar olfactory stimuli. de Greeff et al., 2016), with a more pronounced re- • Sow management: When sow management tri- sponse observed in heavy birth weight pigs (Wolter als (i.e., split suckling, cross-fostering, etc.) are et  al., 2002). Furthermore, pigs that received milk conducted, often piglets are not followed down- replacer from birth to weaning had significantly stream into the nursery. Research instead focuses reduced preweaning mortality (Novotni-Dankó primarily on weaning weight. The question then et al., 2015). Nutrient-dense complex milk replacer becomes, does improving weaning weight, trans- has also elicited increased concentrations of meta- late to improved postweaning performance? bolic fermentation products and expression of • Socialization: In socialization studies, pigs are cell proliferation in the crypts along the piglet GI often not regrouped at weaning with pigs they tract, which may explain the performance response had previously been socialized with before wean- (de Greeff et  al., 2016). Alternatively, research in ing. This suggests an opportunity to assess the the last decade has demonstrated that bovine col- effects of postweaning placement strategies in ostrum may be a beneficial substitute for milk re- combination with preweaning socialization on placer because of its high immunoglobulin levels latency to feed and potentially BW loss after (de Lange et al., 2010). Piglets supplemented with weaning. At what time point should we start bovine colostrum had reduced E. coli colonization mixing pigs before weaning? in the intestine, similar to the colonization seen in • Environmental enrichment: Combining enrich- suckling litters (Sugiharto et  al., 2015). Likewise, ment with feeding strategies, such as large, de- the ileal microbiota population of pigs offered bo- structible pellets or play feeders on feed con- vine colostrum more closely resembled sow-reared sumption after weaning. piglets compared to those that received milk re- • Creep feeding: Providing lactation feed on far- placer (Poulsen et  al., 2017). Despite these bene- rowing stall mats prior to weaning as a strategy fits, milk replacer is not widely used throughout to familiarize pigs with solid feed. the industry due to increased labor and hygiene • Topsoil or other bacteria source: Influence of bac- challenges. Additionally, the added cost of milk re- teria exposure on the gut microbial population, placer has prevented further application. piglet performance, and health. While current data on water supplementation for suckling pigs is limited, previous research has demonstrated the importance of preventing dehy- CONCLUSION dration in piglets. This is particularly important as litter size increases and sows milk yield remains rela- Weaning is an important phase of swine pro- tively constant. These data also demonstrate that duction marked by some of the most profound providing milk replacer to pigs prior to weaning stressors. It is during this time period that pigs ex- offers an additional source of nutrients that may hibit low voluntary FI, much of which stems from Translate basic science to industry innovation Pre-weaning effects on postweaning intake Baxter, E. M., K. M. D. Rutherfored, R. B. D’Eath, G. Arnott, their physiological response to stress and the be- S.  P.  Turner, P.  Sandøe, V.A.  Moustsen, F.  Thorup, havioral mechanisms that follow, therefore prevent S.  A.  Edwards, and A.  B.  Lawrence. 2013. The wel- weanling pigs from searching out and consuming fare implications of large litter size in the domestic feed. Several factors are known to influence nu- pig II: management factors. Anim. Welf. 22:2019–238. trient intake after weaning including: doi:10.7120/09627286.22.2.219 Blavi,  L., D.  Solà-Oriol, J.  J.  Mallo, and J.  F.  Pérez. 2016. • Wean age: Weaning older, more developmentally Anethol, cinnamaldehyde, and eugenol inclusion in feed mature pigs helps prevent many of the adverse affects postweaning performance and feeding behavior effects of weaning associated stressors. of piglets. J. Anim. Sci. 94:5262–5271. doi:10.2527/ jas.2016-0760 • Cross-fostering and split-suckling: While there is Boudry, G., V . Douard, J. Mourot, J. P. Lallès, and I. Le Huërou- limited research on the effects of these manage- Luron. 2009. Linseed oil in the maternal diet during ges- ment strategies immediately after weaning, it is tation and lactation modifies fatty acid composition, understood that providing greater opportunities mucosal architecture, and mast cell regulation of the ileal for pigs to nurse prior to weaning should im- barrier in piglets. J. Nutr. 139:1110–1117. doi:10.3945/ jn.108.102640 prove nutrient intake and weaning BW, creating van  den  Brand,  H., D.  Wamsteeker, M.  Oostindjer, a more robust pig for the postweaning period. L. C. M. van Enckevort, A. F. B. van der Poel, B. Kemp, • Socialization: Allowing pigs to mix prior to and J.  E.  Bolhuis. 2014. Effects of pellet diameter dur- weaning improves social skills and encourages ing and after lactation on feed intake of piglets pre- and play behavior, minimizing mixing stress and in- postweaning. J. Anim. Sci. 92:4145–4153. doi: 10.2527/ jury from aggression immediately postweaning. jas2014-7408 Bruininx, E. M. A. M., G. P. Binnendijk, C. M. C. van der Peet- • Creep feeding: Providing creep feed to pigs dur- Schwering, J.  W.  Schrama, L.  A.  den  Hartog, H.  Everts, ing lactation encourages exploratory behavior and A. C. Beynen. 2002. Effect of creep feed consumption and familiarizes pigs with solid feed before wean- on individual feed intake characteristics and perfroamcne ing, increasing immediate postweaning FI. of group-housed weanling pigs. J. Anim. Sci. 80:1413– ◦ Water supplementation in combination with 1418. doi:10.2527/2002.8061413x Cabrera,  R.  A., J.  L.  Usry, C.  Arrellano, E.  T.  Nogueira, creep feed may help pigs learn the difference M. Kutschenko, A. J. Moeser, and J. Odle. 2013. Effects of between hunger and thirst prior to weaning. creep feeding and supplemental glutamine or glutamine • Milk supplementation: Provides an additional plus glutamate (Aminogut) on pre- and post-weaning source of nutrients that may help to reduce pre- growth performance and intestinal health of piglets. J. weaning mortality, particularly in the lightweight Anim. Sci. Biotechnol. 4:29. doi:10.1186/2049-1891-4-29 pig population. Clark, A. B., J. A. De Jong, J. M. DeRouchey, M. D. Tokach, S. S. Dritz, R. D. Goodband, and J. C. Woodworth. 2015. Effects of creep feed pellet diameter on suckling and nur- LIST OF ABBREVIATIONS sery pig performance. Kansas Agric. Exp. Sta. Res. Rep. 8:13. doi:10.4148/2378–5977.1118 GI, gastrointestinal; HPA, hypothalamic pituitary Craig,  J.  R., C.  L.  Collins, K.  L.  Bunter, J.  J.  Cottrell, adrenal; CRF, corticotropin release factor; MC, F.  R.  Dunshea, and J.  R.  Pluske. 2017. Poorer lifetime mast cell; BCAA, branched-chain amino acids; growth performance of gilt progeny compared with sow progeny is largely due to weight differences at birth and FA, fatty acids; PUFA, polyunsaturated fatty acids; reduced growth in the preweaning period, and is not im- BW, body weight; IS, intermittent suckling; ADG, proved by progeny segregation after weaning. J. Anim. Sci. average daily gain; FI, feed intake; FG, feed-to- 95:4904–4916. doi:10.2527/jas2017.1868. 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Amino of non-littermate piglets before weaning improves piglet Acids 50:1289–1299. doi:10.1007/s00726-018-2608-5 Translate basic science to industry innovation

Journal

Translational Animal ScienceOxford University Press

Published: Feb 8, 2021

Keywords: feed intake; nutrient disruption; preweaning; pig

References