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ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
* Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University,3584 CL Utrecht, The Netherlands; and
and
Animal Health and Reproduction Group, Wageningen Institute of Animal Science, Wageningen University and Research Centre,6700 AH Wageningen, The Netherlands
Abstract
An experiment was conducted to study effects of intermittent suckling on creep feed intake and weight gain of litters. Loss of weight and backfat during lactation, as well as reproductive performance, were also measured. Batches of multiparous sows (Parity 1 to 12, 4.1 on average) were either suckled intermittently (IS, eight batches; n = 50) or continuously (control, eight batches; n = 62). Litters were weaned at 27 ± 2 d of age, on average. Litter size (11.1 ± 0.2 piglets, on average) was standardized within a batch within 3 d of birth. All litters had free access to creep feed and water from 1 wk of age onward. In the IS group, litters were separated from the sow for a period of 12 h/d (0930 to 2130), starting 11 d before weaning. Rectal ultrasonography was applied at d 3 after weaning to check the ovaries for follicle development or presence of corpora lutea. Creep feed intake by the litters during lactation was higher in IS litters than in control litters (686 ± 57 vs. 314 ± 42 g/piglet, P < 0.01). The distribution of creep feed intake shifted from a skewed one, with a majority of litters consuming less than 250 g/piglet in control litters, to a normal distribution, with an average creep feed intake of 500 to 750 g/piglet in IS litters. During the 7 d after weaning, creep feed intake in IS litters was also higher (281 ± 15 vs. 204 ± 9 g•piglet-1•d-1, P < 0.01). The ADG of piglets during lactation was negatively affected by IS, resulting in lower weight at weaning (7,229 ± 140 vs. 7,893 ± 145 g/piglet, P < 0.05). During the 7 d after weaning, however, ADG was higher in IS litters (255 ± 10 vs. 177 ± 8 g•piglet-1•d-1, P < 0.01), and 7 d after weaning, the weights of the litters were similar (9,011 ± 167 vs. 9,132 ± 164 g/piglet, P = 0.81). The IS litters that consumed little or no feed during lactation had an ADG after lactation that was higher than in control litters, with comparable creep feed intake during lactation: 204 vs. 136 g/d. Body weight loss by the sows during lactation was lower in IS sows (-10 ± 2 vs. -16 ± 1 kg, P < 0.05). A higher percentage of IS sows ovulated during lactation (22 vs. 3%, P < 0.01), and weaning-to-ovulation interval (excluding sows with lactational ovulation) was shorter in IS sows (4.7 ± 0.2 vs. 5.3 ± 0.2 d, P < 0.05). We conclude that IS increased creep feed intake during lactation, and that IS increased ADG after weaning, despite lower weaning weights. Ovulation during lactation was induced in 22% of the IS sows.
Key Words: Feed intake • Growth • Pig • Reproductive Performance • Sow • Suckling
Introduction
In the modern pig industry, piglets are usually weaned before 4 wk of age, thus changing abruptly from a diet of highly digestible milk to a relatively poorly digestible starter diet. As a result, feed intake and growth are reduced after weaning and piglets are more vulnerable to develop diarrhea. Intake of a sufficient amount of creep feed during lactation creates a more gradual transition at weaning and can reduce postweaning disorders (English, 1980
). However, creep feed consumption during lactation is usually low and is also highly variable between piglets and litters (Aherne et al., 1982; Barnett et al., 1989; Appleby et al., 1992).
One way to increase feed intake during a lactation period of 3 to 4 wk could be intermittent suckling (IS), a management technique in which piglets are separated from the sow during a number of hours every day in the second part of lactation. Intermittent suckling could also improve reproductive performance of the sows by diminishing the negative energy balance of the sow during lactation and by diminishing the suckling stimulus (Foxcroft, 1992). Previous work on IS was performed during lactation periods longer than 35 d (Henderson and Hughes, 1984; Grinwich and McKay, 1985; Appleby et al., 1991) or using short separation times ranging from 3 to 6 h/d (Newton et al., 1987; Costa and Varley, 1995), and extensive research on both piglets and sow has never been integrated into a single experiment.
