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Perinatal mortality still plagues the swine industry despite improving knowledge on neonatal physiology, nutrition, health and management. Currently, across Europe one out of 5 to 6 piglets born (i.e., 17 to 20%) does not survive from the onset of farrowing until weaning at 3-4 weeks of age. In France, this means that 6.5 million piglets are lost each year. It is clear that these losses have a serious economic impact while being unacceptable for ethical reasons.

Piglet mortality comprises stillbirths and live-born piglets that die before weaning.

Most stillborn piglets die during farrowing as a result of asphyxiation or soon after birth as they have been weakened by the birth process. Overlying is often reported as a major cause of pre-weaning mortality, with this ultimately probably being the final act in a chain of events. In fact, the underlying causes are not fully understood.

In this paper, after a brief survey of the extent of perinatal mortality, we provide new insights on the importance of colostrum for piglet survival. Emphasis is given to the nutritional and immunological roles of colostrum and to insufficient consumption of colostrum as a major underlying cause of postnatal mortality.


Perinatal mortality

In major pig producing countries, total piglet mortality is in the range of 17-20% and is even higher in litters from highly prolific sows. For example (Figure 1), during the past decade in Denmark and France the increase in total number of piglets born per litter from 11.5-11.9 to 13.5-14.0 has resulted in an increase in total mortality from 17-18% to 21-23%. Selection for increased litter size has resulted in more light weight piglets.

The increase in litter size from 11 to 16 increases the proportion of light piglets (<1.0 kg) from 9 to 23%, while the litter is more heterogeneous in birth weight (Quiniou et al., 2002). Therefore, the question arises: to what extent is saving these light piglets of interest? Literature data (Le Dividich et al., 2003) indicate that every 0.1 kg decrease in birth weight translates into 2.3 more days from birth to slaughter.

An important point to note is that within the range of 0.8 to 2.0 kg, birth weight has no marked effect on feed conversion efficiency and carcass lean meat content. It is suggested that a birth weight of 0.90-0.95 kg represents a limit above which saving piglets from modern genotypes is not questionable.




Figure 1. Stillbirths and pre-weaning deaths throughout the past 10 years in Denmark and in France (C.R. Jultved, personal communication; Institut Technique du Porc).



Understanding piglet mortality

Approximately 40 to 48% of total losses are classified as stillbirths. Therefore, reducing both stillbirths and postnatal deaths are of equal importance.


STILLBORN PIGLETS

Stillbirths are usually classified as either pre-partum or intra-partum deaths. Of total stillbirths, 70 to 80% are intra-partum deaths. However, stillbirths are often misdiagnosed and overestimated. They can be halved using an appropriate supervision of farrowing (Holyoake et al., 1995; White et al., 1996).


MORTALITY OF LIVE-BORN PIGLETS

Many surveys have been conducted to examine causes of death of live-born piglets.

However, while the major causes (including overlying) are well-known, underlying mechanisms are less well understood (Edwards, 2002). These mechanisms may depend on at what age pre-weaning losses occur. Most losses (50 to 70%) occur in the first 48 hours after birth. There is increasing evidence that failure to achieve a regular and adequate intake of colostrum (energy) is likely to be a direct and an underlying cause of the majority of deaths (Dycks and Swierstra, 1987; de Passillé and Rushen, 1989; Edwards, 2002; Damm et al., 2005).

Reports by Le Dividich et al. (2006c) and Devillers (2004a) also indicated that, with the exception of some piglets where overlying was the primary cause of death, piglets dying in early life gained several times less weight or consumed much less colostrum and hence less energy than survivors during the first 24 h after birth (Table 1). It is assumed that piglets consuming less colostrum would be less vigorous and less able to compete for productive teats, and hence more prone to die by hypothermia and/ or undernutrition.

The acquisition of insufficient passive immunity is unlikely to be a major factor underlying these early production losses. This is substantiated by the fact that (i) piglet mortality recorded in a SPF herd did not differ from that recorded in production herds (Cariolet et al., 2004), and (ii) piglets born later in the birth order are not at a higher risk of dying while having less immune protection (Le Dividich et al., 2006c). Together, the above suggests that an early and high intake of colostrum (energy) is a major determinant of survival during the early suckling period when most losses occur.


Table 1. Characteristics of piglets dying after birth.


1g/kg birth weight Only litters (35) with at least one death are included in the analysis Le Dividich et al. (unpublished observations)



Importance of colostrum for piglet survival

As most farm animals, the pig is born with low energy reserves (Mellor and Cockburn, 1986) and without immune protection (Gaskins, 1998). The two major roles of colostrum are to provide the piglet with energy for heat production and metabolism and with passive immunity to prevent infections.


