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Contents

  1. Top of page
  2. Contents
  3. Introduction
  4. Extending the Onset of Follicle Recruitment after Lactation
  5. Post-weaning Altrenogest Use
  6. Intermitted Suckling
  7. Conclusions
  8. Acknowledgements
  9. Conflicts of interest
  10. Author contributions
  11. References

Normally, sows are in anoestrus during lactation and start their new cycle at the day of weaning. Modern hybrid primiparous sows that suckle large numbers of piglets may lose substantial amounts of body reserves during lactation. This compromises follicle development during lactation. As modern sows have short weaning-to-oestrus intervals, these compromised follicles are recruited for ovulation directly after weaning, resulting in lower ovulation rates and lower embryo survival. Postponing or skipping first oestrus after weaning in primiparous sows may help to limit the negative consequences of lactation on subsequent reproduction. Multiparous sows may have very high litter sizes, especially after long lactations as applied in organic sows. These high litter sizes compromise piglet birthweight and survival and subsequent performance. Inducing lactation oestrus in multiparous sows may help to limit litter size and improve piglet survival and performance. This study discusses physiological and reproductive effects of extending the start of a new pregnancy after lactation in primiparous sows and induction of lactation oestrus in multiparous sows. We thereby challenge the view that weaning is an ideal start for the reproductive cycle in modern sows.


Introduction

  1. Top of page
  2. Contents
  3. Introduction
  4. Extending the Onset of Follicle Recruitment after Lactation
  5. Post-weaning Altrenogest Use
  6. Intermitted Suckling
  7. Conclusions
  8. Acknowledgements
  9. Conflicts of interest
  10. Author contributions
  11. References

The modern hyper-prolific sow is another animal than the sow we had some 20–30 years ago. In the 1980s, consequences of primiparous sow lactational weight losses (partly because of mismanagement or low feeding levels) were mainly found in substantially extended intervals from weaning to oestrus. Hughes (1989) showed in a review of research from the 1980s that gilts fed low feeding levels during first lactation had weaning-to-oestrus intervals that averaged 19.3 days. In recent studies, effects of high first lactation weight losses on weaning-to-oestrus intervals are much less pronounced, and more effects are found on ovulation rate and embryo survival, thereby negatively affecting litter size and farrowing rate (Table 1). The current thinking is that in sows with high weight losses during first lactation, ovarian antral follicle development is compromised owing to metabolic intermediates affecting directly and indirectly (via pituitary LH release), follicle growth and follicle quality. In the modern sow with short weaning-to-oestrus intervals, these compromised follicles are recruited at the day of weaning because of the high frequency/low amplitude LH release from the hypothalamus/pituitary system that starts at piglet removal. Compromised follicle development during lactation results in fewer developing follicles and in compromised follicle and oocyte quality. This results in lower ovulation rates and lower embryonic and foetal survival (see Quesnel 2009; for review). In sow genotypes of 20–40 years ago, eventual compromised follicle development during lactation was restored after lactation during long (>15 days) weaning-to-oestrus intervals; therefore, effects on ovulation rate or embryo survival were hardly found (Table 1).

Table 1.   Effects of high or low lactation feed or protein allowance on weaning-to-oestrus interval (WOI), ovulation rate and embryonic survival rate at days 28/35 of pregnancya
ReferenceParityWOI (days)Ovulation rateEmbryo survival (%)
HighLowHighLowHighLow
  1. Adapted from Quesnel 2009.

  2. aHigh ∼ad libitum allowance; Low ∼ 50–75% of ad libitum allowance.

  3. bcDifference between High and Low feed allowance p < 0.05.

  4. dRestriction during last week of a 28-day lactation.

