Science of bottle feeding

T H E J O U R N A L OF

PEDIATRICS OCTOBER

Volume 119

1991

Number 4

MEDICAL PROGRESS Science of bottle feeding O o m m e n P. M a t h e w , MD From the Departments of Pediatrics and of Physiology and Biophysics, University of Texas Medical Branch, Galveston, Texas

For a newborn infant, there is hardly a more complex motor act than feeding, which can be broken down into three components: sucking, swallowing, and breathing. Each of these motor acts involves sequential and coordinated contraction of a number of muscles. What follows is an attempt to put in perspective the science of bottle feeding; only limited references will be made to breast-feeding. SUCKING Ontogeny of sucking. Sucking has been documented in the fetus as early as the fifteenth week of gestation. 1 Gryboski2 reported an immature suck-swallow pattern in infants born at 32 to 34 weeks of gestation; the pattern consists of swallowing before or after short sucking bursts. The hallmark of the mature sucking pattern, multiple swallows during a sucking burst, was seen by 6 to 12 weeks of postnatal age in preterm infants born at 32 to 34 weeks of gestation, and by 2 weeks of age among infants born at 34 to 36 weeks of gestation. No evidence of rhythmic organization of sucking was observed until 33 to 36 weeks by Wolff) Recently, Hack et al. 4 reported mouthing movements in infants at 28 weeks, a clear burst-pause pattern by 32 weeks, and a stable pace and rhythm by 34 weeks of gestational age (Fig. 1). Both Gryboski 2 and Hack et al. 4 observed in preterm infants with postnatal maturation an increase in sucking frequency attributable primarily to a shortening of interburst intervals. Most preterm infants are ready for full bottle feeding by 34 to 36 weeks, a time that coincides with maturation of other physiologic processes. For example, Reprint requests: O. P. Mathew, MD, Department of Pediatrics, East Carolina University, Greenville, NC 27858. 9/18/31166

apnea of prematurity decreases markedly around this time, indicating functional maturation of the brain-stem respiratory centers. A concurrent decrease in conduction time of the auditory evoked response suggests that this maturational step may result from increased myelination. 5 Physiology of sucking. Recent physiologic studies of nutritive sucking show that pressure change in the oral cavity is mostly negative. 6, 7 The criteria used to define nutritive sucking in our studies 7-12 were as follows: the amplitude of pressure change must be greater than 10 cm H20; the change should occur in 0.5 second or less; the return of SIDS

Sudden infant death syndrome

pressure toward baseline should be at least 5 cm H20 in 1 second; and the total cycle time must not exceed 1.5 seconds. These criteria are reasonably liberal, include essentially all sucks, and are only slightly different from those reported by Kaye 13 for nonnutritive sucking. Both radiologic and physiologic studies have shown that newborn infants can suck and breathe simultaneously. This capability requires that while respiratory activity continues, the oral cavity has to be functionally isolated from the respiratory tract. The primary purpose of nutritive sucking is to express milk from the breast or bottle into the oral cavity. Nutritive sucking, therefore, can be considered as a preparatory phase of the swallow. Rhythmic contractions of jaw muscles generate suction pressure in infants, whereas respiratory muscles are used to create suction pressure in adults. During the key initial phase of sucking, labial and facial muscles are contracted to form a seal around the nipple (Fig. 2, panel 1). The nipple itself is compressed against the palate by the tongue (Fig. 2, panels 2 and 3). In breast511

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The Journal of Pediatrics October 1991

