3.1.1. Provision of Solid Creep Feed Pre-Weaning
The provision of dry creep feed to suckling piglets is a common practice which has previously been well reviewed [
22,
26]. Creep feed provision has the primary objective to support sow milk production as this becomes a limiting factor for piglet growth during mid-lactation, especially in large litters [
26]. In addition, providing dry creep feed to suckling piglets can help to habituate them to solid feed prior to weaning and to increase feed intake and growth, and improve intestinal structure and function post-weaning. The effects of dry creep feeding on pre and post-weaning growth are not always consistent; some studies find the practice beneficial, while others do not (reviewed by Tokach et al. [
26]). Inconsistencies in the response to dry creep feeding of suckling piglets can be explained by the different approaches to creep feed provision taken by the authors. The duration of creep feeding and piglet age at weaning were reviewed by Tockach et al. [
26] as two important factors affecting the response to creep feeding. Studies in which litters were weaned at 35 days of age or greater demonstrated a consistent gain in weaning weight with creep feeding [
26], which was most likely due to increased creep feed consumption with increasing weaning age. Creep feeding can start as early as two days of age to as late as couple of days before weaning [
26]. The percentage of piglets within each litter eating creep feed (i.e., piglets considered as “eaters”) can also explain differences in outcomes between studies with litters with a higher proportion of ‘eaters’ benefitting most from creep feeding. Several factors can affect creep feed intake of individual pigs, such as the availability of sow’s milk (e.g., if the pig has access to a teat producing a low quantity of milk), piglet birth weight, size of the pellets provided, creep feeding duration, the composition of the creep feed itself, its accessibilty and organoleptic properties (as reviewed by Hunting et al. [
22] and Tokach et al. [
26]). Providing dry creep feed can help to develop the intestinal tract so that it can cope better with the post-weaning diet and this is a principal benefit of the practice. It may stimulate earlier enzyme secretory capacity in the gastrointestinal tract (GIT) of piglets, thereby enabling digestion of non-milk ingredients normally found in diets after weaning. The effect of providing dry creep feed on gut structure are not always consistent either (as reviewed by Hunting et al. [
22]). In order to obtain the greatest benefit, it is generally accepted that creep feed should be offered in small amounts to avoid feed wastage and to keep the feed as fresh as possible. Creep feed supplementation should be started at day 7 to 10 of age to maximize intake. In practice, creep feed intakes can be very variable. Therefore, providing creep feed in liquid form might be a solution to promote intake.
3.1.2. Provision of Supplemental Milk Pre-Weaning
Providing piglets with a liquid diet (supplementary milk or a diet mixed with milk/water) pre-weaning could be a promising strategy to increase creep feed intake prior to weaning. This strategy could reduce the feed neophobia experienced by suckling piglets toward solid feed, increasing DMI and the number of eaters, thereby positively influencing weaning weight [
62] and post-weaning growth [
63]. The provision of supplementary milk replacer to suckling piglets enables the rearing of large litters while they remain suckling their mother [
64]. However, there is no consensus regarding when milk replacer provision should commence, how often milk replacer should be offered during the day and for how long during lactation the practice should be implemented. Supplemental milk can be provided during the entire lactation period starting from 24 hours after farrowing [
65,
66] or for a shorter amount of time starting 5 to 10 days before weaning [
67,
68]. Milk can be supplemented ad libitum [
63,
64] or access to milk may be restricted to a set period of time each day [
62,
69]. Milk can be prepared and fed to piglets manually or through an automated delivery system. Automated delivery systems for supplemental milk replacer are now quite common on European farms (see schematic,
Figure 1). These systems mix milk replacer powder with warm water at a pre-determined concentration. The feeding frequency can be set to approximate ad libitum feeding. Usually fresh milk is prepared at least twice daily. Where milk cups are used, the cups contain a push lever which piglets use to release milk[
70] and milk is available on demand (e.g., Neopigg RescueCare system by Cargill, United States; CulinaCup by Big Dutchman, Germany). Alternatively, some systems contain sensors within troughs and when the milk in the trough is below the level of the sensor, fresh milk is delivered to that trough at the next pre-determined feeding time (e.g., Babyfeed system by Schauer Agrotronic GmbH, Austria; CulinaFlex by Big Dutchman, Germany). Regardless of milk feeding system type, hygiene of the system is essential and systems are normally flushed with an acid daily and an alkaline detergent flush is performed once per week but sometimes as infrequently as once a month. This is done to minimise biofilm formation and to help to ensure good microbial quality in the milk. By cleaning with peracetic acid daily and using an alkaline detergent once a month, Pustal et al. [
64], did not observe any increases in bacterial counts in milk sampled from the tank at the end of the day every 5 days from the 3rd to the 23rd day of supplementation.