King and Williams 1984a110.8b23.0c14.413.57072
King and Williams 1984b 14.2b17.9c12.312.66261
Kirkwood et al. 198724.3b5.8c18.218.783c68b
Kirkwood et al. 199026.9b8.9c17.617.779c72b
Baidoo et al. 199225.9b7.3c16.417.281c67b
Zak et al. 1997d13.6b5.0c19.9c15.4b88c64b
Zak et al. 199814.2b6.3c14.415.68372
Van Den Brand et al. 200015.15.718.2c16.2b88c64b
Vinsky et al. 200615.35.418.318.279c68b

Another aspect of the modern hyper-prolific sow is the significant increase in litter size because of successful breeding programmes. On Dutch farms, the number of weaned piglets per year has shown an increase of 35% in the last 20 years, reaching an average of 27.9 piglets in 2011 (Kengetallenspiegel Agrovision, 2011). The selection for increased litter size has resulted in a substantial increase in ovulation rate, but has also increased the number of embryonic and foetal deaths because of a limited uterine capacity (reviewed by Kemp et al. 2007) and also decreased birthweights of the surviving foetuses (reviewed by Foxcroft et al. 2009). The latter leads to increased risks for piglet mortality (Quesnel et al. 2008) and has long term-consequences for, for example, lean growth potential (Foxcroft et al. 2009, Foxcroft et al. 2012).

Especially in systems where extended lactation periods are demanded (like organic farming systems), older parity sows may have very high litter sizes and associated piglet mortality. Leenhouwers et al. (2011) showed that organic sows farrow larger litters than conventional sows and have substantial pre-weaning piglet mortality. Wientjes et al. (2012) reported litter sizes of approximately 17.0–18.8 piglets total born and mortality rates of 21–33% in organic sows with an average lactation length of 41 days. These consequences seem related to the fact that these sows become anabolic during lactation, and follicle development and litter size are not compromised by the catabolic state during lactation.

So, on the one hand, the metabolic demands of lactation compromise follicle development and subsequent reproductive performance. This is typically seen in primiparous sows. From a management and physiological point of view, it is the question if weaning should be the start of the new cycle. It might be better to delay the moment of recruitment of follicles for subsequent reproduction by applying skip-a heat or post-weaning use of progesterone analogues. This will be dealt with in sections Extending the Onset of Follicle Recruitment After Lactation and Post-weaning Altrenogest Use of this paper.

On the other hand, in older parity sows (especially those with long lactation periods, such as organic sows), the question arises if litter size could be limited by insemination during lactation. This may prevent very high litter sizes and associated piglet development problems. Moreover, insemination during lactation also provides an opportunity to extend lactation lengths in conventional sows, which improves post-weaning piglet performance (Berkeveld et al. 2007, 2009). A management system that can be used to induce lactational oestrus is intermittent suckling. This system will be discussed in the section Intermitted Suckling of this paper.

Extending the Onset of Follicle Recruitment after Lactation

  1. Top of page
  2. Contents
  3. Introduction
  4. Extending the Onset of Follicle Recruitment after Lactation
  5. Post-weaning Altrenogest Use
  6. Intermitted Suckling
  7. Conclusions
  8. Acknowledgements
  9. Conflicts of interest
  10. Author contributions
  11. References

There are several indications that reproductive performance of young sows can be improved if the interval from weaning to onset of recruitment of follicles for the next pregnancy is extended. Recently, Hoving et al. (2011) confirmed the findings of Tummaruk et al. (2001) that parity 1 and 2 repeat-breeder sows have significantly higher litter sizes (+0.3 and +0.7 for first and second parity sows, respectively) after successful insemination in their second oestrus after weaning. Furthermore, studies in which sows were not inseminated during the first oestrus, but in the second oestrus after weaning, showed substantial increases in litter size (+1.3 to +2.5 piglets) and pregnancy rates (+0 to +15%) (Morrow et al. 1989; Clowes et al. 1994; Vesseur 1997 and Werlang et al. 2011). This improved reproductive performance is largely attributed to higher embryo survival rates (Clowes et al. 1994). The downside of skip-a-heat is that it increases the number of non-productive days by 21 days and that detection of the second oestrus can be a management challenge. Providing a shorter recovery period than a full cycle length by providing a progesterone analogue post-weaning may improve reproductive performance while limiting the effect on non-productive days and preventing the issue of poor detection of second oestrus.

