DEVELOPMENT OF CO-ORDINATION OF SUCKING, SWALLOWING AND BREATHI NG: ULTRASOUND STUDY OF TERM AND PRETERM INFANTS Frances Bu ’Lock M . W . Woolridge J. D. Baum
Establishing effective feeding is a prerequisite for the survival of newborn infants. Efficient and safe feeding requires co-ordination of breathing with sucking and swallowing and involves the functional interaction of lips, jaw, tongue, palate, pharynx, larynx and oesophagus (Doty 1968, Miller 1982). There is increasing interest in the sucking performance of preterm infants (Daniels et al. 1986), but few studies have increased our knowledge of the development of feeding co-ordination during fluid intake (cf non-nutritive sucking-Hack et al. 1985). Feeding difficulties make up a major proportion of the problems that arise in otherwise healthy term and preterm infants. In order to intervene appropriately, the problem must be adequately defined. This can usually be done by careful history-taking and examination, combined with observing the mother feeding her baby. Occasionally, however, more specialised investigation is indicated, including the imaging of events occurring inside the baby’s mouth. A variety of electrophysiological and radiographic techniques have been used experimentally to define the intra-oral organisation of the feeding process (Halverson 1944, Kron et al. 1963, Johnson and Salisbury 1977, Woolridge and Drewett 1986). Of these, cineradiography has been the most useful
(Ardran et al. 1985a, b); however, the risks of irradiation restrict the use of this technique. Recently it has become possible to image intra-oral events during feeding by using real-time ultrasound (Smith et al. 1985, Weber et al. 1986). This technique has no known sequelae, and allows imaging at the bedside in the ‘normal’ feeding position for mother and infant, whether breast-feeding or bottle-feeding. There is little information in the literature about the development of feeding co-ordination in preterm infants (Gryboski 1969). The present study examined the way in which preterm infants co-ordinate sucking, swallowing and breathing during bottle-feeding. Meier and Anderson (1987) suggest that babies may be developmentally competent to breast-feed at an earlier stage than that at which they can bottle-feed. However, we elected to study the infants during bottle-feeding, as this permitted standardisation of feeding across babies, which would not have been possible with breast-feeding.
Normal feeding dynamics There are diverse opinions in the literature about the organisation of the normal feeding process (Woolridge 1986), but the general consensus for term infants is that a bolus of fluid is delivered to the pharynx by a phased application of the dorsum of
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Fig. 1. Feeding movements. I. ‘Resting’ posifion. Teat is held firmly and fully within mouth, with tongue beneath teat. Soft palate is relaxed and nusopharynx is in continuity wifh trachea. Laterally, tongue and buccal mucosa form seal around teat to roof of mouth.
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2. This view is approximately 0.25sec later than in I (similar interval separates subsequent views). Lower jaw is elevated, compressing base of teat, while front of tongue moves upward, initiating expression of milk from teat; back of tongue is depressed, leaving space for milk to collect.
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3. Wave of upward movement of tongue progresses backward, further expressing milk from teat into mouth. This is facilitated by negative pressure generafed by downward movement of back of tongue and of lower jaw.
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the tongue to the nipple or teat in an antero-posterior peristaltic wave of contraction. Co-ordinated movement o’f the mandible and apposition of the gums traps milk in the lacteal sinuses of the breast or teat of the bottle. Milk is then expressed, by compression of the ‘teat’, into the pharynx. This is assisted by the negative intra-oral pressure generated posteriorly by lowering of the jaw and posterior depression of the tongue which occur during this movement sequence. From the pharynx, a series of reflex
muscular contractions and relaxations transfer milk into the oesophagus and onward into the stomach by peristalsis (and gravity). At the same time, milk is prevented from entering the nasal/ tracheal airway by elevation of the soft palate and closure of the larynx. The exact relative contributions of intra-oral negative pressure and of nipple compression to the process of transferring milk from the breast or bottle to the baby are controversial. However, efficient feeding probably requires co-ordinated
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4. The swallow. A s wave of tongue contraction sweeps off back of teal, it impinges on soft palate, thus sealing milk within oropharynx. Swallowing is triggered, levator muscles of palate contract and nasal cavity is sealed off from milk, aided by contraction of muscles of posterior pharyngeal wall. Upward movement of laryngohyoid complex, approximation of arytenoids and movement of epiglottis effectively close off airway. Only at this point in feeding cycle is airway closed and breathing temporarily interrupted. Milk is then propelled into upper oesophagus, whence it is expelled into stomach by peristalsis.
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5. A s in I , soft palate returns to resting position, larynx descends and airway re-opens. Tongue is then in position f o r another sucking cycle to commence, a complete cycle lasting approximately Isec. Anterior segment of tongue begins to move again, before contraction of posterior segment is fully complete.