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4 = 5 SEC Fig. 1. Progressivedevelopment of nonnutritive sucking. (From Hack M, Estabrook M M, Robertson SS. Early Hum Dev 1985;11:133-40. Reproduced by permission.) fed babies the action of the tongue appears to be rolling, whereas in bottle-fed babies it seems to be largely pistonlike. 14The human nipple is highly elastic. During active feeding it elongates to approximately twice its resting length, whereas its height is reduced by almost half. 15 During sucking, rhythmic movements of the oral portion of the tongue and lower lip, in conjunction with the mandible and hyoid, result in an initial lowering of the mandible and protrusion of the tongue followed by mandibular elevation, b In two landmark cineradiographic studies, Ardran et all6, 17 investigated breast and bottle feeding, On the basis of these studies, they argued that even during bottle feeding infants express milk from the nipple by squeezing, while acknowledging that success of the squeezing process depends mostly on the rigidity of the nipple and the size of the feeding hole] 6 Babies could obtain an adequate milk supply only if the hole is relatively large. Suction was believed to play a primary role only in refilling the bulb of the nipple. These conclusions are still considered valid by many, although several studies have i"eported contradictory results. Physiologic studies of sucking have shown the presence of both positive and negative pressure changes in the oral cavity; these changes have been termed expression and suction components, respectively. The relative importance of expression and suction pressures in creating milk flow was reinvestigated as early as 1958 by Colley and CreamerJ 8 Pressure measurements indicated that squeezing of the nipple by the jaw and tongue played little part in extracting milk. Their data suggested that during bottle feeding the suction created by the pistonlike movements of the tongue and jaw was the critical factor in milk expression. Unlike

early cineradiographic studies, which were limited to one plane, recent ultrasonographic studies permit visualization in both horizontal and transverse planes) 5, 19-21 Although the human nipple is significantly compressed and lengthened during sucking, milk is ejected approximately 30 msec after maximal nipple elongation, an event that coincides with the downward movement of the tongue and jaw. 15 These results suggest that the suction component is a critical factor even in breast-feeding. 15 Milk flow begins as the intranipple pressure decreases, and tapers as the intranipple pressure increases. 22 Sucking efficiency. Several factors determine how much milk is expressed per suck. For example, the ability of the infant to generate pressure changes depends both on the integrity of the labial and facial muscles to create a seal around the nipple and on the magnitude of contraction of the pressure-generating muscles. Paralysis of the facial muscles, especialIy if bilateral, leads to a loss of the seal and may result in inadequate pressure changes despite vigorous contraction of tongue muscles. The inability of infants with cleft palate to generate adequate sucking pressure is another demonstration that the seal around the nipple is essential for effective sucking. The decreased pressure changes seen among infants born to mothers receiving sedation during labor 23 may result from decreased motor output to the pressure-generating muscles. The volume of milk expressed per suck during both breast and bottle feeding depends not only on the infant's ability but also on the characteristics of the container system. Rigid glass containers are generally used in bottle feeding. Unless the bottle is vented periodically during sucking, a vacuum

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Science o f bottle feeding

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Fig. 2. Schematic representation of bottle feeding (see text for details). (From Bu'Lock F, Woolridge MW, Baum JD. Dev Med Child Neurol 1990;32:669-78. Reproduced by permission.) will develop, resulting in decreased expression of milk. Vent holes in the nipple will prevent the development of a vacuum. Alternatively, the container can be made collapsible, in which case the vent holes are not needed. Feeding time has been reported to be shorter when a collapsible plastic bag is used, 24 but sucking pressures were not measured in that study and it is not clear whether the shorter feeding time reflected differences in the container or increased sucking pressures. Nipple units differing in shape, size, consistency, and type of feeding hole are commercially available. These can be divided into the standard (single-hole) and the Nuk type of nipple units. The Nuk type (trademark owned by Mapa GmbH, Gummi-und Plastikwerke, Zeven, Germany) is promoted as being similar in shape to the human nipple, but the functional superiority of these nipples is yet to be proved. Among the standard nipple units, some are made specifically for term infants and others for preterm infants. The nipples for premature infants in general have a softer consistency and bigger feeding holes. In addition, some of the standard nipple units for both term and preterm infants have a crosscut opening presumed to become functional at greater negative pressures. We recently used an artificial sucking device to investigate the functional characteristics of various types of nip-

