Lactation in motion: The sow-litter barn dance

Assume for a moment that you had never been to a dance before. If you walked into one, initially you might be overwhelmed by what would seem to be a chaos of motion. There is a constant movement and changing of positions. After further observation, you might recognize that there was a pattern to the movement, a synchrony of motion, even a coordination among dancing partners. Watching carefully, you might also come to recognize that an enhanced level of performance is achieved when there is an effective synergy between dancing partners. The constant motion and apparent chaos you noticed at the start has been revealed as a highly structured and proficient activity.

The sow's ability to lactate is a critical factor in the successful rearing of her litter (Boyd and Kensinger, 1998). Lactation is a dynamic activity involving the sow and her litter. Successful lactation involves a complex, coordinated interplay between the behavior and physiology of the sow and that of her pigs. The nature of this interplay is constantly changing from the birth of the first pig through to the removal of the litter at weaning, and even beyond. This overview of lactation in swine focuses on two levels of this sow-litter dance, the relationship between the sow and her litter, and the interplay between an individual pig and the mammary gland it suckles. The consequences of a successful lactation dance are considered, as well as how an unsuccessful performance may occur. 

When the pregnant gilt or sow enters the farrowing barn several days prior to the expected farrowing date, the intent is to acclimate her to that environment prior to undergoing the stresses associated with farrowing. At this time, her mammary gland is in the late stages of a rapid period of growth. Most of the increase in mass of the mammary gland occurs in the last third of pregnancy (Ji et al. 2006). This growth is driven by the stimulation of the gland by several mammogenic hormones (hormones that stimulate mammary growth), especially estrogen from the placenta, progesterone and relaxin from the ovary, and prolactin and growth hormone from the pituitary. While all of her mammary glands are stimulated to grow, typically the middle glands achieve the greatest mass prior to farrowing, while the posterior glands are the smallest.

In the period immediately prior to farrowing the gland starts producing the antibody-rich colostrum. However, ejection of colostrum from the gland does not occur until farrowing. This is in contrast to some other domestic farm species such as the dairy cow where colostrum-like secretions can be collected from the udder even several days prior to calving. In the sow, colostrum can be removed more easily from the gland starting with the farrowing process when there is an increased release of oxytocin from the posterior pituitary in association with the birthing process. Oxytocin also is the milk ejection hormone, and plays an important role in the sow-pig interaction during lactation, as discussed below.

At the time of farrowing, each gland undergoes the twostage process of lactogenesis (initiation of lactation). The initial stage involves cellular development of the milk synthesis apparatus, expression of genes associated with synthesis of milk components (milk proteins, fat and lactose), and secretion of a limited amount of the milk components. This stage overlaps or is simultaneous with the formation of colostrum in the gland. In the sow, this initial stage of lactogenesis seems to only be occurring within a very few days prior to farrowing. The second stage of lactogenesis is referred to as copious milk secretion. This involves a large scale expression of all genes associated with milk synthesis and rapid secretion of large quantities of all milk components. In the sow, this second phase of lactogenesis is initiated shortly after farrowing.

Colostrum formation, particularly transport of immunoglobulins into the colostrum, is thought to be regulated by hormones including glucocorticoids from the adrenal glands. Glucocorticoids also are part of the complex of hormones that regulate lactogenesis. However, the major hormone involved in regulating lactogenesis is prolactin from the anterior pituitary. The surge of prolactin secretion associated with parturition results in a decrease in the transcellular transport of immunoglobulins in the mammary gland, marking the beginning of the decline in active colostrum formation. In the sow, the peripartum surge of prolactin secretion starts a couple of days prior to farrowing and continues for several days post-farrowing (Devillers et al. 2004), stimulating the gland to switch from formation and accumulation of colostrum to synthesis and secretion of milk components. Anything that inhibits prolactin secretion around the time of farrowing can inhibit lactation. 

In terms of lactation, the sow is ready to engage with the pigs once they start suckling. Each of her mammary glands has developed structurally and functionally to the point of producing some colostrum. From that time forward, changes in the functioning of each gland will be determined by whether and how much it is suckled. In contrast, the new born pigs take time to engage effectively with the sow. Pigs are born in a relatively mature state compared with many other species. They can fairly quickly move around after birth, allowing them to act on their strong behavioral drive to suckle (Brooks and Burke, 1998).

For some swine breeds, especially those most often used in the US swine industry, pigs establish a well-defined teat order or teat preference. This strong teat order has a number of implications in terms of the mammary biology of the sow. Generally each pig will suckle from only one gland, although there are some pigs that are able to maintain some lactation function in two adjacent glands. Glands that are not suckled undergo regression (discussed below). If for any reason a pig is removed from the litter, the gland that pig suckled typically will not be adopted by another pig in the litter, rather the gland will undergo regression. In situations where part of the litter is weaned and the remaining pigs are left with the sow, the remaining pigs will not relocate to another gland, even if that was a high-producing gland. 