Post-weaning Altrenogest Use

  1. Top of page
  2. Contents
  3. Introduction
  4. Extending the Onset of Follicle Recruitment after Lactation
  5. Post-weaning Altrenogest Use
  6. Intermitted Suckling
  7. Conclusions
  8. Acknowledgements
  9. Conflicts of interest
  10. Author contributions
  11. References

Postponing oestrus after weaning by daily administration of a progesterone analogue (altrenogest) positively affected subsequent ovulation rate (Koutsotheodoros et al. 1998; Patterson et al. 2008), early embryonic development (Martinat-Botté et al. 1995), foetal development (Patterson et al. 2008), farrowing rates (Morrow et al. 1989; Martinat-Botté et al. 1995) and litter size (Morrow et al. 1989, 1990; Martinat-Botté et al. 1995). However, some reports show no or negative effects of altrenogest treatments after weaning (Santos et al. 2004; Werlang et al. 2011). Table 2 summarizes the effects of altrenogest treatments on farrowing rate and litter size. There is considerable variation in dosage, timing of onset and duration of the treatments, which may at least in part explain the variation in responses. To better understand this, we have to understand the physiological effects of the treatment and the variation in physiology of the treated sows.

Table 2.   Reproductive performance after post-weaning altrenogest treatment (Alt) compared to untreated controls
TreatmentParityLact. length (days)Farrowing rateLitter size (n)Reference
StartDose (mg/day)Length (days)ControlAltControlAlt
  1. ns, not significant (p > 0.05).

Before weaning (h)
−481572–71811.8nsPatterson et al. 2008
−4815142–71811.8+1.8 
−2420412089ns11.9nsVan Leeuwen et al. 2011a
−2420812089ns11.9ns 
−24201512089ns11.9+2.5 
−2420812188ns11.9+1.5Van Leeuwen et al. 2011b
−242082–32193ns13.7ns 
After weaning (h)
020313510.5nsBoland 1983
02071351–.5ns 
020712846+228.9nsStevenson et al. 1985
020713510.7nsKirkwood et al. 1986
+320512184–1411.1–1.7Werlang et al. 2011
+320512197–3010.7ns 
+24201211210.3+2.6Koutsotheodoros et al. 1998
+2420512112.3nsFernandez et al. 2005

In Fig. 1, follicle development is shown for sows that were given altrenogest for 8 or 15 days as compared to non-treated controls (adapted from Van Leeuwen et al. 2010). The data show that follicle size increases during a 7-day altrenogest treatment and subsequently stabilizes. Compared to the controls and regardless of dosage or duration of treatment, follicle size at recruitment (withdrawal of altrenogest) is approximately 4.8 mm whereas in weaned control it is approximately 2.9 mm. The increase in follicle size may be related with metabolic effects, as the sows are in an anabolic state post-weaning (Ferguson et al. 2003). Conversely, the effects of altrenogest on follicle development may also be explained by LH secretion during altrenogest treatment. Van Leeuwen et al. (2011c) showed that altrenogest effectively blocks pulsatile LH release during the first 9 h after treatment, but LH pulse release is restored during the last 9 h before the next dose is applied in a daily treatment regime.

image

Figure 1.  Follicle diameter (mean ± SD) during altrenogest treatment and the follicular phase. Day 0 = weaning for the control sows and day of last altrenogest administration for treated sows. Altenogest treatment started the day before weaning: RU 8–15 (8-day treatment at a dose of 15 mg/day), RU 8–20 (8-day treatment at dose of 20 mg/day) and RU 15–15 (15-day treatment at a dose of 15 mg/day) (from Van Leeuwen et al. 2010)

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Studies that investigated consequences of duration of altrenogest treatment for fertility (Table 2) consistently show that 10–14 days of altrenogest treatment resulted in a 1.8–2.6 piglet increase in total litter size compared to non-treated controls. Shorter periods of application give variable or non-significant results. An explanation for treatment duration on reproductive performance can be found in follicle development profiles during altrenogest treatment. Recent results of our group show that on the day of weaning, pulsatile LH release is only blocked for a period of approximately 4 h after altrenogest treatment (Van Leeuwen 2011). This apparently recruits the larger follicles, as is evident from the increase in oestradiol levels. However, while follicle size increases until day 6 after weaning, peripheral oestrogen levels start to decrease approximately 3 days after weaning (Van Leeuwen 2011). One may speculate that the recruited follicles fail to grow out to ovulatory sizes because of insufficient support of LH and therefore become atretic. These follicles may still be present when altrenogest treatment stops at day 5–7 after weaning and may subsequently ovulate, but result in low quality eggs with less potential to form a good quality embryo. At longer periods of altrenogest treatment, these follicles probably have regressed.