pies. Uniform negative pressure pulses at a fixed frequency were applied to exclude the variability in sucking pressures introduced by the infant. 25 Wide variability in milk flow was present within and among the nipple types studied (Fig. 3). Milk flow correlated highly with airflow measurements, the industry standard in nipple testing. Investigation of feedinghole sizes showed that within each type of nipple, the most important determinant of milk flow was the size of the feeding hole. 26 The role of the crosscut hole in altering milk flow is not clear; no milk flow occurred through this hole at negative pressures generally observed during bottle feeding. Our recent evaluation of laser-cut nipple units with different feeding-hole sizes suggested that variability in milk flow within a given nipple type can be significantly reduced by decreasing the variability in hole size.z7 Sucking patterns. At the beginning of a feeding, infants usually suck vigorously and continuously, often for periods lasting at least 30 seconds. This initial continuous sucking period is generally followed by a period in which the sucking burst alternates with periods of no sucking or pause; this period is termed intermittent sucking. Several investigators have studied the sucking pattern of infants under a variety of experimental conditions. The sucking frequencies are relatively constant during bottle feeding, but the sucking pressures vary markedly. 6 Technical problems associated

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The Journal of Pediatrics October 1991

Pressure - 1 2 0 cm H20

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Fig. 3. Comparison of flow characteristics of various types of nipples. Number of simulated sucks (means _+ SD) required to express 120 ml of formula at -120 cm HaO is shown on abscissa. In each cluster, columns represent SMA (Wyeth Laboratories, Philadelphia, Pa.), Enfamil (Mead Johnson Nutritional Group, Evansville, Ind.), and Ross (Ross Laboratories, Columbus, Ohio) nipple units. Wide variability in number of sucks among and within different nipple types can be noted. (From Mathew OP. Pediatrics 1988;81:688-91. Reproduced by permission of Pediatrics).

with oropharyngeal pressure measurements during feeding account in part for this observation, but variability in milk flow is another important factor. Other factors can also alter the sucking pattern. Taste buds are well developed in newborn infants. The sensory apparatus for assessing the relative sweetness of sugars is competent in the newborn infant and is capable of eliciting a graded response. 2a Continuity and speed of sucking may be modified by sucrose solutions differing in sweetness. 29 However, most newborn infants will tolerate any formula regardless of taste, although an occasional infant will refuse a certain formula or will feed poorly. Differences in fat content do not account for this phenomenon, 3~ but it is not clear whether the formula's odor plays any role in this process. Sucking pressure also is reported to decrease as environmental temperature increases. 31 The infant's state of wakefulness also affects the sucking pattern. The state-dependent effects of nonnutritive sucking have been investigated more thoroughly than those of nutritive sucking; however, these is not the focus of this review. A decrease in sucking pressure and an increase in time between sucking clusters are seen toward the end of the feeding. It is not known how much of this change is related to sensory feedback from the stomach and satiety centers, and how much is related to the onset of drowsiness or sleep. Blass and Teicher 32 stated that infants younger than 12 weeks of postnatal age terminate suckling with sleep onset and