The process of pigs settling on a specific gland for suckling, thereby establishing teat order, continues for several hours post-farrowing. The periods of milk ejection gradually occur at increasingly regular intervals. By approximately 11 to 12 hours post-farrowing the litter and sow have synchronized their respective behaviors and interact in a coordinated, repeatable manner. Teat order has been established so that the relationship among pigs is mostly stabilized. The sow has started to let down her milk at fairly regular intervals, and the pigs have learned to pick up on the sow's cues when she is going to let down her milk. At this point, the suckling dance between the sow and her litter occurs at intervals ranging from about 45 to over 60 minutes. In addition, the sow's mammary gland is refilling with milk between nursings, while the ingested milk in the pig's gastrointestinal tract is slowly digesting, making room for the next feeding.

It is also important to consider the dynamic interplay of the pig and the gland it suckles. Each gland responds to stimuli carried in the blood, such as the lactogenic hormone, prolactin. Prolactin secretion from the pituitary is stimulated by the pigs nuzzling the mammary glands and by their suckling action on the teats (Algers et al. 1991). In addition, each gland responds to local inhibitory factors which are produced within the gland (Knight et al. 1998). The mammary epithelial cells secrete an inhibitory factor, referred to as feedback inhibitor of lactation, as part of the normal cellular mechanism of milk secretion. As the feedback inhibitor accumulates in the alveolar lumen, it has an inhibitory effect on further milk secretion by the cells. When the pig removes the milk during suckling the negative effect of the feedback inhibitor is also removed, allowing milk synthesis and secretion to be stimulated again by the suckling-induced elevated prolactin concentrations. Maintenance of lactation in each gland is determined by the repeated removal of the milk produced by that gland. Each pig is different in its demand for milk from its preferred gland and each gland is independent from the other glands in its responsiveness to the pig's demands.

As a consequence of this synergy and coordination, the pig and the gland it suckles can be thought of as an interdependent, functionally-linked unit. The more milk removed by the pig, the more the gland is stimulated to produce more milk and to grow, and the more the pig is stimulated to grow. The larger the pig, the more demanding it is for milk from the gland and perhaps the more effective it is at removing milk from the gland. This relationship results in a positive and statistically significant correlation between growth rate of the pig and size of the mammary gland the pig is suckling. Pigs suckling heavier glands gain faster than pigs suckling lighter glands, although there is substantial variability among individual sows. 

A climax in the lactation dance occurs each time the pigs are physically interacting with the mammary gland during suckling. Oxytocin release from the pituitary occurs in response to physical manipulation of the mammary gland and teats. The sow has a high threshold to stimulation to release oxytocin from her pituitary. This explains the extensive nuzzling of the udder by the pigs leading up to milk ejection in an effort to stimulate milk ejection, as well as the short duration of actual milk ejection.

While this important event, milk ejection, occurs multiple times daily, it typically is accompanied by an intricate and highly coordinated behavioral sequence involving activity of the sow and of the litter (Brooks and Burke, 1998). Typically the sow initiates a period of grunting that alerts the pigs. She lies on her side exposing the udder. While the sow continues her rhythmic grunting, the pigs assemble at the udder, nuzzling the glands and sucking on the teats. Release of oxytocin from the pituitary occurs approximately at the point where the sow increases the rate of grunting. Milk ejection starts roughly 25-30 seconds later, however it only lasts for about 10-15 seconds. It is only during this short period of milk ejection that the pigs can remove milk from the gland. During the period of milk ejection, pigs will be focused on sucking their preferred gland and will not be moving about or engaging in any other activity than sucking on the teat. The end of milk ejection is evident when the pigs release the teat and start testing other teats. They will continue sucking the teats and nuzzling the udder for several minutes after the nursing event. In addition to stimulating release of oxytocin, the nuzzling of the udder both before and after milk ejection stimulates continued release of prolactin from the anterior pituitary, which stimulates the refilling of the gland.

The period between sucklings is when the gland refills with milk. Typically when the pig successfully suckles at milk ejection most of the milk is removed from the gland. We can consider the gland as "empty" after each suckling. Synthesis of milk to refill the gland after each suckling is nearly complete by about 35 minutes after emptying of the gland, with only an additional 25% accumulated within the subsequent hour (Spinka et al., 1997). As milk accumulates in the gland, the inhibitory factor also accumulates, gradually slowing the rate of further milk secretion until no additional milk is secreted from the mammary epithelial cells. Suckling during milk ejection not only removes the milk, but also removes the inhibitory factor 

Total milk production by the sow and mammary growth during lactation are affected by many factors, including nutrition, environment, breed, stage of lactation, and parity (King, 2000; Hurley, 2001). Individual mammary glands also differ in their production ability according to teat location (Dyck et al. 1987). For the purposes of this discussion, we will focus on the concept of suckling intensity and how that affects total milk production by the sow. Because of the strong teat order of the pigs, the larger the litter size, the more glands of the sow are maintained in a functional, milk secreting state, and the more total milk will be produced by the sow (litter size is positively correlated with total milk production). This also means the larger the litter size the greater the total amount of mammary gland mass that develops on the sow during lactation. However, the increment of increase in total mammary mass or total milk production decreases with each additional pig in the litter. That is, the larger the litter size the lower amount of milk received per pig.