Table 3 summarises the effect of milk replacer supplementation to suckling litters on pre-weaning and post-weaning piglet growth and health. Milk intakes are very variable within and between litters. Intakes can be influenced by several factors, such as room temperature or quantity of milk produced by the sow (as reviewed by Huting et al. [
22]). Several studies show an increase in pre-weaning ADG and weaning weight when suckling piglets were supplemented with liquid milk [
62,
63,
67,
68,
71]. Wolter et al. [
63] observed a 16% increase in weaning weight when piglets were supplemented with liquid milk from day 3 post-farrowing to day 21 (weaning). This observation was confirmed in a study conducted by De Greeff et al. [
62] in which piglets supplemented with milk from day 2 to 21 (weaning) were 8% heavier at weaning. Contrary to this, Pustal et al. [
64] failed to find an increase in pre-weaning piglet ADG and weaning weight when supplementary milk was provided to piglets from day 2 post-farrowing to day 28 (weaning). However, in the latter study milk-supplemented litters weaned 1.1 piglets more than litters that were not supplemented and litter weaning weight was increased as a consequence. Wolter et al. [
63] also found that pre-weaning milk supplementation increased the number of pigs weaned by 0.5 piglets per litter. The effect of milk supplementation on pre-weaning mortality is variable, with some studies finding a reduction in pre-weaning mortality when piglets were supplemented with milk [
63,
69] and others showing no effect [
65,
66,
72]. Relatively few studies have followed the growth of milk-supplemented piglets into the post-weaning period and beyond. Wolter et al. [
63] did not observe any effects of pre-weaning milk supplementation on pig growth immediately post-weaning (from weaning to 25 kg). However, they found that pigs supplemented with milk replacer pre-weaning had a 4.5% increase in average daily feed intake (ADFI) and tended to have an increase in ADG (of 3.3%) during the middle of the grower period [from 25 to 65 kg body weight (BW)]. As a consequence, supplemented pigs reached target slaughter weight (110 kg) 3 days before their non-supplemented counterparts [
63]. Park et al. [
69] also recorded the post-weaning growth of pigs that had been provided with supplementary milk from day 4 after birth up to weaning at day 21. In an experiment conducted in the Autumn, weaning weight and pre-weaning mortality were not influenced by milk provision to suckling pigs. In an other conducted in July, weaning weight was increased and pre-weaning mortality reduced in pigs supplemented with milk replacer. Therefore, it would seem that the prevailing temperatures during the period in which pre-weaning milk supplementation to suckling litters is performed can greatly influence the intake of supplemental milk and the response observed. However, in the latter study there was no effect on final slaughter weight in either experiment.
Few studies have investigated the effect of supplementing milk replacer pre-weaning on gut maturity at weaning. De Greeff et al. [
62] observed a 26% increase in small intestinal weight in suckling piglets supplemented with milk replacer for 21 days, as well as a higher relative weight:length ratio compared with control non-supplemented piglets, indicating that the milk supplement stimulated intestinal growth. These authors also observed an increase in crypt depth and a lower villus height:crypt depth ratio in the ileum of milk-supplemented piglets at day 21 (weaning). This indication of higher cell-proliferation rates could imply an impairment of intestinal integrity in this study. However, Hu et al. [
73] did not observe any differences in villus height or crypt depth in the jejunum at day 28 (weaning) and day 35 (8 days post-weaning), in pigs supplemented with milk during the suckling period compared to non-supplemented pigs. Regarding enzyme production, they found lower lactase and higher sucrase activity at day 28 and higher maltase activity at day 35 in the jejunum of pigs supplemented with milk, suggesting that pre-weaning supplementary milk provision to suckling pigs may induce earlier maturation of the jejunum. The effect of pre-weaning liquid milk supplementation on intestinal microbiota composition is not consistent, with some studies demonstrating a benefit from pre-weaning milk supplementation [
73] and others not [
74]. Hu et al. [
73] observed a greater abundance of
Clostridium XI,
Turicibacter and
Moraxella at day 28 of age in the jejunum of piglets supplemented with milk from day 4 to 28 after birth in comparison to control unsupplemented pigs. In addition, they demonstrated an increased abundance of
Lactobacillus and a decreased abundance of
Streptococcus and
Blautia in the jejunum at day 35 (7 days post-weaning), indicating that the milk supplement may have increased the abundance of beneficial bacteria in the small intestine, therefore helping to maintain intestinal homeostasis. In a study in which pigs were supplemented with milk from day 7 post-partum until day 21 (weaning), Jin et al., [
74] observed that the supplemented group had higher bacterial species richness estimates (ACE and Chao1) in the jejunum compared to control unsupplemented pigs, indicating a higher number of bacterial species. However, the supplemented group had similar Simpson and Shannon diversity indices compared to the control, indicating that there were no differences in the abundance of each species. The supplemented group had lower abundances of
Romboutsia,
Actinobacillus,
Bacteroides and
Lactobacillus than the control group (
P<0.05), indicating that the abundance of some beneficial bacterial (such as
Lactobacillus) was reduced in pigs supplemented with milk. The authors surmise that the decrease in
Lactobacillus abundance could be the result of reduced ingestion of sow milk containg oligosaccharides. However, this would also have been the case in the Hu et al. [
73] study and they observed the opposite. This lack of agreement across studies is liley due to differences in the composition of the supplementary milk fed. De Greeff et al. [
62] observed an increase in concentrations of the volatile fatty acids (VFA), acetate, propionate, butyrate and valerate in the colon of milk-supplemented versus non-supplemented piglets at day 21 of age (weaning). Volatile fatty acids are fermentation end-products of the colonic microbiota and the higher concentrations in the milk-supplemented pigs reflect a change in the composition of the colonic microbiota which is likely explained by the high total dietary fiber content of the milk used in this study compared to sow milk. However, no microbiome analysis was conducted in this study.