resume it on awakening, whereas in infants older than 12 weeks, suckling is not necessarily terminated by sleep; no data were provided in support of the authors' contention. Sucking in term versus preterm infants. The nipples used for preterm infants have greater flow; the premise is that higher milk flow compensates for the lower sucking pressures generated. However, the presumption that preterm infants generate significantly less pressure than term infants under similar experimental conditions has little factual support. When we compared sucking pressures of term and preterm infants, the differences between them were not statistically significant, although preterm infants had a tendency toward lower sucking pressures.] 2 Sucking frequency in the two groups was also not significantly different. 12 Previous studies of bottle-fed term infants have indicated that they are capable of decreasing sucking pressure when flow rate increases. 18 A linear relationship between milk flow and sucking frequency has also been demonstrated in breast-fed term infants) 3 These observations suggest that at least term infants have a compensatory mechanism to limit volume per suck. When we studied preterm infants, we found no significant difference in sucking pressures between nipples for term and those for preterm infants, even though milk flow through the preterm nipples was, in general, higher.12 This finding suggested either that preterm infants do not have the ability to regulate milk flow or that the variability of flow within these two types of nipples is too great. When we repeated the same studies with laser-cut nipples with less variable hole sizes, we were able to document a difference in sucking pressures in preterm infants between high- and low-flow nipple units. 27 This finding indicates that preterm infants may have at least a limited ability to regulate milk flow. Work of sucking. It is important to know the energy expended in ingesting nutrients, but there is a dearth of knowledge in this area. The only investigators who have addressed this question concluded that both work and energy expenditures were greater for term than for preterm infants34; however, several methodologic issues were not adequately addressed. For example, the two most important variables in determining the work of sucking are the pressure generated and the volume expressed per suck. An 8F Foley catheter was used to deliver milk from the reservoir to the oral cavity. The flow rate of this system is at least two or three times that of the nipples used in bottle feeding, and the volume of suck reported is markedly higher. Infants generate less pressure when the milk flow is higherZS; hence the work of individual sucks during routine bottle feeding is likely to be significantly higher than that reported by these investigators. In addition, the efficiency of the muscles was assumed to be 100%. However, the current estimate of the efficiency of skeletal muscles, especially for respiratory muscles, is much lower. Intake was markedly different between term and preterm infants (110 to 125 ml/kg per day

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for term infants vs 150 to 170 ml/kg per day for preterm infants). If the results obtained by these investigators were expressed on the basis of intake per kilogram per day, instead of per deciliter, the work of sucking would be higher in preterm infants. More studies that address these and other issues related to the energetics and mechanics of feeding are needed. SWALLOWING Swallowing is an integral part of feeding. In this complex motor act, sequential activation and coordination of various upper airway muscles are essential and must be integrated with other ongoing vital functions such as respiration. Physiology of swallowing. Deglutition has three phases: oral, pharyngeal, and esophageal. These phases will be discussed only briefly here (see references 35 to 37 for reviews). The oral phase is a preparatory phase of swallowing and, in neonates, is coincident with nutritive sucking. The pharyngeal stage involves conveyance of the bolus through the pharynx to the esophagus. The esophageal phase beings as the bolus enters the esophagus and is a continuation of the pharyngeal motion. Generally this phase begins 600 to 900 msec after initiation of the pharyngeal phase. The oral stage is predominantly under voluntary control, whereas the other two phases are under involuntary control. Superficially located, slowly adapting receptors that respond to water and light touch are presumed to initiate the swallow. 38 Water is the most effective stimulus for the laryngeal mucosa, whereas touch or light pressure is more effective for the pharyngeal mucosa. Although topical anesthesia of a limited region does not impair elicitation of swallow, anesthesia of the entire oropharyngeal-laryngeal mucosa does. Swallowing has been investigated with cineradiography, ultrasonography, and electromyography. Cineradiographic studies have shown that during the initial collection phase, food is contained in a depression in the midline on the dorsal aspect of the tongue. Subsequently, the bolus is conveyed posteriorly. These observations have been confirmed recently by ultrasonography) 9 Horizontal transbuccal projections and transverse and longitudinal submental projections show a depression in the posteromedial aspect of the tongue along the median raphe. A peristaltic wave moves posteriorly in the medial portion toward the pharynx, propelling the expressed milk while the lateral portion of the tongue encloses the nipple and the bolus. During swallowing, the pharynx initially moves anteriorly and cranially. The larynx is elevated and pulled forward under the root of the tongue. Laryngeal adductors contract (Fig. 2, panel 4), and the cricoesophageal sphincter relaxes just before the bolus enters the esophagus. Each swallow is a patterned peristalsis descending through the constrictor, palatopharyngeal, submental, and laryngeal muscles. The sequence of activation of various muscles during pharyngeal swallowing has been studied in several species by elec-