6. Breast-fed infant at ‘rest’. Note that tongue is extended more anteriorly, and there is deeper penetration of nipple than of bottle teat. Unlike bottle teat, human nipple does not recoil elastically in vertical plane, so is maintained in moderate state of compression.
tongue- and jaw-movements, producing both positive expression pressure and negative suction pressure (Darwin 1877, B a h t 1948, Colley and Creamer 1958, Farriaux and Milbled 1967). Thus, as first described by Ardran et al. (1985a, b), there is a basic, repetitive, rhythmic rolling movement of the tongue, produced by differential contraction of the longitudinal and transverse intrinsic musculature of the tongue. The best visualisations of feeding movements were obtained in the lateral/sagittal plane by Ardran and
colleagues for both breast-fed and bottlefed babies. Based on their work, and on more recent observations of the dynamic three-dimensional process of feeding with the use of ultrasound (Smith et al. 1985, Weber et al. 1986), we have compiled the pictorial representations shown in Figure 1 . The process is shown for a term infant bottle-feeding, to facilitate comparison with the ‘abnormal’ features described in the present study, and a single stage during breast-feeding is inset for comparison. We have noted relatively few
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TABLE I Characteristics of infants studied Group
N
Birth weight
(s)
Age at study (days)
Postconceptional age (wks)
1 (33-34 wks) 2 (35-36 wks) 3 (37+ wks)
5 4
1750-2173 1905-2650 2650-3860
10-19 4-7 4-7
34.5-37 36.5-37.5 38.5-41
5
qualitative differences in sucking behaviour on a bottle compared with the breast. One feature, shown in Figure 1 , is that during bottle-feeding the tongue is not projected so far forward as during breast-feeding.
Co-ordination of normal feeding In a normal, co-ordinated, nutritive* sucking cycle, breathing is interpolated between swallows, a fact which has been overlooked historically (Balint 1948, Pieper 1963). In a perfectly co-ordinated cycle, suck, swallow and breathing movements are related in a 1:l:l sequential pattern (Halverson 1944, Wolff 1965, Johnson and Salisbury 1977, Weber et af. 1986). These form a rhythmically repetitive unit, in which breathing appears to be continuous and uninterrupted. During less well co-ordinated feeding, breathing is always interrupted by swallowing (Halverson 1944, Logan and Bosma 1967, Weber et al. 1986), and indeed may be subordinate to it (Johnson and Salisbury 1977).
Material and method Subjects In this cross-sectional study of 14 infants, nutritive and non-nutritive feeding movements were observed in three groups of normally grown, bottle-feeding babies, defined according to gestational age at delivery (Table I). Gestational age was determined by obstetrical assessment of last menstrual period and/or ultrasound scan. The study was approved by the Regional Ethical Committee. The parents were given a printed explanatory sheet
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*Operationally defined for bottle-feeding as that type of sucking observed when fluid is delivered from the teat (cfnon-nutritive sucking when fluid is withheld).
and their informed verbal consent was obtained. Previous research suggests that it may take three to four days for ‘normal’ feeding to become established in term babies. Day four postpartum therefore was chosen as the earliest day for the study of term infants. The preterm babies were studied as early as possible after starting sucking feeds, which began independently of the study as determined by experienced nursing staff. There was some overlap, therefore, between groups 1 and 2 in their postconceptional age at the time of study, but a clear difference remained between groups 1 and 3. Babies were not included in the study if there was evidence of complications of preterm birth: Apgar < 8 at five minutes; respiratory distress requiring artificial ventilation for > 12 hours; or other postnatal complications, including severe jaundice (peak bilirubin > 240pmoV~). Eight male and six female infants were recruited. At the time of study, all babies were being predominantly bottle-fed. All group 1 infants had been given tube-feeds initially, followed by bottle-feeds, although efforts were being made to establish breast-feeding in two cases. A11 group 2 and 3 infants were wholly bottle-fed. During the study the babies were fed with either Cow & Gate ‘Premium’ formula or expressed breast-milk in a standard glass bottle with a disposable teat. There was a one- to two-minute period of sucking on a sealed teat (nonnutritive sucking) at the beginning, midpoint or end of each feed to allow comparison of nutritive and non-nutritive sucking performance. The volumes of each baby’s three previous feeds were noted, and the
midpoint of the test feed was predetermined as half the mean of these volumes. The mean volumes varied from 3 0 m ~for small babies to 7 0 m ~for larger ones.