Besides the duration of treatment, follicle status at the moment of weaning seems to partly determine the success of the treatment, especially after short treatments of altrenogest. The first indication for this is that sows treated with altrenogest for 8 days, which had small follicles at weaning, showed significantly higher farrowing rates than sows that had large follicles at weaning (Van Leeuwen et al. 2011a). Secondly, split weaning followed by an 8-day altrenogest treatment resulted in larger follicles compared to non-split-weaned controls and also in lower embryo survival (Van Leeuwen et al. 2012). In the studies of Van Leeuwen, altrenogest treatment always started the day before weaning. If altrenogest treatment starts after weaning, this may result in lower subsequent pregnancy rates and litter sizes (Werlang et al. 2011), possibly due to initial stimulation of follicles by weaning-induced LH release. Van Leeuwen et al. (2011b) used altrenogest treatment before weaning to try to control outgrowth of follicles into large-sized categories. However, treatment with 20 or 40 mg altrenogest for three extra days before weaning failed to affect follicle development during lactation.

Based on the above, altrenogest use for periods shorter than 8 days only seems effective if follicle development during lactation is severely compromised, which is expected in sows with a substantial loss of body reserves. Van Leeuwen et al. (2011b) showed that primiparous sows that have low backfat thickness at weaning benefit from a 7-day altrenogest treatment. Longer treatments (e.g. until day 14 after weaning) always give a substantial improvement in litter size in first parity sows (+1.8 piglets in Patterson et al. 2008; +2.5 in Van Leeuwen et al. 2011a) if treatment starts before weaning. In modern hybrid primiparous sows with high lactation weight losses and short weaning-to-oestrus intervals, extending the period from weaning to first ovulation seems a promising route to improve reproductive performance.

Intermitted Suckling

  1. Top of page
  2. Contents
  3. Introduction
  4. Extending the Onset of Follicle Recruitment after Lactation
  5. Post-weaning Altrenogest Use
  6. Intermitted Suckling
  7. Conclusions
  8. Acknowledgements
  9. Conflicts of interest
  10. Author contributions
  11. References

Sows normally remain anoestrus during the lactation period because the pulsatile GnRH/LH release by the hypothalamus/pituitary system is inhibited by endogenous opioid release as a result of the suckling stimulus of the piglets (Armstrong et al. 1988). Owing to the sow’s lactational anoestrus, it is thought to be not economically feasible to increase lactation lengths because it would limit the number of litters per sow per year. Short lactation lengths, however, put a burden on the piglets because they hardly consume solid food in early lactation resulting in weaning problems such as reduced growth, anorexia and diarrhoea (Van Beers-Schreurs et al. 1992). As a solution to this problem, already in the 1970s and 1980s, intermitted suckling (IS) was studied as a management tool to induce lactational oestrus in the sow (see Matte et al. 1992, for review). Intermitted suckling is a system in which the sow and piglets are separated for a number of hours per day during lactation. On the one hand, the system stimulates solid feed intake of the piglets and makes the weaning process more gradual, which reduces the drop in growth at weaning and reduces damage to the gastrointestinal tract (see for extended review Langendijk et al. 2007a). On the other hand, the daily periods of separation may induce lactational oestrus, which makes it, in principle, possible to extend lactation lengths without compromising number of litters per sow per year or may control litter size in older parity sows with extended lactation periods.

The studies in the 1970s and 1980s showed variable responses in the percentage of sows showing oestrus and in synchrony of oestrus (see for review Langendijk et al. 2007a). Potential factors explaining this variation are, for example, stage of lactation that treatment started, duration of daily separation of sows and piglets, use of boar contact or not, parity and breed. Thus, these studies show that lactational oestrus can be induced, but the success rate is dependent on multiple factors. The studies date back quite some years, and little information was available on physiological aspects of lactational oestrus and consequences for subsequent reproduction. Furthermore, sows have changed over the years. One important change is that they have been selected for short weaning-to-oestrus intervals, which suggests that modern breeding sows may be more responsive to regimes like IS.