Suckling intensity also is related to interval between sucklings, or how often the sow is suckled. Suckling intervals between 35 and 50 minutes, resulting in milk removal about 30 times per day, offers maximal daily production of milk. Sows that nurse every 45 minutes vs those that nurse every 60 minutes, will produce less milk per nursing, but more total milk in a day. Because the duration of milk ejection is very short and the process of milk ejection is negatively impacted by stress, some sucklings may be non-nutritive. The sow and litter go through the normal behavioral sequence of the nursing, but milk ejection, and therefore milk removal, does not occur 

The concept of the inhibitory factor accumulating in a gland along with accumulation of the milk means that the functioning of each gland will differ depending on whether the gland is suckled. When milk is not regularly removed from a gland the inhibitory factor gradually stops milk secretion in that gland. Lactation function is maintained only in those glands actively suckled by the pigs. Those glands that are not suckled undergo a process of involution. At the beginning of lactation, the milk secretion function of nonsuckled glands is irreversibly lost for that lactation cycle within 3 days of farrowing (Theil et al. 2005; 2006). At weaning, with the complete absence of suckling and milk removal, the mammary gland undergoes extensive regression and remodeling for about a week or more before reaching a regressed state that will be maintained until mammary development is initiated during the subsequent pregnancy (Ford et al., 2003). 

Coordination of the behaviors of the sow and the pigs in her litter are critical for a successful outcome to her lactation. This is underscored when considering that milk ejection only occurs at intervals and only for a matter of seconds. Anything that disrupts the coordinated behaviors of the sow or litter will negatively impact the success of the pigs receiving milk during the very short milk ejection period. Pigs that are not able to participate in the suckling processes, for any reason, will miss a meal. If that persists, they will quickly become weakened and unable to participate in further feedings. From the sow's perspective, stressors of any type in the farrowing barn may compromise her ability to let down her milk. Stress affects milk ejection at several levels, impacting the release of oxytocin from the pituitary and inhibiting the responsiveness of the mammary gland to oxytocin. A sow's responsiveness to stressors may impact her ability to sustain regular milk ejection.

Considering the relationship between suckling of a mammary gland and its functioning during lactation, a question that arises is whether the lactation history of a gland has any impact on that gland in a subsequent lactation. Recent evidence indicates that glands that are suckled in a gilt's first lactation will produce more milk and have a greater development in her second lactation than glands that were not suckled during the first lactation (Farmer et al. 2012). This indicates that there is some level of carry-over from the gland development that occurs in one lactation to the next. At this time, it is not known whether such a carryover would occur between the second and subsequent lactations; nor is it known if a gland not suckled in the first lactation, but suckled in the second lactation, would respond with further development if suckled in the subsequent lactation. It is worthwhile to note that much of the research on mammary biology of swine has been done on first parity gilts, with considerably less information available on multiparous sows.

Another implication of the effect of non-removal of milk from a gland relates to opportunities for successful cross fostering of pigs. Optimal success in cross fostering a pig onto a nonsuckled gland may be achieved on day 1 of lactation, with limited success on day 2, and no success by day 3. Even if a gland is not suckled during day one after farrowing and subsequently a pig suckles that gland, the gland will not produce to the level it might have if regular suckling began sooner (Theil et al. 2005; 2006). If a pig dies during lactation, the gland it is suckling will also undergo a regression similar to the involution process occurring at weaning. Efforts to successfully foster another pig onto that gland must be achieved rapidly before the regression process becomes established. 

Successful lactation of a sow involves a highly coordinated interplay between the behavior and physiology of the sow and her litter. This interplay occurs to a great extent at the point of physical interaction of the individual pigs and the mammary glands they suckle. The nature of this interplay is continually changing from the time of farrowing to weaning the litter. While there are many other factors that go into a successful lactation of a sow, ultimately it is the highly controlled milk ejection process of the sow, coordinated with the physical removal of milk from the gland by the pig, that determines whether and how much the pig grows, as well as how much the gland continues to produce milk. This inspired performance by the sow and her litter occurs many times daily in the farrowing barn. Our own careful observation of the sow-litter dance may help us better understand those factors that would compromise their performance. 

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