Human Milk: Composition, Clinical Benefits and Future Opportunities. Группа авторов

and, most recently, 3D ultrasound [8]. All such methods were unambiguous in observing peristaltic tongue movements (PTMs), on the basis of which it was assumed that they played a role in expressing milk from the breast; we have since confirmed that this collective view is essentially correct [9, 10].

Two studies, principally Eishima [7] and Geddes et al. [11], identified a novel feature of infant feeding, involving a localized drawing down of the central region of the tongue, adjacent to the nipple tip. To this movement was imputed the ability to generate increased (added) suction at the nipple surface, claimed to play a predominant role in milk extraction from the breast; subsequent studies have extended and elaborated on these claims [12–14]. We can similarly confirm that these authors are correct in their observations, and in their proposition that the action aids milk extraction; nonetheless, some vital caveats need to be considered when evaluating the full validity of their claims.

      What We Already Know

      Seven principal forces are present and active during breastfeeding, the first three affect the pressure of milk within the breast; all but one is active in milk transfer, while one plays a key role in retaining the breast within the baby’s mouth.

      (1) Atmospheric pressure is an important force in the process, although it is eclipsed by the positive pressure created by (2) the mother’s “let-down” or milk ejection reflex (MER). The MER creates phasic (intermittent) increases in positive pressure in the milk held within the breast, while also causing the milk ducts to dilate, so providing less resistance to the flow of milk to the nipple surface. Because breastfeeding is such a highly dynamic form of milk extraction, atmospheric pressure is more likely to play a role in milk extraction by breast pump (being less dynamic). These two forces constitute one side of an active pressure gradient.

      A less obvious process creating positive pressure in the breast is (3) the compressive pressure of the baby’s lips against the breast, pressing cyclically on the breast surface surrounding the ducts during feeding. Its role in milk extraction is not dissimilar to that of the flanged cone of a breast pump, pressing against the breast; an awareness of this subsidiary process has largely arisen from studies of breast pumping. A well-attached baby, making a wide flange at the breast, will capitalize on this, while also taking a large mouthful of breast tissue.

      Within the baby’s mouth, creating the other side of the active pressure gradient, is (4) intense negative suction pressure created by the baby cyclically lowering the rear surface of its tongue. This is responsible for generating baseline suction pressure which both draws the breast into the baby’s mouth and retains it throughout the feed. This force is unstable, however, as any milk issuing from the breast into the oral cavity negates it, making it necessary for it to be reapplied in a cyclical manner throughout feeding.

      These four principal forces are necessary and sufficient for a breast pump (electric or manual) to create adequate milk removal from the breast. The cyclical application of negative suction pressure at the nipple surface (aided by the three other factors) is adequate for sustaining milk collection from the breast.

      The two unique features which the baby brings to the process are: (5) the compressive action of the baby’s jaws (and gums), and (6) PTMs applying retrograde waves of positive pressure to the underside of nipple surface. The peristaltic action of the baby’s tongue is obligate, playing the primary role in both milk transfer and expelling the milk bolus into the oro-pharynx for swallowing. The action of these two forces alone is not dissimilar to hand expression of the breast, which requires no negative suction pressure to remove milk. The fingers press into the breast at the base of the ducts, in a similar action to the baby’s jaws, and the opposed fingers are drawn towards the nipple end to express milk; this emulates the peristaltic action of the baby’s tongue. The role of the baby’s jaws should never be overlooked, as they effectively “gate” the release of milk, letting it enter the milk ducts, lying within the nipple/breast teat complex, in packaged bundles, rather than as a continuous outflow of milk from the breast.

Accordingly, there are two sets of forces – the first four alone are capable of milk extraction, and are employed specifically when a breast pump is used to extract milk. The next two forces alone are capable of milk expression from the breast, in the absence of the other forces. They are akin to “pump extraction” and “hand expression” and use entirely different modes of action, yet both are effective for expressing/extracting milk from the breast (just as “hand milking” and “machine milking” are equally effective with dairy animals). The essential beauty of mammalian suckling is that these separate forces combine in the baby’s mouth, and are most likely to be acting synergistically to remove milk in the most efficient way possible (the same is true of feeding by most dairy animals studied (sheep and goats) [15], and by pigs [16]).

Fig. 1. Example of output from sensors. Right: 60 s selection of the signals acquired during an experimental test. Left: zoom of a single burst and extracted parameters [17].

Two of these forces are well illustrated in a recent study by Grassi et al. [17] who fitted two sensors to a pacifier, one monitoring positive pressure from the jaws and gums, and one measuring negative suction pressure within the oral cavity. Their figure (Fig. 1) shows the negative suction profile and positive pressure profile superimposed on each other, illustrating the relative scale and timing of these pressure forces at play during sucking on a pacifier.

      Negative pressure (–150 to –200 mbar) is some 3–4 times greater in intensity than positive pressure (50 mbar). Negative suction pressure starts being generated while the jaws are relaxed/open, thereby ensuring the “teat” (or nipple/breast complex) is drawn into the oral cavity. Positive pressure by the jaws causes the gums to clamp on the base of the “teat,” thereby retaining it in the mouth. Shortly after jaw pressure reaches its peak, and starts to decline, negative pressure begins being regenerated. This is caused by lowering of the rear surface of the tongue, which, itself, is the end phase of the peristaltic wave as it completes its traverse of the oral cavity.

      This is a key demonstration that even when feeding on an artificial teat (pacifier), the same natural forces are at play, despite them no longer having the normal function they would during breastfeeding.

      The final force (7) is localized drawing down of the tongue surface adjacent to the nipple tip [7], the existence of which, and its role in milk removal, has only been confirmed in the past decade [11]. Unlike PTMs, this action is not obligate, but appears more facultative or opportunistic, only being superimposed on PTMs for a proportion of the time spent sucking. These localized depressions of the tongue surface are deployed at particular times during most feeds. Nonetheless, while they are ubiquitous, they cannot exist in isolation from PTMs; recent evidence (below) indicates they are generated by the same process. Their effect is to produce increased or added suction pressure local to the nipple surface; in all likelihood, this facilitates or enhances milk extraction. The phrase extractive tongue depressions (ETDs) will be used to refer to these, in view