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tromyography.39, 40 The muscles constricting at the onset of the swallow, labeled the leading complex, are the superior pharyngeal constrictor, genioglossus, styloglossus, stylohyoid, geniohyoid, and mylohyoid muscles. Disorders of sucking and swallowing. For a more detailed discussion of disorders of suck and swallow, readers are referred to reviews on the subject. 41"44 Dysphagia. Symptoms of dysphagia are vomiting, nasal regurgitation, cough, stridor, hoarseness, and difficulty in sucking and swallowing. Dysphagia in neonates can have any of a number of causes. They may be categorized as anatomic (e.g., palatal and laryngeal clefts, pharyngeal and laryngeal cysts, choanal atresia, macroglossia, esophageal atresia) or neuromuscular (e.g., prematurity, mental retardation, cerebral palsy, pharyngeal incoordination, muscular dystrophy, myasthenia gravis, hypertonia). Most infants with dysphagia show eventual improvement. Pharyngonasal reflux. Nasal regurgitation occurs in disorders such as velopharyngeal dysfunction and certain neuromuscular diseases, and even with prematurity. It appears to be rare, but its prevalence has not been documented. 45

BREATHING The interaction among sucking, swallowing, and breathing during feeding has caught the attention of several investigators for a number of years, but difficulties in measuring ventilation during feeding had prevented accurate quantification of these interactions. The recent development of small flowmeters to measure nasal airflow was a major advance. Although effects on breathing of sucking and swallowing are discussed separately, the two are closely related and are often difficult to separate distinctly. An increase in transcutaneous oxygen values has been reported during nonnutritive sucking. 46 A shortened expiration and an increased breathing frequency have been observed during sucking bursts. 11 However, breathing frequency, tidal volume, and minute ventilation remain unchanged across the entire nonnutritive period.11 This finding suggests that the improvement in oxygenation may be due to a decrease in ventilation-perfusion mismatch. For a long time, young infants were believed to be capable of feeding without interrupting breathing. This belief was based on the suggestion by Negus 47 that many herbivorous animals are able to pass food through the pharynx without interrupting breathing. However, cineradiographic studies by Ardran et al. 16 indicated that this is not true for infants. Recently, several studies measuring airflow have unequivocally shown that airflow is interrupted during swallowing in human beings. 6,48-5~ Effect of feeding on ventilation. The effect of feeding on ventilation in infants has not been studied extensively. Significant methodologic and analytic differences among previous studies make generalizations difficult, as discussed in a recent review. 6 In spite of these differences, the results of

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The Journal of Pediatrics October 1991

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is significantly lower than control values in both groups. Note that greater reduction in ventilation occurs in more immature group of infants. (From Shivpuri CR, Martin R J, Carlo WA, Fanarof AA. J PEDIATR1983;103:285-9. Reproduced by permission.) all these studies concur: ventilation decreases markedly during nipple feeding. In the first study to quantify the effects of feeding on ventilation (Fig. 4), Shivpuri et al. 51 investigated two groups of premature infants and found that a reduction in both frequency and tidal volume accounted for the reduction in ventilation. Similar findings were reported in term infants by Mathew et al. 9 After the initial continuous sucking phase, in which ventilation is markedly reduced, most term and preterm infants stabilize their respiration during the intermittent sucking period. Complete recovery of ventilation in term infants and partial recovery in premature infants are observed in this period. 9, 51 However, within this intermittent sucking period, the ventilation, breathing frequency, and tidal volume are markedly lower during sucking bursts than in pause periods, in both term and preterm infants. 9, 51 In fact, overall recovery depends on the duration of these pauses and the infant's ability to increase ventilation during the pause periods when they occur. Although ventilation decreases markedly during nipple feeding, the cause of this ventilatory depression is less certain. Several factors have been implicated, including behavioral overriding, laryngeal chemoreflex, repeated swallowing, and prolonged airway occlusion; these are not necessarily mutually exclusive. Durand et al. 52 reported a