Langendijk et al. (2007b) showed that at first separation of sows and piglets starting 14 days of lactation, most sows changed from a low frequency/high amplitude LH release pattern to a high frequency/low amplitude LH release pattern typical for weaning. After reuniting sows and piglets after 12 h, the LH pattern was suppressed again but restored after re-separating the sows and piglets after 12 h.

In the recent experiments (see Table 3) with multiparous sows, in which IS started at 14–21 days for 12 h per day, the percentage of sows that responds to IS with lactational oestrus and ovulation varies considerably (22%Kuller et al. 2004; 83%Langendijk et al. 2007b; 92–100%, Gerritsen et al. 2008a; 70–83%Gerritsen et al. 2009; 19–25%Langendijk et al. 2009). By comparing the experiments, the lowest responses were found in experiments in which a TOPIGS20 line was used, and the highest responses were found in experiments in which the TOPIGS40 line was used. Moreover, Gerritsen et al. (2009) showed that when IS started at 21 days of lactation, 83% of the sows responded compared to 70% when IS started at 14 days of lactation. In a field experiment with TOPIGS20 mixed parity sows that were subjected to IS from days 19 or 26 of lactation on average 50–64% of the sows showed lactation oestrus (Soede et al. 2012). However, in that study, primiparous sows were considerably less likely to show oestrus in lactation than older parities (23% vs 68%). In most of these studies, boar contact was not given during lactation, nor was oestrus detection performed with a boar. Boar contact may increase the oestrous response rate to intermittent suckling (Kemp et al. 2005). In an organic farming system, Kongsted and Hermansen (2009) found that boar introduction and grouping of sows at 35 days of lactation induced oestrus in all sows, of which 84% was within 1 week.

Table 3.   Oestrous response in limited nursing regimes
Start (day of lactation)Duration of daily separation (h)Lactation Length (days)ParitySows in oestrus during lactation % (n/N)Timing of lactational oestrus (days after start)Referencea
  1. ND, not determined.

  2. Adapted and extended from Langendijk et al. 2007a).

  3. aAll references: oestrus detection based on Back Pressure Test only.

  4. bBreed Topigs20.

  5. cBreed Topigs40.

41228Multiparous22 (11/49)NDKuller et al. 2004b
13–181220–25Multiparous83 (10/12)<7Langendijk et al. 2007bc
1412∼42Multiparous100 (14/14)4.2 ± 1Gerritsen et al. 2008ac
2 × 692 (12/13)4.9 ± 0.7
1412∼42Multiparous70 (21/30)4.7 ± 0.3Gerritsen et al. 2009c
2183 (19/23)4.4 ± 0.1
1412>21Multiparous25 (4/16)a5.3 ± 0.6aLangendijk et al. 2009b
12 + boar19 (3/16)a5.8 ± 0.9a
191026Mixed50 (20/40)5.0 ± 0.1Soede et al. 2012b
 3564 (27/42)
263561 (25/41) 

Lactational oestrus and ovulation seems to be an all or non-phenomena. Sows that respond to IS show follicle growth rates, time of ovulation after onset of treatment, ovulation rate and pre-ovulatory oestradiol levels that are comparable to that of weaned control sows (Gerritsen et al. 2008a). However, when IS starts early in lactation (14 days), some of the sows may develop cystic ovaries, which is likely explained by sows failing to induce a pre-ovulatory LH surge (Gerritsen 2008). Most non-responding sows seem to show only limited follicular growth after the start of IS, although some non-responders did show increased follicular size, but oestradiol concentrations remained low. These sows apparently were not responsive to FSH or LH stimulation (Langendijk et al. 2009).