Scans The scans were performed using an ATL 20 MK300C real-time ultrasound scanner with a 7.5MH.z scanhead (Advanced Technology Labs. Inc.). The image was inverted and adjusted so that the teat always appeared on the left of the screen. Depth and contrast were adjusted for each baby t o optimise the quality of the image. The frame counter was activated at the start of each feed. All feeds were recorded on a linked VHS video-recorder. Recordings were made throughout any period when the teat was in the baby’s mouth; however, the technique did not always permit a completely continuous record. A Graseby Dynamics Apnoea Alarm was attached to the baby with elasticated adhesive tape over the anterolateral thoraco-abdominal junction. This provides reliable compression and triggering of the sensor on inspiration, whether breathing is predominantly abdominal or thoracic, thereby overcoming the problems that Selley and colleagues (1986) encountered with such a device. The output from the alarm was connected to the ECG input of the scanner via a variable KC^ resistor to produce a clear signal on the in-built ECG display facility. The device also produces a simultaneous audible ‘click’, which was recorded, together with any comments during the feed, via the microphone input onto the video record. Previous studies have shown that maximum information from a single view is obtained from the submental midline sagittal plane, so all scans were recorded from that position. Possible additional information from coronal scanning (Smith et al. 1985) was sacrificed in order to obtain near-continuous recordings of the feeds. Feeds The breath sensor was positioned and adjusted. The baby was fed in the usual position at the usual time, either by the mother, or if this was usually the case, by
a nurse. There were pauses for ‘winding’ as necessary. The babies were allowed to feed to satiety, or to their maximum milk allowance in the case of preterm babies, and feeds lasted for an average of 30 minutes. Mothers said that they did not feel that the scanning process materially affected the feeds.
Analysis Each scan was viewed several times at both normal and slow speeds. The scans were reviewed in random order, without knowledge of the infants’ maturity. A qualitative description of the type and frequency of tongue movements was noted, as were temporal relationships between the three separate eventssucking, swallowing and breathing-and any changes in these relationships during the feed. The relative proportions of time spent in nutritive and non-nutritive sucking were also noted. We were unable to obtain continuous records of every complete feeding sequence, so it was not possible to quantitate the exact proportions of feed occupied by the various sucking patterns seen. Consequently, a scoring system was used throughout each scan. A formal statistical analysis would not be appropriate for a study of this kind, in which a large proportion of observations are concerned with the nature and quality of certain activities.
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Results Interpretable scans were obtained for all infants throughout one entire feed. Although the quality of the scans varied, it was always possible to identify separately the teat, tongue and palate for most of each feed (Fig. 2). At rest, the palate is separated from the tissues adjacent to the scanhead by the air gap of the nasopharynx, so it is difficult t o identify the palate at rest or during non-nutritive sucking, except when (presumably) saliva is being swallowed. However, swallowing could also be identified by upward movement of the hyoid and anterior cervical tissues, as well as occasionally by peristaltic movements of the upper oesophagus. No infant had any external evidence of mechanical feeding difficulties, gagging
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TABLE I1
Summary of results Group I (33-34 WkS)
Group 2 (35-36 wks)
Group 3 (37-40 wks)
++ +
+ +
0 0
++
++
+++
Suck:swallow:breath ratio: 1:l:l other
++ ++
++
+ + t
Breathing abnormalities: ‘Apnoeas’ ‘Breath bursts’ Abnormalities: trend during course of feed
++
+
+/-
+/-
Increase
Some increase
Nutritive sucking Tongue movements: ‘Abnormal’ ‘Obstructive’ Suck:swallow ratio: 1:l
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2:1-4: 1
Non-nutritive sucking Tongue movements: ‘Abnormal’ ‘Obstructive’ Relationship of sucking to breathing Sucks disrupt regular ‘at rest’ breathing Breathing abnormalities: ‘Apnoeas’ ‘Breath bursts’ Abnormalities: trend during course of feed Code: 0 =none; + + + times/absent at others.
+
+
++
+/-
+/-
+/-
No trend
+
+/-
0
0
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++
+/-
+/-
+
0
0 +/-
Some increase
No trend
0 0 No trend
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+
+
0
+ + + =present (by degree); + / - =present at
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or distress during the test feeding. Major features of the scans for each group of infants are summarised in Table 11. (Full details for individual babies are available on request.) No differences in feeding behaviour were noted between babies receiving formula feeds and those receiving expressed breast-milk (cf Johnson and Salisbury 1977). Tongue movements The normal mature pattern of tongue movements during sucking (as described above) was dominant throughout the feed in all three groups. However, various ‘abnormal’ movement patterns were seen, particularly among infants in group 1 (33 to 34 weeks). These were less evident among group 2 infants (35 to 36 weeks) and virtually absent in group 3 (37 to 40 weeks). The movements took three forms:
(1) incomplete or fragmentary peristaltic
waves of motion passing along the tongue, starting from and finishing at abnormal regions of the tongue and/or progressing in a posterior-anterior direction (Fig. 3); both the direction and duration of these movements were unpredictable; (2) apparently purposeless ‘non-peristaltic’ movements, which appeared as flickering or writhing movements in the two-dimensional view; (3) twitching or tremulous movements (‘microtremors’), probably equivalent to the ‘Quiver frequency’ noted by B a h t (1948). These tongue movements were more conspicuous during nutritive than nonnutritive sucking in both group 1 and 2 infants. They lessened during the course of the feed in four infants, but increased in two others.