ENERGY ROLE OF COLOSTRUM

Colostrum is the first secretion of the mammary gland. Its composition has been recently reviewed by Xu (2003). Briefly, it is characterised by a rapid change to that of milk in the course of a 24-36 h transition period. Compared with milk, colostrum contains more dry matter, protein, bioactive components and less fat and lactose, however its gross energy (GE) remains practically constant over the first 24 h post-partum.

Utilisation of colostral energy by the newborn pig

Colostrum is remarkably well utilised by the piglet (Table 2). Compared with milk, its metabolisability, i.e., the metabolisable energy (ME):gross energy (GE) ratio is however lower (0.93 vs 0.98), while both have a ratio of N retained:N intake of 0.88-0.91. The efficiency of ME utilisation for total energy retention and for energy retained as protein is higher for colostrum than for milk, these being 0.91 vs 0.72 and 0.90 vs 0.56, respectively.

Compared with mature milk, colostrum specifically stimulates muscle protein synthesis (Burrin et al., 1992), with the synthesis being mostly restricted to the myofibrillar protein compartment (Fiorotto et al., 2000). This may contribute to muscle maturation since at birth skeletal muscle contains very few myofibrils (Herpin et al., 2002).


Table 2. Digestibility and utilisation of energy and protein of sow colostrum and milk.


¹Ratio ME:GE
Le Dividich et al. (in press) and Marion and Le Dividich (1999)



Energy requirement of the neonatal pig

As any animal, the neonatal pig needs energy to meet its requirements for maintenance, including thermoregulation, physical activity, and growth. Under the conditions of minimum energy expenditure associated with thermoregulation, feeding (i.e., bottle feeding) and physical activity, energy required for maintenance approximates 275 kJ/kg body weight (BW) (Le Dividich et al., 1994; Marion and Le Dividich, 1999). In practice, however, the piglet experiences a period of cold stress after birth and displays a high physical activity associated with sucking. The energy required for thermoregulation is very high, amounting to 48 kJ/kg BW0.75/°C, a value 2.6 higher than in a weaned pig.

There are no data on the energy cost of sucking activity, but it must be high as illustrated by the energy cost of standing which, expressed per kg BW, amounts to about 105 kJ during the first day after birth (Le Dividich et al., 1994). Based on the body weight gain of surviving piglets, minimum accreted energy averages 300 kJ/kg BW. In practice (Figure 2), the minimum net energy required for survival of a 1.0 kg piglet may be in the range of 900 to 1000 kJ during the first postnatal day (Le Dividich et al., 2006a).


Meeting the energy requirement of the newborn pig

This energy requirement is met by body energy reserves and colostrum since the first suckling usually occurs some 20 min after birth. Body glycogen is the major energy reserve of the newborn pig, ranging between 30 and 38 g/kg BW. However, glycogen stores are rapidly depleted after birth (Elliot and Lodge, 1977). The total amount of fatin the newborn pig is very low, ranging from 10 to 20 g/kg BW. Further, selection of pigs for reduced carcass fatness has resulted in pigs that are leaner at birth (Herpin et al., 1993) and have lighter weight livers and less liver glycogen (Canario et al., 2005).




Figure 2. Energy available at birth and energy requirement (birth-24 h) for survival (kJ net energy/kg birth weight (Le Dividich et al., 2006a).



Overall, available energy derived from body reserves is low, amounting to about 420 kJ/kg BW (Mellor and Cockburn, 1986), which barely meets the energy required for maintenance during the first day of life (Figure 2), thus emphasising the importance of colostrum as a source of energy. Le Dividich et al. (2006a) and Devillers (2004a) estimated that the piglet must consume approximately 160 g colostrum/kg birth weight to survive.


Colostrum production of the sow and consumption by the piglet

Sow colostrum production and its consumption by the piglet result from a close interaction between the sow and her litter because both are dependent on the sow’s ability to produce colostrum, and on that of the piglets to reach and extract colostrum from the udder.

Litter or individual piglet weight gain from birth to 24 h is a very good marker of colostrum produced by the sow or consumed by the piglet (Devillers et al., 2004b, Le Dividich et al., 1997a). A 1 g increase in individual weight between birth and 24 h of life is associated with an increase of 1.6 g of colostrum intake.

The main characteristic of colostrum production by the sow is its very high variability.

In a study involving 48 sows, litter weight gain during the first 24 h after birth averaged 1087 g with a CV of 67% (Le Dividich et al., 2006a). According to Devillers et al.

(2005) total colostrum production in the first 24 h after birth averaged 3570 g. Thompson and Fraser (1988) also found large differences between sows in litter weight gains during the first few days after farrowing, suggesting that there were large differences between sows in the early availability of colostrum and milk. A similar variability has been reported in ewes (Pattinson and Thomas, 2004).