It would appear that supplementing suckling piglets with milk from 1-4 days after birth until weaning can increase weaning weight [
62,
63,
65,
67,
68,
71,
72], and the number of piglets weaned [
63,
64] and reduce mortality pre-weaning [
63,
69]. The benefit of pre-weaning milk supplementation on intestinal maturation and microbiota after weaning is not consistent and likely linked to milk composition [
62,
73]. Although not extensively studied, some studies report increased post-weaning growth in response to providing liquid milk replacer to suckling pigs [
63,
67,
68].
Table 3.
Effect of pre-weaning milk replacer supplementation on pre-weaning and post-weaning piglet growth and health. Litters provided with milk replacer are compared to litters not provided with milk replacer, unless otherwise stated (modified from Middelkoop, [
21]).
Table 3.
Effect of pre-weaning milk replacer supplementation on pre-weaning and post-weaning piglet growth and health. Litters provided with milk replacer are compared to litters not provided with milk replacer, unless otherwise stated (modified from Middelkoop, [
21]).
SA1 (days) |
WA2 (days) |
Pattern of Provision
|
Pre-weaning effects (d0 = birth) |
Post-weaning effects (d0 = weaning) |
Reference |
Litter size |
Supplemental Milk Intake |
ADG3
|
Weaning weight |
Other |
ADFI4
|
ADG |
FCR5
|
Other |
1 |
21 |
Ad libitum |
2.5 L of milk/pig (375 g DM6 cool season) 9.9 L of milk/pig (1.49 kg DM warm season) |
NA7
|
↑ |
↑ total litter weight= mortality↑ glucose, IGF-I8 and thyroxine in serum at weaning |
NA |
NA |
NA |
NA |
[65] |
10.4 |
4 |
28 |
Ad libitum |
4.76 L of cow’s milk/pig; 10.96 L artificial milk/pig (200 g total solids/ L) |
= from d0 to d14 ↑ from d14 to 28 ↑ from d0 to 28 |
↑ |
NA |
NA |
NA |
NA |
NA |
[71] |
12 |
10 |
20 |
Ad libitum |
3.9 L of milk/pig (200 g of skim milk powder/ L) |
↑ |
↑ |
NA |
↑ from d0 to d21 |
↑ from d0 to d21 |
NA |
↑ weight at d21 |
[67] |
12 |
3 |
21 |
Ad libitum |
1000 g of milk powder /pig |
= |
↑ |
↘ % mortality↗ number weaned |
↑ from 25 to 65 kg (grower period) |
↑ from 25 to 65 kg (grower period) |
= |
reached slaughter weight 3 days earlier |
[63] |
12 |
3 |
26 |
Ad libitum |
13.8 mL to 10.35 L of milk/ pig (winter); 43.7 mL to 17.25 L of milk/pig (summer) (150 g powder/L of water) |
= |
↑ |
= % mortality= % medicated piglets |
= from d0 to 42 |
= from d0 to d42 |
= from d0 to 42 |
= % mortality= % medicated pigs |
[72] |
10 to 11 |
4 |
21 |
From 8:00 to 16:00 h daily |
NA (Trial 1 – late fall) 22 g of milk powder/pig (Trial 2 - summer) |
=(Trial 1) ↑(Trial 2) |
=(Trial 1) ↑(Trial 2) |
↘ % mortality (Trial 2) |
NA |
↑ d21 to d54 (trial 1)= (trial 2) |
NA |
= carcass weight, back fat thickness, dressing percentage |
[69] |
10 |
1 |
28 |
Twice a day or as needed |
3.86 L/pig or 138 mL/pig/day (150 g of powder/L of water) |
= |
= |
= % mortality↑ antibiotic treatments |
NA |
= from d0 to d21, d21 to d72, d72 to 115 |
NA |
= % mortality |
[66] |
11 to 12 |
2 |
28 |
Ad libitum |
520 g of powder/pig (20 g/pig/day) |
= |
= |
↑ number weaned↑ total litter weight= mortality, diarrhoea↓ treatment of facial lesions |
NA |
NA |
NA |
NA |
[64] |
16.8 |
2 |
21 |
Twice a day from 7:00 to 8:00 and from 15:00 to 16:00 h |
From d0-d7: 75 g DM6 (litter/day) From d7-d14: 225 g DM (litter/day) From d14-21: 773 g DM (litter/day) |
NA |
↑ |
↑ IGF-18 gene expression at d21 in jejunum mucosa↑ small intestine weight at d21↑ crypt depth and ↓ villus height:crypt ratio in the ileum at d21↑ Volatile fatty acids in the colon at d21 |
NA |
NA |
NA |
NA |
[62] |
13 to 14 |
22 |
27 |
200 ml/pig per day |
172.5 g of creep/pig |
↑ |
↑ |
NA |
↑ from d0 to d14↑ from d14 to d28 |
↑ from d0 to d14↗ from d14 to d28 |
= from d0 to d14↑ from d14 to d28 |
NA |
[68] |
NA |
4 |
28 |
Ad libitum |
NA |