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Fig. 2. Scan at moment of swallowing by infant of38 weeks gestation (as in 4 in Fig. I ) .
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-- ‘Tong u e “-Teat Respiratory trace Fig. 3. Scan demonstrating abnormal contraction of tongue by infant of 33 weeks gestation.
/- - - - - - - --Hard Palate
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- ‘Reverberation Artefact’
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Fig. 4. Scan showing ‘teat blocking’ by infant of36 weeks gestation.
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Some babies closed off the end of the teat by raising the tip or distal portion of the tongue (Fig. 4). Again, this was more common among group 1 infants and was not seen in group 3.
Co-ordination of sucking and swallowing Co-ordination of sucking and swallowing was far more consistent in babies with longer gestations. In addition, whereas four of the five infants in group 1 showed up to four sucks per swallow for much of the feed, the term infants showed a 1:1 ratio of sucks to swallows for a much higher proportion of the feed. Swallows were rarely observed during non-nutritive sucking at any gestational age. Sucking, swallowing and breathing It was readily apparent that all babies in the study achieved some periods of 1:l:l sequential linking of sucking, swallowing and breathing. The proportion of the feed in which this ratio occurred increased fairly uniformly with maturity, unlike other ratios. In the more preterm infants, sucking occasionally disrupted the regular, quiet breathing of an awake infant, but this was rarely seen in term infants. Such disruption was manifested by periods of sucking (usually associated with regular but asynchronous respiratory movements) being interrupted by a period of rapid breathing unaccompanied by sucks (‘breathing bursts’). This has also been described by Halverson (1944) and more recently by Selley et al. (1986). Similarly, term babies did not exhibit the ‘apnoeic’ pause in breathing movements during nutritive sucking which were prominent in group 1 babies and occurred occasionally in those in group 2.
Discussion
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The co-ordination of the intrinsic muscles of the tongue to produce fully-formed rhythmic, rolling movements seems t o be, at least in part, a product of gestational maturity. This is suggested by the fact that the preterm babies had more poorly co-ordinated tongue movements, despite being ‘older’ in ex utero age than the term babies at the time of the study. The synchronised co-ordination of sucking, swallowing and breathing to produce a ratio of 1:l:l during feeding
appears to be the preferred (and therefore presumably optimal) mode of feeding of term infants. This agrees with observations in other studies (Halverson 1944, B a h t 1948, Wolff 1968, Weber et al. 1986). The sequential linkage of sucking to swallowing and of swallowing to breathing also appears to approach the 1:1:1 ratio more often with increasing gestational maturity. This seems to require the simultaneous mastery of successful intrinsic tongue movements (providing a bolus of milk sufficient to initiate a swallow) and protection of the airway while maintaining regular breathing. In our small series, the linkage of sucking and swallowing with breathing appeared to be achieved consistently only by infants of more than 37 weeks postconceptional age. The linkage of sucking to swallowing usually is well established by 32 weeks, which is not surprising since swallowing can occur in utero from about 11 weeks gestation (Miller 1982). Preterm babies are notably less efficient at ‘safe’ feeding than term babies (Gryboski 1969). In this study we have viewed the mechanisms of their ‘failures’ and their ‘alternative’ efforts to protect the airway. This appears to be achieved by alternation of periods of apnoea during vigorous feeding with ‘breathing bursts’, during which feeding is suspended, and by blocking the teat with the tongue (see Fig. 4). These ‘alternative’ patterns were not seen in infants with consistent 1:1: 1 feeding. As a group, the infants with uncoordinated tongue movements had fewer coordinated 1 :1 :1 sequences than those who did not. However, there was no obvious, absolute relationship between the frequency of the abnormal tongue movements and the frequency of 1:1:1 sequences. Moreover, the number of infants in this study was insufficient to determine whether tongue co-ordination and suck-swallow-breath co-ordination develop independently or in parallel. Relatively few immature infants were studied. Since only those judged by nursing staff to be ‘safe to feed’ were included, it is not possible to state definitely that the abnormalities observed are representative of all preterm infants or clinically uncoordinated feeders. However, our experi-