Litter size is a major factor influencing sow milk production. In contrast, litter weight gain (or colostrum production of the sow) is only marginally dependent on litter size (Figure 3). Similarly, Milligan et al. (2001), found no difference in piglet growth during the first 3 days postpartum between litters of 9 and 12 piglets. Consequently, weight gain available per piglet during the first 24 h after birth (Figure 4) decreases by 19 g (i.e., 30 g colostrum) for each additional pig born (Le Dividich et al., 2006a). It is suggested that the sow itself is the main factor accounting for variability in colostrum production.




Figure 3. Litter weight gain from birth to 24 h of age in relation to litter size (Le Dividich et al., 2006a).





Figure 4. Intra-litter average weight gain of piglets from birth to 24 h of life in relation to litter size (From Le Dividich et al., 2006a).



Either failure to produce or a low yield of colostrum might be the consequence of the occurrence of MMA syndrome. However, in studies by Le Dividich et al. (2006a) and Devillers et al. (2005), this syndrome was only detected in one sow. Premature farrowing (110-111 d) reduces colostrum production by 40% (Milon et al., 1983). In practice, however, less than 2% of sows farrow before 112 days (Aumaître et al., 1979). Marked changes in reproductive hormones occur in the periparturient sow. Abnormally high concentrations of progesterone post-farrowing have been associated with delayed lactogenesis and poor initial (birth to 3 days) litter weight gain (de Passillé et al., 1993).

On the other hand, the metabolism of the periparturient sow changes gradually from an anabolic to a catabolic state. From this viewpoint, the colostral phase is characterised by a large export of protein ranging from 200 to 600 g. Due to the habitual low feed intake of the sow soon after parturition, this export probably results in a high rate of sow body protein catabolism even though most colostral immunoglobulins originate from sow plasma.

These comments suggest that changes in reproductive hormones and metabolism must be closely synchronised with parturition. Milk-type ewes are reported to produce significantly more colostrum than meat-type ewes (Pattinson and Thomas, 2004) suggesting that the ability of the ewe to produce colostrum has a genetic component. However, it is not known whether the ability of the sow to produce colostrum has a genetic component.

Similarly, there are no data on the effect of sow nutrition on colostrum production. The rate of colostrum intake in the piglet is initially very high, representing up to 5 to 7% of birth weight in the first two postnatal hours (Fraser and Rushen, 1992), and decreases gradually thereafter.

When an unrestricted supply of colostrum is available, consumption amounts to 450 g/kg BW (Le Dividich et al., 1997), suggesting that the intake capacity of the pig is very high at birth. In sow-reared piglets, colostrum consumption over the first 24 h after birth ranges from 210 to 280 g/kg BW (Le Dividich and Noblet, 1981; Milon et al., 1983; Bland et al., 2003; Devillers et al., 2005).

Within litter, the main factors influencing colostrum consumption are birth weight, birth order and litter size. Piglets heavier at birth are more competitive at the udder than their lighter siblings. Thus colostrum consumption increases by 29 g per 100 g increase in birth weight (Le Dividich et al., 2006a). This, and the fact that 60 to 80% of sows produce enough colostrum to feed adequately a litter of 12-13 piglets (Devillers, 2004a; Le Dividich et al., 2006a), illustrate the importance of litter homogeneity.

Surprisingly, birth order has no effect on BW gain or colostrum intake during the first 24 h after birth (Devillers et al., 2004a; Le Dividich et al., 2006a). Other factors including cold exposure (Le Dividich and Noblet, 1981) and splayed limbs at birth (Devillers et al., 2005) markedly decrease colostrum consumption, while birth hypoxia results in both an increase in the interval between birth and first suckling and a decrease in colostrum consumption (Herpin et al., 1996).


IMMUNOLOGICAL ROLE OF COLOSTRUM

The most important constituents of colostrum are the immunoglobulins (Ig), which provide passive immune protection both after absorption of intact immunoglobulins prior to ‘gut closure’ and at the gut mucosa level throughout lactation. Colostrum also contains leukocytes, which are absorbed by the newborn and produce a measurable immune activity (Tuboly et al., 1988; Williams, 1993) and numerous soluble factors with antimicrobial and/or immunomodulating activity.

Colostrum is characterised by a high concentration of immunoglobulin IgG, while IgA predominates in milk (Klobasa et al., 1987). Thus colostrum is a source of circulating antibody for the newborn, while milk provides local antibody protection for the intestinal mucosa. Concentrations of IgG in colostrum are initially high but drop rapidly during the first 24 h of secretion (Figure 5). This initial concentration of IgG in colostrum varies widely even between sows on the same unit (Bland and Rooke, 1998; Le Dividich et al., 2006c).