= |
NA |
At d28 in colon:=bacterial diversity9=bacterial species richness10↑ VFA11↓ Lactobacillus, Clostridium XI, Blautia, Clostridium sensu stricto, Escherichia↑ Paraprevotella↗ Ruminococcus, Clostridium XIVa and IV, Succiniclasticum↑ TLR412 gene expression, ↓ IL-613 gene expression in mucosa |
= from d0 to d7 |
= from d0 to d7 |
NA |
↘ diarrhea frequency |
[75] |
8 |
4 |
28 |
Ad libitum access, provision of fresh milk at 9:00 and 19:00h |
NA |
= |
NA |
= villus height, crypt depth in jejunum at d28↓ lactase activity and ↑ sucrase activity in jejunum |
= |
= |
NA |
In jejunum at d7:= villus height, crypt depth↑maltase activity↑ Lactobacillus↓ Streptococcus
|
[73] |
8 |
7 |
21 |
Ad libitum access |
NA |
↑ |
↑ |
↓ diarrheaAt d21, in jejunum:↑ bacterial species richness14= bacterial diversity↓ Romboutsia, Actinobacillus, Bacteroides and Lactobacillus
|
NA |
NA |
NA |
NA |
[74] |
NA |
1 |
28 |
From 15:00h on day 1 until weaning |
For all piglets alive: From d1 to d12, 1.67 L/pig or 125 mL/pig/day) From d12 to d28, 3.2 L/pig or 200 mL/pig/day (150 g of powder/ L of water) |
NA |
↑ in litters of 17 piglets at d1 = in litters of 14 piglets at d1 |
↓ risk of piglets dying |
NA |
NA |
NA |
NA |
[76] |
14 or 17 |
1 |
28 |
From 15:00h on day 1 until weaning |
NA |
= |
= |
= body fat and body protein content |
NA |
NA |
NA |
NA |
[77] |
14 or 17 |
3.1.3. Provision of Supplemental Liquid Feed Pre-Weaning
The provision of supplemental milk pre-weaning can increase pre-weaning DMI, growth and reduce pre-weaning mortality, as outlined in
Section 3.1.2. However, it does little to expose piglets to the plant-based ingredients that they will encounter in the dry diets fed post-weaning. A solution to this is to provide suckling piglets with liquid feed pre-weaning (i.e., dry feed in a gruel form or an enriched milk containing plant-based compounds). Few studies to date have compared the effect of providing supplementary liquid feed to suckling piglets, with dry creep feeding and/or with no creep feeding (dry or liquid). One such study by Lawlor et al. [
78], supplemented a liquid mixture of milk and feed to suckling piglets from 12 days of age to weaning, with creep-fed litters only standardized at 8 piglets. In this study, creep feeding the liquid mixture and standardizing litters at 8 piglets increased weaning weight by 7%. However, the authors concluded that the increase in weaning weight was most likely achieved due to the reduced number of suckling pigs per sow. In a recent study conducted by our group, Arnaud et al. [
79] supplemented suckling piglets with a liquid mixture of milk with an increasing proportion of starter feed from day 3 of age to day 28 (weaning). We did not observe an increase in weaning weight when suckling piglets were supplemented with the liquid mixture. However, pigs supplemented with the liquid mixture pre-weaning had a higher BW at slaughter (~ + 2 kg) than non-supplemented pigs ([
79], unpublished). These results can be explained by a better intestinal structure at 7 days post-weaning (+ 17% in villus height in the ileum), which most likely positively influenced nutrient absorption ([
79], unpublished). Kobek-Kjeldager et al. [
70] supplemented milk to suckling piglets from day 2 to 12 of lactation, followed by liquid feed from day 12 to weaning. This trial also compared two different weaning ages(day 24 or 35). Providing the liquid diet before weaning was found to shorten the latency period to first feed consumption post-weaning but had no impact on the latency to first water consumption following weaning. Interestingly, a change in feeding behaviour was observed at the transition from supplementary milk to liquid feed on day 12, with a reduction in the number of feeding bouts observed the day following the diet change.