ence with non-nutritive sucking by very preterm infants with gestations of 28 to 32 weeks (not part of this study) suggests that the movements are representative. The movements appear to progress from bizarre writhings of the tongue (e.g. around the endotracheal tube or inserted finger-tip), including occasional overt sucks, to the mixed pattern seen in our least mature study infants. Such movements can also be observed in utero at similar gestations. This suggests, as do the results above, that such developmental progression depends more on physiological neuromuscular maturity than on any particular extraneous stimulus. Abnormal feeding movements are also seen occasionally in term infants. A variety of patterns was seen in a separate series of term babies with identified feeding problems studied by the same method (unpublished data). Some patterns were almost identical to those seen in the preterm infants in the present study. Although many were due to developmental abnormalities, some of the abnormal feeding patterns could be explained by the novel ways the baby used to keep the airway open during feeding having become habitual. Thus the persistence of preterm feeding patterns can consistitute feeding ‘habits’, and can be due, in part, t o adverse early experience (e.g. breathing difficulties during feeding). While we would not consider abnormal tongue movements at
the ‘appropriate’ gestational age to be pathological, they may become so if they are inadvertently reinforced. Further studies may provide a clearer understanding of the mechanisms underlying feeding abnormalities in term and preterm infants. Real-time ultrasound studies, linked to respiratory monitoring, have provided new information about the development of feeding co-ordination in preterm infants. They suggest that their feeding failure is caused more by neuromuscular immaturity than by lack of experience. Assessment of feeding function by this technique allows comparison with the performance ‘expected’ at a particular gestational age, and may be helpful in prognosis.
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Accepted for publication 3rd October 1989. Acknowledgements We are grateful to Dr. A. J. Wilkinson, Consultant Paediatrician, Neonatal Unit, John Radcliffe Maternity Hospital, for permission to study his patients; to the parents and nursing staff for their co-operation; and to Lewis Woolf Griptight Ltd. for partial funding of this project. M.W.W. is also funded by a grant from The Health Promotion Research Trust (Grant No. 163) and from Birthright (Royal College of Obstetricians and Gynaecologists No. B1/87). Authors’ Appointments *Frances Bu’Lock, M.A., M.R.C.P.; M. W. Woolridge, B.Sc., D.Phil.; J . D. Baum, M.D., F.R.C.P.; Institute of Child Health, University of Bristol, Royal Hospital for Sick Children, St. Michael’s Hill, Bristol BS2 8BJ. ‘Correspondence lo first author.
SUMMARY Fourteen newborn babies of different gestational ages (33 to 40 weeks) but similar postnatal age (four to 19 days) were studied during bottle-feeding using real-time ultrasonography, combined with respiratory monitoring. Previously undescribed tongue movements and graded changes in the temporal relationships between tongue movements, swallowing and breathing were observed among infants of differing maturity. These were most marked in the least mature infants, but were occasionally seen in term infants. The results suggest that adequate neuromuscular co-ordination is more a function of gestational maturity than of postnatal sucking experience. The pattern of intraoral events for infants of differing maturity described in this study provides a framework for the study of feeding problems of term and preterm infants. RESUME Developpement de la coordination, de la succion, de la deglutition et de la respiration chez les nourrissons nes a terme et chez les prematures Quatorze nouveaux-nes d’8ges differents de gestation (33 a 40 semaines) mais d’8ges post-nataux semblables (quatre a 19 jours) ont ete etudies durant I’alimentation au biberon en utilisant une echographie en temps reel combinee avec un contrBle respiratoire. Des mouvements de langue non decrits anterieurement et des modifications graduees dans les relations temporelles entre les mouvements de langue, la deglutition et la respiration ont ete observes chez les nourrissons de differentes maturites. 11s etaient au plus eleve chez les moins matures des enfants etudies mais observes occasionnellement chez les nourrissons a terme. Les resultats suggerent que la coordination neuro-musculaire adequate est plus une fonction de la maturite de gestation que de l’experience postnatale de succion. La distribution des evenements intra-oraux pour les nourrissons de differentes
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maturites decrites dans cette etude fournit une base de travail pour I’etude des problemes d’alimentation chez les nourrissons a terme et prematures.