reduction in ventilatory response to carbon dioxide during feeding and attributed it to behavioral overriding (cortical influence). After studying nonnutritive sucking in an attempt to dissociate swallow and chemoreceptor-related inhibition of breathing, Mathew et al. l~ argued that behavioral overriding would be similar in both nutritive and nonnutritive sucking. On the basis of the results of the nonnutritive sucking study, they concluded that behavioral overriding is unlikely to account for the reduction in ventilation during feeding.l 1 Laryngeal ehemoreflex. Animal studies have shown that instillation of distilled water into the larynx elicits apnea 53, 54 This reflex apnea is mediated through the superior laryngeal nerve afferents. Perkett and Vaughan 55 and Davies et al. 56 provided data supporting the existence of the laryngeal chemoreflex in human neonates. Johnson and Salisbury 57 suggested that the chemical composition of nutrients can alter the breathing pattern through stimulation of laryngeal chemoreceptors; a greater number of infants showed an altered breathing pattern during artificial-milk feeding than during human-milk feeding, s7 However, neither Guilleminault and Coons 5s nor Mathew and Bhatia 7 were able to show a marked difference in breathing pattern between human-milk feeding and formula feeding. Lack of

Volume 119 Number 4

small anions such as chloride is responsible for the laryngeal chemoreflex, 53 and chloride ions are low in both human milk and formula. Moreover, chloride ions are even lower in human milk than in cow milk and formula. 6 Hence, it appears that the laryngeal chemoreflex does not play a major role in the observed reduction in ventilation during feeding, although a contributory role cannot be excluded. Swallowing. Interruption of airflow during the pharyngeal swallow is now well documented. The duration of a feeding swallow varies from 350 to 700 msec. 49 Infants have been known to swallow up to 30 times per minute, and there is a 1:1 correlation between suck and swallow in the initial phase of feeding. Hence a substantial portion of the feeding time is not available for ventilation because of repeated swallowing. Koenig et al. 49 showed that ventilation during feeding has an inverse relationship to the frequency of swallowing (Fig. 5). After each individual swallow, the airway normally opens in a cephalocaudal sequence and ventilation is resumed. However, airflow sometimes fails to resume despite respiratory efforts because the airway remains closed. At least One such episode of prolonged airway closure is seen during each feeding. 49 Several mechanisms could play a part in this prolonged airway closure: the occurrence of respiratory effort before airway opening, mucosal adhesive forces, insufficient airway dilative forces, and continued activation of airway constrictors. Obstructed respiratory breaths are fairly common during feeding. Two types of obstructed breaths have been reported: the smallamplitude swallow-breath occurring before the swallow and respiratory efforts of normal or increased amplitude occurring at any time. 49 Although the function of the swallow breath is not known, it is thought to remove air from the pharynx and Prevent air swallowing. All infants need burping after a feed, so these swallow breaths are either inefficient or too infrequent to prevent aerophagia. Respiration is normally inhibited during the swallow. 59 Normal-amplitude obstructed breath occurs because either this inhibitory mechanism failed or airway closure was abnormally prolonged. Study of neurons with respiratory activity in the reticular activating system shows that some neurons stop respiratory activity and exhibit a burst of impulses with swallowing. 6~Usually they remain silent for 1.0 to 1.8 seconds before resuming respiratory discharges. Other neurons cease firing during swallows and are silent during repetitive swallowing. Phrenic motoneurons exhibit a swallow discharge, a swallow burst with partial respiratory volley, or silence with repetitive swallowing. 6~ We already showed that neonates have some ability to regulate milk flow during sucking. How does altered milk flow affect breathing pattern and ventilation? A marked decrease in ventilation is seen in both term and preterm infants. However, these studies were conducted with a reservoir nipple system (i.e., milk was delivered from the container through a tube into the oral cavity. 9, 5t This sys-