The objective of this study was to determine the effects of intensive (12 h/d) intermittent suckling during the last 11 d of a 27-d lactational period. Effects of IS on creep feed intake and weight gain of the piglets and on reproductive performance of the sow were integrated into a single experiment.
Materials and Methods
Animals and Housing
The experimental design was approved by the Ethical Committee of the Veterinary Faculty of Utrecht University (The Netherlands).
One hundred twelve sows were used (Dutch Landrace [DL; n = 17], Yorkshire [Y; n = 22] and crossbred [DL x Y; n = 73]) between November, 1999, and June, 2000. Parity ranged from 1 to 12 and was 4.1 ± 0.3 on average. During lactation, the sows were housed individually in pens (2.40 x 1.80 m) in farrowing crates (2.40 x 0.65 m). The farrowing pen consisted of 1.95 m2 of solid floor and 2.37 m2 of slatted floor. At the front of the pen, there was a piglet nest (1.08 x 0.85 m) with an infrared lamp (150 W). Control and intermittent suckling (IS) batches were housed in separate rooms during lactation. After weaning, sows were moved to a mating room and the piglets stayed in the pen. Sows were fed a commercial lactational feed based on tapioca, palm kernel expeller, soybeans (extracted), sunflower seed (extracted), rape seed (extracted), and wheat middlings (9.1 MJ NE/kg, 13.9% CP, and 0.8% lysine) at a level of 1% of body weight at farrowing plus 500 g per piglet (Dutch feeding tables published in 1995), divided over three meals per day (as-fed basis). Water was available ad libitum. Lights were on between 0730 and 2330.
To synchronize the start of intermittent suckling within a batch, d 0 was designated as the start of data collection. Intermittent suckling always started 14 d after d 0, and 11 d later (d 25) weaning took place. Piglets were born between 6 d before and 4 d after d 0. At weaning piglets were 27 ± 2 d old, on average. Litter size at birth varied from 7 to 17 piglets but was standardized within 3 d after birth by cross-fostering within each batch (maximum range at weaning 7 to 12 piglets). Litter size was 11.1 ± 1.9 after cross-fostering and 10.3 ± 1.4 at weaning. Within the first 3 d after birth, piglets received an injection of 1 mL of iron dextran, were identified by tattooing and males were castrated.
Creep feed that was based on milk products (34%), soybeans, corn, sugar, vegetable oil, premix (12.8 MJ NE/kg, 21.7% CP, 1.46% lysine; as-fed basis) was offered to the piglets ad libitum from d 7 onward and given in a round piglet trough. From d 14 to 21, a piglet feeder with two feeding spaces was used. During d 21 to 23, a gradual change (respectively 40, 60, and 100% replacement) to another creep feed based on milk products (18.5%), barley, soy beans, corn, sugar, vegetable oil, premix (11.4 MJ NE/kg, 17.9% CP, 1.25% lysine; as-fed basis) was made. This feed was given until the end of the experiment (7 d after weaning) in a feeder with four feeding places. Drinking nipples were used to give ad libitum water to the piglets.
Treatments
There were two treatments, control and intermittent suckling (IS). Sixteen weekly farrowing batches were alternately allocated to each treatment: eight control batches (total of 62 sows) and eight intermittent suckling batches (total of 50 sows). Each batch consisted of four to nine sows. In the control treatment, piglets had access to the sow for 24 h/d. In the IS treatment, the piglets were separated from the sow for 12 h each day (0930 until 2130) during d 14 to 25. Separation did not allow physical or visual contact, although sow and piglets remained in the same pen. During separation, piglets were kept on approximately 2.0 m2, including a piglet nest, a drinking nipple, and a feeder.
Measurements
Piglets were weighed individually at birth, at d 0, 7, 14, 21, 25 (weaning), and 7 d after weaning, and ADG was calculated. Creep feed residuals were assessed at 2- to 3-d intervals. Because no food wastage was observed (feeder was placed on a solid floor), disappeared creep feed was considered eaten. General health variables were checked daily. Use of medication was monitored.