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Koordinationsentwicklung von Saugen, Schlucken und Atmen bei reif- und friihgeborenen Kindern Bei 14 Neugeborenen mit verschiedenem Gestationsalter (33 bis 40 Wochen), aber etwa gleichern Lebensalter (vier bis 19 Tage) wurden wahrend der Flaschenfiitterung Real-Zeit Ultraschalluntersuchungen mit gleichzeitigen Aufzeichnungen der Atmung durchgefuhrt. Es wurden bisher nicht beschriebene Zungenbewegungen und abgestufte Veranderungen in der zeitlichen Relation zwischen Zungenbewegungen, Schlucken und Atmen bei Kindern mit unterschiedlichem Reifegrad festgestellt. Diese waren bei den unreifsten Kindern a m ausgepragtesten, wurden aber auch bei einigen reifen Kindern beobachtet. Die Ergebnisse zeigen, daR eine richtige neuromuskulare Koordination eher eine Funktion der Gestationsreife als der postnataleri Saugerfahrung ist. Die Muster intra-oraler Ablaufe bei Kindern unterschiedlicher Reife, die in dieser Studie beschrieben werden, bilden die Basis fur Untersuchungen von Fiitterungsproblemen bei reif- und friihgeborenen Kindern.
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RESUMEN Desarrollo d e la coordinacion d e la succion, deglucion y respiracion en lactantes a termino y pretermino Catorce recien nacidos de diferentes edades gestacionales (33 a 4 0 semanas) pero de edad postnatal similar (de cuatro a 19 dias) fueron estudiados durante la toma del biberon usando una ultrasonografia a tiempo real en combinacibn con la monitorizacion de la respiracion. Entre 10s lactantes con diferente madurez se observaron movimientos de lengua no descritos previamente, asi como cambios graduales en las relaciones temporales entre 10s movimientos de la lengua, la deglucion y la respiracion. Esto era marcado sobre todo en 10s lactantes menos maduros mientras que se observaron raramente en 10s lactantes a termino. Los resultados sugieren que la adecuada coordinacion neuromuscular es mas una funcion de la maduracion gestacional que de la experiencia succional postnatal. El esquema de 10s acontecimientos intraorales en lactantes de diferente madurez descritos en este estudio proporciona un marco para el estudio de 10s problemas de alimentacion de lactantes a termino y a pretermino. References Ardran. G. M.. Kemu, F. H.. Lind. J . (1958a) ‘A cineradiographic stbdy of bottle feeding.’ British Journal of Radiology, 31, 11-22. _ _ _ (1958b) ‘A cineradiographic study of breast feeding.’ British Journal of Radiology, 31, 156- 162.
B a h t , M. (1948) ‘Individual differences of behavior in early infancy, and an objective method for recording them. 11: Results and conclusions.’ Journal of Genetic Psychology, 13, 8 1-1 17. Colley, J. R. T., Creamer, B. (1958) ‘Sucking and swallowing in infants.’ British Medical Journal, 2, 422-423.
Daniels, H., Casaer, P., Devlieger, H., Eggermont, E. (1986) ‘Mechanisms of feeding efficiency in preterm infants.’ Journal of Pediatric Gastroenterology and Nutrition, 5, 593-596. Darwin, C. (1877) ‘A biographical sketch of an infant.’ Mind, 285-294. (Reprinted 1971 as Supplement No. 24 to Developmental Medicine and Child Neurology.) Doty, R. W. (1968) ‘Neural organization of deglutition.’ In Code, C. F. (Ed.) Handbook of Physiology, Vol. 6, Part I V: Alimentary Canal. Washington, D.C.: American Physiological Society, pp. 1861-1902. Farriaux, J . P., Milbled, G. (1967) ‘Deglutition in the newborn.’ Medical and Biological Illustration,
17, 191-197. Grvboski. J . 11969) ‘Suck and swallow in the premature infant.; Pediatrics, 43, 96-102. Hack, M., Estabrook, M. M., Robertson, S. S. (1985) ‘Development of sucking rhythm in preterm infants.’ Early Human Development, 11, 133-140.
Halverson, H. M. (1944) ‘Mechanisms of early infant feeding.’ Journal of Genetic Psychology,
64, 185-223.
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Johnson, P., Salisbury, D. M. (1977) ‘Preliminary studies on feeding and breathing in the newborn. In Weiffenbach, J . M. (Ed.) Taste and Development: the Genesis of Sweet Preference. Department of Health, Education, and Welfare,
Publication No. (NIHJ77-1068. Bethesda, MD: National Institutes of Health. Kron, R . E., Stein, M., Goddard, K . E. (1963) ‘A method of measuring sucking behaviour in newborn infants.’ Psychosomatic Medicine, 25, 181-191.