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Relationship between swallow frequency and minute Ventilation. For term and preterm infants, minute ventilation decreases as swallow frequency increases (p <0.001, analysis of variance). (From Koenig JS, Davies AM~ Thach BT. J Appl Physiol 1990; 69:1623-9. Reproduced by permission.)

tern essentially bypasses the nipple. Although milk flow depends on sucking pressure, flow rate in this system is at least twice the milk flow through a nipple. 12 It is unclear from these studies (and even from other studies) how much of the decrease in ventilation is flow dependent. When we compared breathing patterns in breast-fed and formula-fed neonates, minimal alteration in breathing pattern occurred during the first few days of breast-feeding, whereas marked alteration was seen during formula feeding. 7 This difference was attributed to low milk flow because similar alteration occurred when expressed human milk was fed from a bottle, indicating that the difference between formula feeding and breast-feeding was primarily due not to differences in composition but, rather, to a difference in flow rate. Recently we tested this hypothesis by using low- and high-flow laser-cut nipples and found that reduction in ventilation was greater with high-flow nipples. 61 Decreases in frequency and tidal volume accounted for the reduction in ventilation.

Disorders of breathing Apnea, cyanosis, and bradyeardia. Disorders of feeding often result in impairment of respiratory function with resultant hypoventilation, airway obstruction, or apnea. The decrease in ventilation that occurs during feeding decreases partial pressure of oxygen and increases partial pressure of carbon dioxide. 8, 51 This change in ventilation is likely to have a greater impact on preterm infants and sick term infants. In fact, development of apnea and bradycardia during feeding is being recognized with increasing frequency in preterm infants, s, 58, 62 Similarly, the highest incidence of desaturation in infants with bronchopulmonary dysplasia occurred during feeding. 63 A high incidence of apnea and

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bradycardia in the first few days of life was seen even among term infants in a study using a reservoir nipple system. I~ However, the incidence of apnea and bradycardia was lower when the infants were nipple fed from a bottle (Mathew OP: unpublished observations). Unlike term infants, in whom cyanosis and bradycardia usually develop during the initial continuous sucking phase, 1~ preterm infants can have episodes of cyanosis and bradycardia at any time during a feeding; often they may have recurrent episodes during the same feeding) Whether the preterm infants' limited ability to regulate milk flow contributes to the development of these events is not known. Infants who are more immature have greater respiratory depression with the same feeding regimen,51 possibly because they respond more strongly to similar levels of sensory input. A greater respiratory response to a number of laryngeal stimuli has been seen in newborn animals than in adults. 64 Greater breathing difficulties are often seen among infants after prolonged intubation and tracheostomy. Laryngeal penetration of formula during feeding probably accounts for this observation. Sudden infant death syndrome. In 1976 Steinschneider and Rabbuzzi65 reported on two infants with feedingrelated bradycardia who subsequently died of sudden infant death syndrome, In a large prospective study, Steinschneider et al. 66 reported that victims of SIDS had had an increased incidence of apnea and airway obstruction during feeding in the neonatal period. Many normal infants also had similar abnormalities during feeding; this finding was therefore not sufficiently discriminating to identify victims of SIDS prospectively. However, if feeding unmasks some functional abnormality of the respiratory control system that is not present under normal resting conditions, it may have some potential for identification of future SIDS cases. No one has studied the feeding-related apnea in the neonatal period to determine whether this deficit persists in victims of SIDS but disappears in normal infants. CONCLUSIONS In the final analysis, two factors are important in the determination of optimal milk flow: the work of sucking and the depression of ventilation. It is likely that in our attempt to reduce ventilatory depression we would increase the work of sucking and vice versa. Therefore a balance between these two conflicting priorities is needed. Otherwise, one could easily choke the infant by exceeding his or her regulatory capacity or increase the work of sucking by markedly limiting the flow. Reduced variability in hole size is essential to ensure uniform milk flow through any given nipple type; laser-cut nipples hold promise in this regard. For most infants a nipple unit with a flow rate of ~0.15 ml per simulated suck at a negative pressure pulse of 120 cm H20 would be adequate; this volume corresponds to the suck