Vaccination, parity, season, genotype and section of the udder are also reported to influence colostrum Ig concentrations (Inoue et al., 1980; Klobasa et al., 1985, Bland and Rooke, 1998; Wagstrom et al., 2000; Le Dividich et al., 2006c) but not always (Klobasa and Butler, 1987; Voisin, 2005). Feeding mannan oligosaccharides as Bio-Mos® to sows during late gestation improved levels of Ig of colostrum (Quinn et al., 2001; Newman and Newman, 2001). Nevertheless, variation in colostrum Ig concentration is dominated by sow-to-sow variation.




Figure 5. Pattern of IgG concentration (± sd) of colostrum during the first 36 h after the first piglet was born (Le Dividich et al., 2006c).



Transfer of maternal Ig to the newborn piglet

Because of its six tissue layers, the porcine placenta does not allow transport of Ig from the dam to the foetus. The newborn pig is agammaglobulinemic at birth and colostral Ig are its sole source of antibody. The neonatal intestinal epithelium is capable of absorption of macromolecules, such as Ig, prior to gut closure.

Delivery of intact immunoglobulins to the small intestine is facilitated by the low proteolytic activity of the gastrointestinal tract and the presence of trypsin and chymotrypsin inhibitors in colostrum (Zhou et al., 2003). Absorption of Ig occurs by endocytosis and subsequent transfer across the basolateral membrane of the enterocyte to the circulation.

Gut closure corresponds to the cessation of transfer of IgG to the circulation of the piglet rather than cessation of IgG uptake into the enterocyte from the gut. It takes place as early as 24 h of age in suckling pigs. Factors initiating closure are not well known. However colostrum intake, which specifically stimulates the functional maturation of the gastrointestinal tract (Xu et al., 2002) in the first 24 h of life, is the main factor that induces gut closure. It is relevant to note that colostrum intake in amounts insufficient to maintain piglet body weight has a marked effect on gut closure, suggesting that small quantities of colostrum are sufficient to initiate closure (Le Dividich et al., 2006b).


Major factors influencing the acquisition of passive immunity

The acquisition of passive immunity is closely dependent on both the amount of colostrum consumed and on its IgG content. Absorption of IgG by the gut of the newborn piglet is saturated by increasing amounts of colostrum intake. Recently, Le Dividich et al. (2006b) fed piglets different amounts of colostrum in hourly feeds over the first 27 h of life.

Plasma IgG concentrations reached a plateau in the first 20 h of suckling. A key observation was that IgG concentration obtained at the plateau was dependent on the amount of ingested colostrum, averaging 11, 18 and 26 mg/ml in piglets fed 140, 210, and 280 and 350 g colostrum/kg BW, respectively. The position of the piglet in the birth order is one of the main factors cited, with piglets late in the birth order having access to colostrum of lower IgG concentration and, as a result, reduced plasma IgG concentrations (de Passillé et al., 1988; Bland et al., 2003; Klobasa et al., 2004; Le Dividich et al., 2006c).

Increasing the vitamin A and E content of the diet of the sow has been shown to influence the IgG status of the piglet in several studies (Rooke and Bland, 2002). Similarly feeding ewes with Se including Se from selenized yeast (Sel-Plex®) improves absorption of IgG in lambs (Rock et al., 2001). Yet, the mechanisms by which antioxidants increased efficiency of IgG absorption are unclear and warrant further investigation.


Development of active immunity

According to Klobasa et al. (1981), there is a negative relationship between development of active immunity and the acquisition of passive immunity. Recent observations (Damm et al., 2002; Rooke et al., 2003; Le Dividich et al., 2006c), however, comparing concentrations of plasma IgG at 7 and 28 days of age in sow-suckled piglets, found positive relationships between plasma IgG concentration at or before 7 days of age (when there is little de novo IgG synthesis) and 28 days of age. These more recent observations suggest that there is a positive link between colostrum intake and development of immunity in the piglet.


Is there an optimum level for passive immunity?

Coalson and Lecce (1973) postulate that piglets “can acquire from the dam’s colostrum more than adequate passive antibody in the first hour of nursing” corresponding to ~15- 17 mg IgG/ml serum. On this basis it is calculated that piglets consuming approximately 70 g/kg birth weight of the first colostrum would acquire sufficient passive immune protection.

However, this amount of colostrum is largely insufficient to meet the energy requirement for survival. Therefore, as postulated by Tyler et al. (1990), the consumption of colostrum in adequate amount to provide appropriate immunity to the piglet is not necessarily sufficient to guarantee its survival.

From this, it is tempting to speculate that the level of passive immunity is not a determinant of survival. However, inadequate transfer of maternal antibodies to the newborn piglet may increase susceptibility to infections in the latter part of lactation and after weaning (Varley et al., 1987), while low humoral immunity at weaning may influence post-weaning performance (Edwards and Rooke, 1999). This and the above-mentioned positive relationship between development of active immunity and the acquisition of passive immunity, indicate a high level of passive immunisation is desirable.

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