Logan, W. J., Bosma, J. F. (1967) ‘Oral and pharyngeal dysphagia in infancy.’ Pediatric Clinics of North America, 14, 47-61. Meier, P., Anderson, G. C. (1987) ‘Responses of small preterm infants to bottle- and breastfeeding. American Journal of Maternal and Child Nursing, 12, 97-105. Miller, A. J. (1982) ‘Deglutition.’ Physiological Review, 62, 129-183. Peiper, A. (1963) Cerebral Function in Infancy and Childhood. (Translation of: Die Eigenart der Kindlichen Hirntatigkeit, 3rd edn, 1961.) New York: Consultants Bureau. Selley, W. G., Ellis, R. E., Flack, F. C., Curtis, H., Callon, M. (1986) ‘Ultrasonographic study of sucking and swallowing by newborn infants. Developmental Medicine and Child Neurology, 28, 820-823. (Letter.) Smith, W. L., Erenburg, A,, Nowak, A., Franken, E. A. (1985) ‘Physiology of sucking in the normal term infant using real-time US.’ Radiology, 156, 379-381.
Weber, F., Woolridge, M. W., Baum, J . D. (1986) ‘An ultrasonographic study of the organisation of sucking and swallowing by newborn infants.’ Developmental Medicine and Child Neurology,
28, 19-24.
Wolff, P. H . (1968) ‘The serial organization of sucking in the young infant.’ Pediatrics, 42, 943-956.
Woolridge, M. W. (1986) ‘The ‘anatomy’ of infant sucking.’ Midwifery, 2, 164-171. - Drewett, R. F. (1986) ‘Sucking rates of human babies on the breast: a study using direct observation and intra-oral pressure measurements.’ Journal of Reproductive and Infant Psychology, 4, 69-75.
Establishing effective feeding is a prerequisite for the survival of newborn infants. Efficient and safe feeding requires co-ordination of breathing with sucking and swallowing and involves the functional interaction of lips, jaw, tongue, palate, pharynx, larynx and oesophagus (Doty 1968, Miller 1982). There is increasing interest in the sucking performance of preterm infants (Daniels et al. 1986), but few studies have increased our knowledge of the development of feeding co-ordination during fluid intake (cf non-nutritive sucking-Hack et al. 1985). Feeding difficulties make up a major proportion of the problems that arise in otherwise healthy term and preterm infants. In order to intervene appropriately, the problem must be adequately defined. This can usually be done by careful history-taking and examination, combined with observing the mother feeding her baby. Occasionally, however, more specialised investigation is indicated, including the imaging of events occurring inside the baby’s mouth. A variety of electrophysiological and radiographic techniques have been used experimentally to define the intra-oral organisation of the feeding process (Halverson 1944, Kron et al. 1963, Johnson and Salisbury 1977, Woolridge and Drewett 1986). Of these, cineradiography has been the most useful
(Ardran et al. 1985a, b); however, the risks of irradiation restrict the use of this technique. Recently it has become possible to image intra-oral events during feeding by using real-time ultrasound (Smith et al. 1985, Weber et al. 1986). This technique has no known sequelae, and allows imaging at the bedside in the ‘normal’ feeding position for mother and infant, whether breast-feeding or bottle-feeding. There is little information in the literature about the development of feeding co-ordination in preterm infants (Gryboski 1969). The present study examined the way in which preterm infants co-ordinate sucking, swallowing and breathing during bottle-feeding. Meier and Anderson (1987) suggest that babies may be developmentally competent to breast-feed at an earlier stage than that at which they can bottle-feed. However, we elected to study the infants during bottle-feeding, as this permitted standardisation of feeding across babies, which would not have been possible with breast-feeding.
Normal feeding dynamics There are diverse opinions in the literature about the organisation of the normal feeding process (Woolridge 1986), but the general consensus for term infants is that a bolus of fluid is delivered to the pharynx by a phased application of the dorsum of
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Fig. 1. Feeding movements. I. ‘Resting’ posifion. Teat is held firmly and fully within mouth, with tongue beneath teat. Soft palate is relaxed and nusopharynx is in continuity wifh trachea. Laterally, tongue and buccal mucosa form seal around teat to roof of mouth.
04
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2. This view is approximately 0.25sec later than in I (similar interval separates subsequent views). Lower jaw is elevated, compressing base of teat, while front of tongue moves upward, initiating expression of milk from teat; back of tongue is depressed, leaving space for milk to collect.
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3. Wave of upward movement of tongue progresses backward, further expressing milk from teat into mouth. This is facilitated by negative pressure generafed by downward movement of back of tongue and of lower jaw.