Sows were weighed and P2 backfat (65 mm from the midline over the last rib) thickness was measured within a few hours after farrowing and on the day of weaning (d 25). Detection of estrus was performed two times each day from weaning onward, at 0830 and 1600. A sow was considered to be in estrus when showing a standing response induced by a back pressure test in the presence of a boar. Ovarian status (follicle size, presence of corpora lutea) was assessed by using transrectal ultrasonography at d 3 after weaning, and this was repeated if the sow had not shown estrus by d 7 after weaning. Detection of estrus and transrectal ultrasonography was performed by two persons. Sows were mated at first observed estrus after weaning. If weaning-to-mating interval was longer than 7 d and the ultrasound scan on d 3 after weaning showed the presence of corpora lutea, the weaning-to-ovulation interval was calculated as the weaning-to-mating interval minus 21 d. In animals that did not have corpora lutea on d 3 after weaning, weaning-to-mating interval was considered the same as weaning-to-ovulation interval, such that the day of ovulation was the day of mating.
Statistical Analysis
Data were analyzed using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC). Variation between sows within a batch was not regarded independent. Furthermore, only one treatment was applied per batch. Therefore, batch was the experimental unit. Treatment effects were tested against variation between batches. Data were obtained on a litter basis but were expressed on piglet basis. The average daily creep feed intake (ADCFI) of the piglets, ADG of the piglets, and piglet weight were analyzed as litter characteristics using the following model: Yij = µ + Ti + Bj(Ti) + a + bw + eij, with Ti = treatment, Bj = batch (nested within treatment), a = age of the piglets in relation to d 0, and bw = birth weight of the piglets. The ADCFI of the piglets during lactation tended to affect ADG of the piglets after weaning differently in the two treatment groups (P = 0.06). This interaction (Ti x ADCFI) was therefore included in the analysis for ADG after weaning. Weight change of the sow, during the weaning-to-mating and weaning-to-ovulation intervals, was analyzed using the following model: Yij = µ + Ti + Bj(Ti) + eij, with Ti = treatment and Bj = batch (nested within treatment). Weight of the sow after farrowing was included as a covariate in the analysis of weight change of the sow. Sow body weight and sow back fat were also analyzed, with parity as a covariate. Sows were classified either as Parity 1 and 2, or as Parity 3 and higher. Relevant two-way interactions were not significant. Only for sow body weight loss, the interaction of Ti x parity (two classes) was significant and included in the model. Blood line of the sow was never significant and omitted from the model. Correlations between variables were calculated using the CORR procedure of SAS. Data on the number of sows that ovulated during lactation were analyzed using the 
2 test in the FREQ procedure. Data were presented as means ± SE. Differences are considered to be significant if P < 0.05.
Results
Piglet Survival
No difference was found between treatments in number of piglets at birth (11.8 ± 0.4 vs. 11.6 ± 0.3; P = 0.59), d 0 (11.3 ± 0.3 vs. 11.0 ± 1.8; P = 0.64), at weaning (10.4 ± 0.2 vs. 10.2 ± 0.2; P = 0.69) and 7 d after weaning (10.3 ± 0.2 vs. 10.1 ± 0.2; P = 0.81). Therefore, mortality did not differ between treatments (9 vs. 9.1%; P = 0.997). Illness (diarrhea, lameness) and treatment for illnesses did not differ between IS and control piglets.
Piglet Feed Intake
Before start of IS, there was no difference in creep feed intake of the litters between the treatments (Figure 1). After starting IS at d 14, however, creep feed intake was higher in IS litters between d 14 and 21 and between d 21 and 25. Average total creep feed intake during lactation was 686 ± 57 g/piglet for the IS treatment and 314 ± 42 g/piglet for the control treatment (P < 0.01). Distribution of creep feed intake during lactation was shifted from a skewed one, with a majority of litters (66%) consuming less than 250 g in the control piglets, to a normal distribution, with average creep feed intake during lactation between 500 to 750 g in IS piglets (Figure 2). Also during the 7 d after weaning, creep feed intake was higher in the IS piglets.