In most of the recent studies, sows were inseminated during their lactational oestrus, and effects on progesterone profiles, embryo survival and embryo development could be assessed. When IS continues during early pregnancy, progesterone levels are lower than in weaned controls (Gerritsen et al. 2008a, 2009). This must be related with ongoing lactation, because IS sows that were weaned at ovulation had progesterone levels that were similar to those of conventionally weaned sows. Embryo survival rates in sows in which IS continued during early pregnancy were numerically lower when IS started early in lactation (day 14) or had short separation periods (6 h). Figure 2 (based on Gerritsen et al. 2008b, 2009) shows there are no clear relations between progesterone levels at day 3 of pregnancy and embryo survival, regardless of whether IS was continued during pregnancy or not. Furthermore, a recent study of Soede et al. (2012) showed that litter size and farrowing rate were unaffected by IS, even when sows were lactating in the first 2–9 days of pregnancy. Therefore, continuation of IS during early pregnancy does not seem to reduce performance if IS does not start too early in lactation and separation of sows and piglets is 10–12 h.

image

Figure 2.  Relation between progesterone levels (P4) at 72 h after ovulation and embryo survival at day 23 of pregnancy (Gerritsen et al. 2008b) or day 30 of pregnancy (Gerritsen et al. 2009) of sows submitted to intermitted suckling (IS) and lactating at day 23 (IS day 23) or at day 20 (IS day 30), or weaned control sows (C)

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So, we conclude that in modern sows, depending on breed, parity, time of onset of IS and duration of daily separation, a substantial number of sows can be induced to oestrus and ovulation during lactation, which – upon insemination – results in acceptable pregnancy rates and litter sizes. The benefits of such an approach lie in the opportunity for piglets to gradually adapt to non-milk diets, without compromising the number of litters per year. In systems in which long lactation periods are a prerequisite (like organic farming), this approach may prevent very large litters and the associated high piglet mortality rates. The downside of the approach is the relative unpredictability of the oestrous response rate. Soede et al. (2012) did show that the two-peaked oestrous response of sows occurred very synchronous, either at approximately 5 days after start of IS or at approximately 5 days after final weaning. To ease the management of this system, either almost all sows should respond to IS or the response rate should be predictable. Responsive genotypes, start of treatments around day 21 of lactation and exclusion of first party sows limit variability and ensure good reproductive output. Pharmacological treatments such as PMSG in combination with hCG can also induce follicle development and oestrus during lactation (Armstrong et al. 1999), but not consistently so. Combinations of IS with pharmacological interventions might increase consistency of the system but are ethically debatable. Another aspect that needs further investigation is whether IS should be continued during the whole lactation period. Possibly, a 2-day IS treatment could be sufficient to induce a fertile oestrus. This would facilitate introduction of the system.

Conclusions

  1. Top of page
  2. Contents
  3. Introduction
  4. Extending the Onset of Follicle Recruitment after Lactation
  5. Post-weaning Altrenogest Use
  6. Intermitted Suckling
  7. Conclusions
  8. Acknowledgements
  9. Conflicts of interest
  10. Author contributions
  11. References

This review posed the question if weaning should be the start of the reproductive cycle in the hyper-prolific sow. Extension of the weaning-to-insemination interval by management tools like skip-a-heat or progesterone analogue treatment improves subsequent reproduction in primiparous sows. So, especially for those modern sows that suffer substantial body condition losses during lactation, weaning as the start of the reproductive cycle should be questioned.

The modern hybrid multiparous sow produces many piglets with low birthweights, especially when these sows are used in systems with long lactation periods. This results in high piglet mortality rates and reduced piglet performance. Future production systems in which sows are inseminated during lactation may be a solution.

Acknowledgements

  1. Top of page
  2. Contents
  3. Introduction
  4. Extending the Onset of Follicle Recruitment after Lactation
  5. Post-weaning Altrenogest Use
  6. Intermitted Suckling
  7. Conclusions
  8. Acknowledgements
  9. Conflicts of interest
  10. Author contributions
  11. References

The authors thank postdoc Pieter Langendijk, PhD students Rosemarijn Gerritsen and Jessika van Leeuwen and technicians Bjorge Laurenssen and Rudie Koopmanschap for their contribution to the studies that have been reviewed in this paper.

References

  1. Top of page
  2. Contents
  3. Introduction
  4. Extending the Onset of Follicle Recruitment after Lactation
  5. Post-weaning Altrenogest Use
  6. Intermitted Suckling
  7. Conclusions
  8. Acknowledgements
  9. Conflicts of interest
  10. Author contributions
  11. References
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