Introduction

On commercial farms in the US, annual culling rates often exceed 50 per cent and many sows are replaced before their third or fourth parity, corresponding to potentially the most productive period in the life of a sow (Hoge and Bates, 2011). Indeed, it is estimated that gilts require a minimum of three parities to pay for their replacement cost (Stalder et al., 2003). Issues related to reproduction, such as failure to express oestrus, conceive or farrow (35 per cent), and problems with foot and leg structure (22 per cent), are the most common reasons for young sows leaving the herd (Mote et al., 2009). For pork producers to remain globally competitive, research and technological advances are needed to increase sow longevity and lifetime productivity. There is a critical need to develop and evaluate best management practices for gilt development that maximize future reproductive capacity.

Modern swine production has benefited from a large amount of research focused on management of replacement gilts during grow-finish and around the time of sexual maturity to capture reproductive efficiency. And while management during these phases of production may greatly influence lifetime reproductive performance, it is becoming more evident that management during the suckling and nursery periods may have profound effects as well. Moreover, a growing body of evidence supports the notion that the maternal environment in which a gilt foetus develops plays an important role in the development of the reproductive and other physiologic systems that becomes evident later in life- a phenomenon referred to as “foetal programming”.

The objective of this paper is to provide the reader with a brief introduction to the concept of foetal programming and how management of the foetal, suckling, and nursery pig may ultimately influence reproduction and longevity in mature swine. Although this paper focuses mainly on the female, data in boars is also included if it exists.

Prenatal Development in the Pig and Foetal Programming

Fertilization of ovulated oocytes by sperm cells occurs in the oviduct a few hours after mating. Cell division begins soon after and the fertilized ova pass into the uterus by the third day post-mating. Cell specialization and rearrangement begins by the sixth day.

Eleven day-old embryos begin to show initial signs of attachment to the uterine endometrium, and implantation and formation of the placenta occurs around day 18. By this time, the ectoderm, mesoderm and entoderm are clearly formed within the embryo and cell specialization continues. From the ectoderm arise the skin, mammary and sweat glands, hair and hoofs, the intestinal epithelium, teeth enamel and the nervous system. From the entoderm arise components of the digestive tract, thyroid gland, trachea and lungs. From the mesoderm arise the skeleton, skeletal muscle, connective tissue, blood vessels, blood cells, heart, smooth muscle, adrenal glands, reproductive organs and the kidneys. Shown in Table 1 is a chronology of events in the prenatal growth of swine with emphasis on development of the reproductive system.

The concept of foetal programming was first put forth by Barker (1997) with the central premise of the Barker Hypothesis, being that the exposure of a foetus in utero to various acute or chronic stimuli may elicit a permanent response that impacts physiologic function later in life. When reviewing the chronology of foetal development in the pig described above, it is intuitive that prenatal stressors can affect a variety of physiological systems later in life with the presence or magnitude of the effect dependent on the timing and duration of the prenatal experience (Lay, 2000).

Intrauterine Growth Retardation and Foetal Programming

During the last two decades, management advances and selection for prolificacy have greatly increased litter size in swine, as evidenced in Figure 1. An unintended consequence of the increase in litter size, however, has been an increase in the proportion of low birth weight pigs due to IUGR. Intrauterine growth retardation is defined as impaired growth and development of the mammalian embryo or foetus or its organs during pregnancy. In reality, a number of factors, such as inadequate maternal nutrition or disease, can contribute to IUGR in domestic livestock (Wu et al., 2006). However, from a practical sense, the most important cause of IUGR in swine is probably insufficient uterine capacity, which limits the amount of placental attachment and as a consequence, nutrient exchange between the dam and foetuses (Foxcroft, 2010).

Figure 1. Total number of pigs born, pigs born live, and pigs weaned, per litter in the US from 1990 to 2006
(data from National Animal Health Monitoring System, 2008)

Consequences of IUGR on postnatal growth performance in swine are well-documented. Compared with high birth weight offspring, IUGR newborn pigs have greater rates of pre-weaning mortality and lower postnatal growth rates; at slaughter, low birth weight pigs have less muscle, are fatter, and have poorer meat quality (for review, see Rehfeldt and Kuhn, 2006).

The reproductive effects of IUGR have been less studied. Almeida et al. (2009) reported that at seven days after farrowing, testes weight and the number of Sertoli cells and spermatogonia per testicular cord were lower in low-birth weight (mean weight = 1.17kg) compared to high-birth weight (mean weight = 2.02kg) boars. Because the number of Sertoli cells established before puberty determines adult sperm production, low-birth weight boars may have poorer reproductive performance at sexual maturity. Preliminary evidence from the author’s laboratory supports this hypothesis.