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Irrespective of treatment, variation in creep feed intake between litters was fairly consistent over the lactation period. Correlations of creep feed intake between 1 wk and another ranged from 0.55 to 0.76 (P < 0.01). This consistency continued after weaning (r = 0.67, P < 0.001). Thus, piglets with higher creep feed intake during lactation had higher feed intake after weaning (Figure 3). Intermittent suckling litters with low creep feed intakes during lactation had creep feed intakes after weaning that were higher than those of control litters with comparable creep feed intakes during lactation, although the interaction treatment x creep feed intake of the piglets during lactation was not significant: intercept 1,381 vs. 1,103 g/piglet (Figure 3).
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ADG and Weight of the Piglets
Variation in ADG between litters of different sows was considerable and total weight gain during lactation ranged from 3,953 to 7,630 g in IS piglets and from 4,183 to 9,850 g in control piglets. During the 7 d after weaning, ADG ranged between 74 and 422 g/d for the IS piglets and between 31 and 307 g/d for the control piglets.
Piglet ADG (Figure 1
) did not differ between IS and control piglets during the first 14 d of the experiment, when IS had not yet started. Between d 14 and 21 (first 7 d of IS), ADG was lower in the IS piglets. Between d 21 and d 25, ADG was also lower. After weaning, ADG was higher in the IS piglets.
After weaning, ADG was positively related to the total amount of creep feed consumed during lactation (r = 0.63, P < 0.001). This relation tended to be different for the two treatments (creep feed intake x treatment interaction, P = 0.06; Figure 4). Intermittent suckling litters that consumed little or no creep feed during lactation nonetheless had an ADG after lactation that was higher than in control litters with comparable creep feed intake during lactation: intercept 204 vs. 136 g/d (P < 0.001).
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) did not differ between treatments at d 14 (P = 0.72). As a result of the reduced growth of the IS piglets during d 14 to d 21, however, their weight at d 21 was lower than that of the control piglets. At weaning, piglet weight was still lower in the IS piglets. However, 7 d after weaning this difference had disappeared (P = 0.81).
Sow Weight and Backfat Thickness
Sow body weight after farrowing (Table 1) did not differ between treatments. At weaning, however, weight loss was lower in the IS sows and thus body weight after weaning was higher in the IS sows. This difference in sow weight loss was not apparent in sows of Parity 1 and 2 (IS: -12.7 ± 2.7 kg [n = 25] vs. control: -14.6 ± 2.2 kg [n = 16]; P = 0.48) but was significant in sows of Parity 3 or higher (IS: -8.9 ± 1.9 kg [n = 33] vs. control: -16.5 ± 1.8 kg [n = 33]; P < 0.001). In these two parity groups (younger and older sows), no effect of treatment was found on total growth of the litters during lactation (young: 6,074 ± 180 vs. old: 6,168 ± 128 g/piglet; P = 0.30) or on creep feed intake of the litters during lactation (young: 411 ± 53 vs. old: 522 ± 53 g/piglet; P = 0.12). Weight change of the sow was correlated with weight of the piglets at weaning (r = -0.26; P < 0.01) and number of piglets weaned (r = -0.28, P < 0.01).
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Weaning-to-Mating and Weaning-to-Ovulation Intervals
A higher percentage of IS sows (22%; 11 of 49) than control sows (3%; 2 of 61) had an ovulation during lactation. Therefore, the calculated weaning-to-ovulation interval was shorter in IS sows (2.9 ± 0.5 vs. 5.1 ± 0.2 d; P < 0.01; Figure 5). Even when excluding sows with lactational ovulation, weaning-to-ovulation interval was shorter in IS sows (4.7 ± 0.2 vs. 5.3 ± 0.2 d; P < 0.05). Sows that had lactational ovulation returned to estrus and were mated on average at d 18 ± 0.6. As a consequence, the distribution of weaning-to-mating interval was dichotomous, with the majority of sows being mated between d 4 and 6, and the rest of the sows at d 18. Overall, weaning-to-mating interval was 8.1 ± 0.9 d in IS sows and 6.9 ± 0.9 d in control sows.
