Abnormal Nutritive Sucking as an Indicator of Neonatal Brain Injury

Abstract

A term neonate is born with the ability to suck; this neuronal network is already formed and functional by 28 weeks gestational age and continues to evolve into adulthood. Because of the necessity of acquiring nutrition, the complexity of the neuronal network needed to suck, and neuroplasticity in infancy, the skill of sucking has the unique ability to give insight into areas of the brain that may be damaged either during or before birth. Interpretation of the behaviors during sucking shows promise in guiding therapies and how to potentially repair the damage early in life, when neuroplasticity is high. Sucking requires coordinated suck-swallow-breathe actions and is classified into two basic types, nutritive and non-nutritive. Each type of suck has particular characteristics that can be measured and used to learn about the infant's neuronal circuitry. Basic sucking and swallowing are present in embryos and further develop to incorporate breathing ex utero. Due to the rhythmic nature of the suck-swallow-breathe process, these motor functions are controlled by central pattern generators. The coordination of swallowing, breathing, and sucking is an enormously complex sensorimotor process. Because of this complexity, brain injury before birth can have an effect on these sucking patterns. Clinical assessments allow evaluators to score the oral-motor pattern, however, they remain ultimately subjective. Thus, clinicians are in need of objective measures to identify the specific area of deficit in the sucking pattern of each infant to tailor therapies to their specific needs. Therapeutic approaches involve pacifiers, cheek/chin support, tactile, oral kinesthetic, auditory, vestibular, and/or visual sensorimotor inputs. These therapies are performed to train the infant to suck appropriately using these subjective assessments along with the experience of the therapist (usually a speech therapist), but newer, more objective measures are coming along. Recent studies have correlated pathological sucking patterns with neuroimaging data to get a map of the affected brain regions to better inform therapies. The purpose of this review is to provide a broad scope synopsis of the research field of infant nutritive and non-nutritive feeding, their underlying neurophysiology, and relationship of abnormal activity with brain injury in preterm and term infants.

Keywords: brain injury; neuroimaging; non-nutritive; nutritive; sucking.

Figure 1

Waveform pattern of NNS. Graph represents the extent of the movement of the lever inside the bottle nipple, measuring the expression component of sucking with 1.0 being the furthest the lever inside the nipple can move, and 0.5 being half the maximum distance. NNS occurs at up to two sucks per second in short, fast bursts lasting anywhere from 2 to 12 s with a pause between bursts of 3–13 s.

Figure 2

Waveform pattern of NS. Graph from the infant Feeding Solution showing the extent of the movement of the lever inside the bottle nipple measuring the expression component of sucking with 100% being the furthest the lever inside the nipple can move, and 50% being half the maximum distance. A mature NS pattern demonstrates regular, smooth movement about one suck per second.

Figure 3

Skills required for sucking in infants. (A) Infant at rest with the nipple inside the mouth. (B) Suction applied to the nipple to draw further into the mouth to form a teat and the tip of the tongue beginning to compress it. (C) Expression of the teat by the tongue movement against the hard palate.

Figure 4

Stages of NS. Early stages (–3) are seen in preterm infants, while more mature stages (4 and 5) are seen in term infants as well as preterms after enough experience and maturation. Reprinted with permission from Lau (37).

Figure 5

Anatomy and physiology of the infant during feeding. Unlike the adult, the epiglottis moves upward toward the soft palate during feeding. The white indicates the fluid meal and demonstrates how it is made to go around the epiglottis and into the esophagus. The dotted blue arrow indicates the air coming from the nasal passage during the feeding and demonstrates its laminar flow into the trachea.

Figure 6

Sucking and swallowing brain network. Sucking and swallowing is a bilateral process in the brain, each hemisphere has been shown to act both contralaterally and ipsilaterally, therefore, for simplicity, the black arrows on the right, coronal view of the brain indicate the complex integration and communication between the areas in only one hemisphere currently believed to be involved in the motor aspects of sucking. CPGs (blue), are at the core of this complex system. A second level of controls includes subcortical structures including the basal ganglia, hypothalamus (pale olive green), cerebellum, amygdala (purple), and tegmental area (pink) of the midbrain with a third level in the suprabulbar cortical swallowing center and insula (green). The cranial nerves (CN) required for the motor process of feeding and swallowing include CN V and VII to move the jaw and facial muscles, CN XII for tongue movement, CN V, IX, and X for movement of the epiglottis, expansion of the uvula and elevation of the hyoid bone and larynx, and CN X for peristaltic movement of the esophageal muscles.

Figure 7

Technological solutions to assess neonatal sucking. Schematic diagrams of some technological solutions used to measure sucking during bottle feeding in infants. (Left) Non-portable measuring apparatuses [KNSA (77), NSA (79), and Mizuno-Ueda system (80)]: pressure transducers (PTs) are used to measure sucking pressures exerted on a nipple, which is not connected to a regular feeding bottle, but to a reservoir containing milk via a flow-regulating capillary tube or regular catheter. The milk reservoir is always kept at the mouth level to eliminate net hydrostatic pressure (unlike in regular bottle-feeding sessions). Regular nipples were used in NSA and Mizuno & Ueda's systems, while a stiff nipple was used in KNSA. (Right) Portable measuring solutions: feeding bottles instrumented with pressure transducers (PTs) to measure different sucking pressures [Orometer (81) and SuMOD (82): via air-filled catheters] or tongue movement (nFS; via a lever). These solutions were designed to be attached to regular bottles for easy use in clinical settings. Orometer measures the suction component of sucking; nFS measures tongue movement (related to the expression component); while SuMOD measures suction and expression components separately (enabling coordination assessment). nFS is a wireless solution, while Orometer and SuMOD require wired connection to an acquisition system.

Figure 8

Correlation of abnormal NS patterns with integrity of sensorimotor fibers in infants with established in infants with established brain injury [from Tamilia et al. (31)]. (A) Anatomically defined regions of interest overlaid on the T1 MRI of a female 4 day old preterm infant. On the left, regions of interest for the motor tracts; in the middle, regions of interest for the sensory tracts; on the right, regions of interest corresponding to the corpus callosum. (B) Corpus callosum (magenta) overlaid on the fractional anisotropy color-maps. (C) Axial view of the motor (in yellow) and sensory (in purple) tracts reconstructed via probabilistic diffusion imaging tractography, along with the regions of interest used for their delineation. Neural tracts and regions of interest are overlaid on the patient's MRI that shows ischemic injury in the right frontal lobe. (D) The values of nutritive sucking smoothness and irregularity are predictive of the fractional anisotropy and mean diffusivity values, respectively, for the motor tracts. High smoothness in the nutritive sucking pattern, which is indicative of good sucking skills, is associated with high-fractional anisotropy, which is indicative of intact neural tracts. High irregularity in nutritive sucking, which is indicative of poor sucking skills, is associated with high-mean diffusivity, which is indicative of low integrity of neural tracts. (E) Two bursts of nutritive sucking from patients 3* and 8*. The left waveform demonstrates a poor NS behavior of patient 3* characterized by low smoothness and high irregularity (i.e., presence of multiple peaks); while the right waveform demonstrates a good NS behavior of patient 8* characterized by the smooth and regular nutritive sucking pattern.