In their study (Estienne and Harper, 2010b), the birth weights of boars successfully trained for semen collection (mean weight = 1.67kg; n=29) were significantly greater than birth weights of un-trainable boars (mean weight = 1.29kg; n=8), although body weights at training were similar between groups. Semen was collected from trained boars weekly for eight weeks and sperm concentration and total sperm per ejaculate were positively correlated with birth weight in these individuals. Moreover, a subset of boars classified as light weight (less than 1.36kg; n=7) had lower sperm concentrations and total sperm per ejaculate than boars classified as high-birth weight (greater than 1.86kg; n=9). Thus, the results are consistent with the concept that birth weight is a predetermining factor impacting reproductive potential in adult boars.

In gilts, Da Silva-Buttkus et al. (2003) reported that at birth, runt pigs (mean weight = 0.7kg) had more primordial follicles but fewer primary and secondary follicles than normal weight littermates (mean weight = 1.5kg), indicating the IUGR delayed follicular development.

The author recently reported on a pilot study examining age at puberty in gilts farrowed in litters with various average birth weights (Estienne, 2012). Age at puberty, defined as the first standing oestrus in the presence of a mature boar, was determined for two to seven gilts from each of 33 litters that had a range of average pig birth weight of 1.13 to 1.98kg. Age at puberty was negatively correlated (r=-0.43; P<0.01) with average pig birth weight.

Foxcroft (2010) suggested that differences among litters is the major source of variation in pig birth weight in populations of mature sows producing between 10 and 15 pigs per litter, and the low birth weight phenotype was repeatable.

Management of the Foetal Pig and Future Reproduction

Relatively little research has been conducted to determine the effects of sow management and husbandry on foetal programming. Most studies conducted to date have examined the effects of experimentally subjecting pregnant sows to “stress” conditions on the future performance of offspring, with a postulate being that at least some foetal programming occurs as a consequence of enhanced secretion of maternal cortisol.

Haussmann et al. (2000) demonstrated that stress caused by restraint or injection of adrenocorticotropin (ACTH) to stimulate cortisol secretion in the pregnant sow, resulted in offspring with altered endocrine profiles and adrenal gland morphology, enhanced cortisol secretion in response to stress, and a decreased ability to heal a wound. There was a tendency for control pigs to have greater birth weights than pigs farrowed by sows treated with ACTH.

In terms of reproduction, boars born to dams that received ACTH during gestation, had similar birth weights but smaller ano-genital distances than boars farrowed by control sows (Lay et al., 2008).

O’Gorman et al. (2007) conducted a study during which sows were allocated to one of two treatment groups: control or stressed. Stressed sows were subjected to daily restraint for five minutes during weeks 12 to 16 of gestation. Female offspring were checked for oestrus twice daily beginning at 122 days of age. Age at first oestrus was significantly delayed in gilts farrowed by stressed sows (around 172 days) compared to gilts farrowed by control females (around 158 days). Potential involvement of the adipocyte-produced hormone leptin was suggested by the finding that leptin receptor mRNA in the choroid plexus was greater in pubertal gilts from control sows compared to gilts from stressed sows.

A recent experiment from the author’s laboratory compared growth performance and reproductive characteristics of gilts farrowed by sows that were kept in individual crates throughout gestation, group pens throughout gestation, or individual crates for the first 30 days post-mating and then group pens for the remainder of pregnancy (Estienne and Harper, 2010a). Pig birth weights, and growth performance prior to weaning and during the nursery phase of production were similar among treatments but during the last four weeks of the grow-finish period, body weights of gilts farrowed by females housed in crates throughout gestation were greater than body weights of gilts in the other two groups. Also, the efficiency of feed conversion was greatest, and the amount of ultrasonically determined last-rib backfat the least, in gilts farrowed by females housed in crates throughout gestation.

Consistent with these findings, Foxcroft et al. (2006) reviewed the scientific literature and concluded that environmental influences on embryonic and foetal development most often express themselves in the late grower or finisher stages of production. Interestingly, in the Virginia study, fewer gilts farrowed by females kept in crates throughout gestation reached puberty by 165 days of age than other two groups. Although the mechanisms responsible for these effects were not addressed, maternal cortisol secretion could be involved. Circulating cortisol levels were greater for gilts kept in individual gestation crates compared with group-penned individuals (Estienne et al., 2006).

Management of the Suckling Pig and Future Reproduction

Nelson and Robison (1976), reported that at day 25 post-mating, gilts that were raised in litters of six pigs prior to weaning had more corpora lutea (an indication of ovulation rate) and embryos, than did gilts raised in litters of 12 pigs. Moreover, through three parities, sows raised in litters of seven pigs or less were less likely to be culled and had higher farrowing rates and larger litters than sows raised in litters of 10 or more pigs; boars raised in litters of six pigs or less reached puberty sooner and produced more sperm cells per ejaculate compared with boars raised in litters of nine pigs or more (Flowers, 2008). This suggests that lactation litter size can impose some type of stress that negatively impacts future reproduction of the suckling pigs.

Management of the Nursery Pig and Future Reproduction

There are many potential environmental stressors in intensively managed swine operations and clinical signs of these stressors are often easily detected.