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Discussion
Intermittent suckling (IS) increased creep feed intake during lactation 218% on average. This increase is in agreement with results of a early study (Thompson et al., 1981), in which IS almost doubled creep feed intake in one experiment and tripled it in another during a 33-d lactation. Later, in another study (Plagge and Van der Peet-Schwering, 1998), IS had no effect, probably due to the fact that IS and control piglets were housed in the same room. Nursings are accompanied by noise and are synchronized within one room. Intermittent suckling piglets that do not have access to the sow can hear these nursings but cannot start drinking. This probably resulted in a high level of restlessness and did not encourage piglets to go to the feeder. In our experiment, this restlessness was possibly prevented by separating the IS and control sows into different rooms.
During lactation, IS resulted in an increase in creep feed intake although it did not prevent the usual high variation in creep feed intake between litters (Aherne et al., 1982; Barnett et al., 1989; Appleby et al., 1991; Pajor et al., 1991; Delumeau and Meunier-Salaun, 1995). Sixty percent of the IS litters had an average creep feed intake per piglet during lactation of more than 600 g, which is a level needed for better performance after early weaning as suggested by English (1980). In the control litters, by contrast, only 20% consumed more than 600 g/piglet during lactation and 66% of the litters consumed less than 250 g/piglet. So, IS resulted in a shift in the distribution of creep feed intake and improved creep feed intake especially in litters with an otherwise low creep feed consumption.
The higher creep feed intake caused by IS resulted in better performance after weaning: IS litters had higher creep feed intake and higher ADG after weaning. The higher ADG after weaning compensated for the negative effects of IS on ADG during lactation, which had led to lower weaning weights of IS litters. The growth depression during lactation as a result of IS was in agreement with results from previous studies (Thompson et al., 1981; Henderson and Hughes, 1984), although others found no effects on weight gain (Newton et al., 1987). Apparently, IS decreased the milk intake in our study, and piglets failed to compensate for their milk intake deficit during the 12 h that they were with the sow. When separation takes place for only 6 h/d (Newton et al., 1987), milk intake is possibly not reduced or can be compensated for and will thus not affect weight gain during lactation. The lower weaning weights in our experiment did not negatively affect growth during the first 7 d after weaning. So growth shortly after weaning seems to depend on adaptation of the piglet to solid food rather than on weaning weight.
Weight gain and feed intake of the litters after weaning was positively related to creep feed intake during lactation. However, IS litters that had little or no creep feed intake during lactation still tended to have a weight gain after weaning that was 68 g/d higher than control litters with comparable creep feed intake during lactation. Also, feed intake after weaning tended (P = 0.08) to be higher in IS litters than control litters with comparable creep feed intake during lactation, although this was not significant. Apparently, positive effects of IS on the growth and feed intake of the litters after weaning were also mediated by some mechanism other than by increased creep feed intake during lactation. Possibly, IS litters experienced weaning as a less-stressful event because they were already used to separation from the sow.
Weaning is associated with the withdrawal of nutrients from sow milk, and intake of a starter diet can be delayed for 4 to 20 h in pigs that eat during lactation and up to 48 h in pigs that do not eat (Bruininx et al., 2002). The withdrawal of nutrient supply to the small intestine, together with the stress of weaning, results in a transient shortening of the small intestinal villi and a reduction in the absorptive capacity (Marion et al., 2002). Nabuurs et al. (1996) showed that offering creep feed during lactation, in combination with IS, partly prevents piglets from the usual decrease in villus height and net absorption in the small intestine that occurs after weaning. So IS could result in a healthier gut of the piglet after weaning by increasing creep feed intake during and after lactation and possibly by reducing stress at weaning. As a result, the risk of developing postweaning diarrhea might be decreased and litter performance could be improved. In this experiment however, the influence of IS on diarrhea after weaning could not be assessed because the incidence of postweaning diarrhea was already low in the control group.