Some studies demonstrated a benefit to supplementing liquid creep feed in comparison to dry creep feed in terms of increased pre-weaning ADFI [
80,
81]. Martins et al. [
81] observed that pigs supplemented with a gruel feed (pre-gelatinized rice, micronized soybean, and whey mixed with water at a 1:1 ratio) from day 3 of age to day 21 (weaning) had a ~566% higher ADFI during the first days of supplementation (day 3 to 7) than pigs supplemented with dry creep feed. Similarly, Byrgesen et al. [
80] showed that pigs supplemented with liquid creep from day 10 of age to day 28 (weaning) had a ~270% higher dry matter disappearance during the first week of supplementation (day 10 to 18) than pigs supplemented with dry creep. However, these studies found no increase in pre- and post-weaning ADG in response to pre-weaning supplementation of liquid creep feed. Despite higher intakes, Byrgesen et al. [
80] and Martins et al. [
81] found that weaning weight in piglets offered liquid creep feed did not differ from piglets offered dry creep feed. This could be due to the higher number of piglet eaters observed in litters offered dry creep feed compared to litters offered liquid creep feed, even though piglets supplemented with liquid creep had a higher average intake. In the study by Byrgesen et al. [
80] , suckling pigs supplemented with dry creep feed were 9.6% heavier at day 61 post-weaning compared to pigs fed liquid creep feed during the suckling period. Futhermore, Martins et al. [
81] showed that suckling pigs supplemented with dry creep feed had less variation in BW at day 133 post-weaning and a similar slaughter weight compared to pigs fed gruel creep feed during the suckling period. On the contrary, Arnaud et al. [
79] found that pigs which were offered a liquid mixture of milk and starter diet pre-weaning were 1.6% heavier at slaughter (157 days of age) than pigs offered dry creep pre-weaning.
In a recent study, Amdi et al. [
82] compared the growth and intestinal morphology and function of piglets fed milk replacer to that of piglets fed the same milk replacer with added wheat from day 3 to 25 post-farrowing. No treatment differences were found for weaning weight, jejunal morphology (villus height, crypt depth and villus height to crypt depth ratio) and intestinal gene expression. However, an increase in the activity of sucrase and maltase in the small intestine was found just prior to weaning (~25 days of age) in response to the addition of wheat to the liquid milk. These enzymes are important for the digestion of vegetable-based ingredients, and an increase in their activity at weaning suggests that these pigs should be better equiped to digest ingredients in the normally dry diet fed post-weaning. In another study, enzyme activities just before weaning (~25 days of age) were compared between piglets offered liquid creep feed and piglets offered dry creep feed [
80]. Here, the activities of sucrase and maltase in the proximal part of the small intestine were highest in piglets supplemented with dry creep even though DMI was highest when liquid creep feed was provided. Therefore, it is possible that the form of the creep feed (solid vs. liquid) may influence enzyme activity more than DMI [
80]. This could be due to the occurrence of spontaneous fermentation in liquid creep feed, which changes its physicochemical properties and its effect on the GIT.
From those studies, it appears that supplementing liquid creep feed instead of dry creep feed can increase pre-weaning ADFI [
80,
81]. In addition, supplementing liquid creep feed instead of milk can improve intestinal enzyme maturation [
80,
82]. However, increases in liquid creep feed intake and changes in intestinal function do not always result in increased growth pre- and post-weaning due to the low number of piglets consuming creep feed within litters.