For example, temperatures below the thermo-neutral zone cause pigs to huddle and shiver. Inadequately ventilated barns may cause coughing indicative of respiratory distress and animals housed in pens with poor flooring may display lameness.

A stressor that is often operative but which may not have easily discernible consequences, is stress due to inadequate floor space. For example, the percentage of gilts reaching puberty at less than 285 days of age tended to be greater for females allowed adequate floor space during the grower and finisher phases of production (0.56 and 0.72 square metres, respectively) than gilts allowed less floor space (0.28 and 0.56 square metres, respectively) (Lindemann et al., 1988).

Kuhlers et al. (1985) placed grower gilts in pens of eight or 16 animals each and the females reared in the smaller groups ultimately farrowed one more pig per litter than did gilts reared in the larger groups. More recently, Young et al. (2008) conducted an experiment during which 1,257 gilts at 75 days of age and 38kg body weight were each given 0.76 or 1.12 square metres of floor space during rearing. Space allowance in rearing did not affect total pigs produced over three parities or removal rate. However, a greater percentage of gilts attained puberty and attained puberty at a younger age, when given the greater amount.

It is reasonable to speculate that the immediate post-weaning environment, i.e. nursery phase of production, in which gilts are raised can ultimately influence reproduction as well. Floor space allowance during the nursery phase of production impacts growth performance, as demonstrated by Cho et al. (2010) who allotted weaned barrows and gilts to three treatments: I. six pigs per nursery pen and 0.5 square metres of floor space per pig; II. 12 pigs per pen and 0.25 square metres per pig, and III. six pigs per pen and 0.25 square metres per pig. Crowding significantly reduced average daily gain in both sexes during the six-week trial.

Effects of nursery floor space allowance and stocking density on subsequent reproduction in gilts has not been adequately studied. However, gilts kept in pens of 16 during a five-week nursery period subsequently farrowed 1.25 live pigs less during parity 1 and 3.5 live pigs less during parity 2 than gilts kept in pens of eight in the nursery (Figure 2).

Figure 2. First and second litter size for sows that were kept in pens of eight or 16 gilts each during the nursery phase of production.
For both parities, the number of pigs born alive was greater (P<0.01) for females previously housed in the less crowded conditions.
(M.D. Lindemann, personal communication)

In a study by Kim et al. (2008), 68 weaned gilts were allotted to: I. six pigs per nursery pen with 0.5 square metres of floor space per pig; II. nine pigs per pen with 0.33 square metres per pig; III. 12 pigs with 0.25 square metres per pig, and IV. six pigs with 0.25 square metres per pig. In the first parity, litter size was largely unaffected by treatments. However, in the second parity, total litter size (10.86, 10.38, 8.79 and 8.67; linear effect for treatments I to III, P=0.24) and pigs born live (8.43, 9.38, 7.79 and 7.67; quadratic effect for treatments I to III, P=0.30) were numerically decreased by crowding stress.

These studies were limited in terms of the number of animals employed but nevertheless provide solid preliminary evidence consistent with the concept that space allocation during the nursery phase of production affects future gilt reproductive performance. Further, they demonstrate that the potential detriment increases in parity 2 after the female has experienced the normal rigors of the parity 1 lactation. These effects, however, must be substantiated in a commercial setting, using large numbers of experimental animals.

Summary and Conclusions

The research summarized herein provides evidence that stimuli to which gilts are exposed in utero and early in life may result in developmental adaptations that have lifelong physiological consequences. The current trend of increasing litter size in swine has concomitantly increased the proportion of low-birth weight pigs due to inadequate uterine capacity. Pigs born with the IUGR phenotype have poorer reproductive performance compared to normal bodyweight pigs.

Currently, there is a need for the development of strategies and techniques to “rescue” low-birth weight pigs. For example, treatment of gilts with porcine growth hormone from day 10 to day 27 of gestation increased total fibre number in semi-tendinosus muscle in low-birth weight pigs that were ultimately farrowed (Rehfeldt and Kuhn, 2006).

Foxcroft (2010) suggested two strategies to address variation in litter average birth weight and postnatal performance including: 1)segregated management of litters based on birth weight phenotype, and 2) nutritional strategies in gestation and lactation and interventions in the farrowing house targeted at low birth weight phenotypes. Subjecting sows to treatments that result in stimulation of the hypothalamic-pituitary-adrenal axis and the attendant increase in cortisol secretion may have long-term consequences on the foetus.

Although the mechanism for these effects must be ascertained, it is not, in all likelihood, due solely to changes in pig birth weight. Given the evidence that experimentally induced hyper-secretion of cortisol in gestating sows may have negative effects on postnatal performance of pigs, producers should strive to minimize factors that result in stress to the breeding herd.

Finally, stress experienced by gilts in large litters during the suckling period or in crowded conditions during the nursery phase of production can not only impact growth performance immediately but may also have long-term consequences. Research will continue to identify prenatal or early-in-life stressors and to develop management strategies for mitigating adverse effects on reproduction and increasing sow longevity.

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