The method of IS is only acceptable if sow reproductive performance is not compromised. Therefore, the effects on reproductive performance of the sow also were studied in this experiment. Ovulation was advanced by IS, resulting in lactational ovulation in a number of sows and shortened weaning-to-ovulation interval. Reproductive performance is affected by the metabolic state of the sow and the suckling stimulus of the piglets (Foxcroft, 1992). As a result of lactation, the sow often becomes catabolic, which can result in suboptimal reproduction after weaning (Foxcroft, 1992; Einarsson and Rojkittikhun, 1993; Foxcroft et al., 1996). In our experiment, weight loss of the sows was significantly reduced during the 11 d of IS. This probably resulted from lower milk production in IS sows because piglet weight gain, which is highly correlated with milk nutrient production (Noblet and Etienne, 1989) was lower in IS sows.
In our experiment, however, no relationship was found between weight loss of the sow and weaning-to-ovulation interval, although both were decreased in IS sows. This is in contrast with a review by Foxcroft et al. (1996), who reported that a catabolic state has a negative effect on weaning-to-estrus interval. In our study, sows lost less than 8% of their body weight, which was probably not enough to result in prolonged weaning-to-estrus interval. Vesseur et al. (1994) showed that weaning-to-estrus interval was prolonged when weight loss exceeded 12.5%, especially in first-parity sows. It was suggested earlier (Foxcroft, 1992) that "in sows with a reasonable energy balance, the inhibitory effects of suckling are more potent inhibitors of LH secretion than the metabolic demands of milk production." Suckling of piglets blocks GnRH secretion by the hypothalamus (Britt et al., 1985; Armstrong et al., 1988) and thereby blocks follicular development during lactation. In agreement with these findings, IS increased the incidence of lactational ovulation in our experiment. Costa and Varley (1995) did not find lactational ovulation, possibly because of the short duration of separation (3 h/d, during 9 d). Even higher percentages of sows showing lactational ovulation can be achieved by increasing the duration of separation (Grinwich and McKay, 1985) or increasing lactation length (Crighton, 1970; Stevenson and Davis, 1984). So in our experiment, IS decreased weaning-to-ovulation interval probably mainly by decreasing the suckling stimulus and not by decreasing the negative energy balance.
Further research should be done on the effect of IS on the behavior and welfare of the piglets, the performance of the piglets until slaughter, and the development of the gastrointestinal tract. More research is also needed on the effect of IS on ovarian activity during lactation and the (hormonal) mechanisms behind it.
Implications
Intermittent suckling increases feed intake and growth in piglets after weaning, partly by enhancing creep feed intake during lactation. In addition, intermittent suckling probably affects growth and feed intake after weaning independent of creep feed intake during lactation. Metabolic stress in the sow and the suckling stimulus of the piglets was decreased by intermittent suckling. This can result in shortened weaning-to-mating interval but also in lactational ovulation. In practice, however, lactational ovulation can only be useful if sows can be mated during lactation.
Footnotes
1 The authors gratefully acknowledge the help of J. Berends and J. van Mourik during the experiment, and Denkavit Nederland. 
2 Correspondence—phone: +31 30 2531820; fax: +31 30 2521887; e-mail: w.i.kuller{at}vet.uu.nl.
Received for publication July 29, 2003. Accepted for publication November 3, 2003.
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M. Berkeveld, P. Langendijk, H. M. G. van Beers-Schreurs, A. P. Koets, M. A. M. Taverne, and J. H. M. Verheijden Postweaning growth check in pigs is markedly reduced by intermittent suckling and extended lactation J Anim Sci, January 1, 2007; 85(1): 258 - 266. [Abstract] [Full Text] [PDF]
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= intermittent suckling, 
= control. The interaction of treatment x feed intake during lactation was not significant (P = 0.06).