The Journal of Pediatrics October 1991

volume observed at the beginning of a feeding in breast-fe d babies.67 For infants who generate markedly higher or lower pressure than average, the availability of a nipple with lower or higher flow may be beneficial to keep both milk flow and suck within the range of the infants' ability to regulate flow. I thank Drs. C. D. Baldwin, J. S. Bhatia, and C. J. Richardson for their helpful suggestions. REFERENCES

1. Ianniruberto A, Tejani E. Ultrasound study of fetal movements. Semin Perinatol 1981;5:175-81. 2. Gryboski JD. Suck and swallow in the premature infant. Pediatrics 1969;43:96-102. 3. WolffPH. The serial organization of sucking in the young infant. Pediatrics 1968;42:943-56. 4. Hack M, Estabrook MM. Developmentof sucking rhythm in preterm infants. Early Hum Dev 1985; 11:133-40. 5. Henderson-Smart DJ, Pettigrew AG, Campbell DJ. Clinical apnea and brain-stem neural function in preterm infants. N Engt Med 1983;308:353-7. 6. Mathew OP. Regulation of breathing pattern during feeding: role Of suck, swallow and nutrients. In: Mathew OP, Sant'Ambrogio G, eds. Respiratory function of the upper airway. New York: Marcel Dekker, 1988:535-60. 7. Mathew OP, Bhatia J. Sucking and breathing patterns during breast- and bottle-feedingin term neonates. Effects of nutrient delivery and composition. Am J Dis Child 1989;143:588-92. 8. Mathew OP. Respiratory control during nipple feeding in proterm infants. Pediatr Pulmonol 1988;5:220-4. 9. Mathew OP, Clark ML, Pronske ML, Luna-Solarzano HG, Peterson MD. Breathing pattern and ventilation during oral feeding in term newborn infants. J PEDtaTR 1985;106:810-3. 10. Mathew OP, Clark ML, Pronske MH. Apnea, bradycardia, and cyanosis during oral feeding in term neonates [Letter]. J PEDLaTR 1985;106:857. 1I. Mathew OP, Clark ML, Pronske MH. Breathing pattern of neonates during non-nutritive sucking. Pediatr Pulmonol 1985;1:204-6. 12. Mathew OP, Belan MA, Thoppil CK. Sucking pattern of neonates during bottle feeding: comparison of different nipple units. Am J Perinatol (in press). 13. Kaye H. Infant sucking behavior and its modification.In: Lipsitt LP, Spiller C, eds. Advances in Child Development and Behavior; vol 2. New York: Academic Press, 1967:1-52. 14. Weber F, Woolridge MW, Baum JD. An ultrasonographic study of the organization of sucking and swallowingby newborn infants: Dev Med Child Neurol 1986;28:19-24. 15. Smith WL, Erenberg A, Nowak A. Imaging evaluation of the human nipple during breast-feeding. Am J Dis Child 1988;142:76-8. 16. Ardran GM, Kemp FH, Lind J. A cineradiographic study of bottle feeding. Br J Radiol 1958;31:11-22. 17. Ardran GM, Kemp FH, Lind J. A cineradiographic study of breast feeding. Br J Radiol 1958;3l:I56-62. 18. ColleyJRT, Creamer B. Sucking and swallowingin infants. Br Med J 1958;2:422-3. 19. Bosma JF, Hepburn LG, Josell SD0 Baker K. Ultrasound demonstratiorz of tongue movements during suckle feeding. Dev Med Child Neurol [990;32:223-9. 20. Bu'Lock F, WoolridgeMW, Baum JD. Development&co-ordination of sucking,swallowing,and breathing. Dev Med Child Neurol 1990;32:669-78.

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