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the tongue to the nipple or teat in an antero-posterior peristaltic wave of contraction. Co-ordinated movement o’f the mandible and apposition of the gums traps milk in the lacteal sinuses of the breast or teat of the bottle. Milk is then expressed, by compression of the ‘teat’, into the pharynx. This is assisted by the negative intra-oral pressure generated posteriorly by lowering of the jaw and posterior depression of the tongue which occur during this movement sequence. From the pharynx, a series of reflex
muscular contractions and relaxations transfer milk into the oesophagus and onward into the stomach by peristalsis (and gravity). At the same time, milk is prevented from entering the nasal/ tracheal airway by elevation of the soft palate and closure of the larynx. The exact relative contributions of intra-oral negative pressure and of nipple compression to the process of transferring milk from the breast or bottle to the baby are controversial. However, efficient feeding probably requires co-ordinated
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4. The swallow. A s wave of tongue contraction sweeps off back of teal, it impinges on soft palate, thus sealing milk within oropharynx. Swallowing is triggered, levator muscles of palate contract and nasal cavity is sealed off from milk, aided by contraction of muscles of posterior pharyngeal wall. Upward movement of laryngohyoid complex, approximation of arytenoids and movement of epiglottis effectively close off airway. Only at this point in feeding cycle is airway closed and breathing temporarily interrupted. Milk is then propelled into upper oesophagus, whence it is expelled into stomach by peristalsis.
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5. A s in I , soft palate returns to resting position, larynx descends and airway re-opens. Tongue is then in position f o r another sucking cycle to commence, a complete cycle lasting approximately Isec. Anterior segment of tongue begins to move again, before contraction of posterior segment is fully complete.
6. Breast-fed infant at ‘rest’. Note that tongue is extended more anteriorly, and there is deeper penetration of nipple than of bottle teat. Unlike bottle teat, human nipple does not recoil elastically in vertical plane, so is maintained in moderate state of compression.
tongue- and jaw-movements, producing both positive expression pressure and negative suction pressure (Darwin 1877, B a h t 1948, Colley and Creamer 1958, Farriaux and Milbled 1967). Thus, as first described by Ardran et al. (1985a, b), there is a basic, repetitive, rhythmic rolling movement of the tongue, produced by differential contraction of the longitudinal and transverse intrinsic musculature of the tongue. The best visualisations of feeding movements were obtained in the lateral/sagittal plane by Ardran and
colleagues for both breast-fed and bottlefed babies. Based on their work, and on more recent observations of the dynamic three-dimensional process of feeding with the use of ultrasound (Smith et al. 1985, Weber et al. 1986), we have compiled the pictorial representations shown in Figure 1 . The process is shown for a term infant bottle-feeding, to facilitate comparison with the ‘abnormal’ features described in the present study, and a single stage during breast-feeding is inset for comparison. We have noted relatively few
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TABLE I Characteristics of infants studied Group
N
Birth weight
(s)
Age at study (days)
Postconceptional age (wks)
1 (33-34 wks) 2 (35-36 wks) 3 (37+ wks)
5 4
1750-2173 1905-2650 2650-3860
10-19 4-7 4-7
34.5-37 36.5-37.5 38.5-41
5
qualitative differences in sucking behaviour on a bottle compared with the breast. One feature, shown in Figure 1 , is that during bottle-feeding the tongue is not projected so far forward as during breast-feeding.
Co-ordination of normal feeding In a normal, co-ordinated, nutritive* sucking cycle, breathing is interpolated between swallows, a fact which has been overlooked historically (Balint 1948, Pieper 1963). In a perfectly co-ordinated cycle, suck, swallow and breathing movements are related in a 1:l:l sequential pattern (Halverson 1944, Wolff 1965, Johnson and Salisbury 1977, Weber et af. 1986). These form a rhythmically repetitive unit, in which breathing appears to be continuous and uninterrupted. During less well co-ordinated feeding, breathing is always interrupted by swallowing (Halverson 1944, Logan and Bosma 1967, Weber et al. 1986), and indeed may be subordinate to it (Johnson and Salisbury 1977).
Material and method Subjects In this cross-sectional study of 14 infants, nutritive and non-nutritive feeding movements were observed in three groups of normally grown, bottle-feeding babies, defined according to gestational age at delivery (Table I). Gestational age was determined by obstetrical assessment of last menstrual period and/or ultrasound scan. The study was approved by the Regional Ethical Committee. The parents were given a printed explanatory sheet
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*Operationally defined for bottle-feeding as that type of sucking observed when fluid is delivered from the teat (cfnon-nutritive sucking when fluid is withheld).
and their informed verbal consent was obtained. Previous research suggests that it may take three to four days for ‘normal’ feeding to become established in term babies. Day four postpartum therefore was chosen as the earliest day for the study of term infants. The preterm babies were studied as early as possible after starting sucking feeds, which began independently of the study as determined by experienced nursing staff. There was some overlap, therefore, between groups 1 and 2 in their postconceptional age at the time of study, but a clear difference remained between groups 1 and 3. Babies were not included in the study if there was evidence of complications of preterm birth: Apgar < 8 at five minutes; respiratory distress requiring artificial ventilation for > 12 hours; or other postnatal complications, including severe jaundice (peak bilirubin > 240pmoV~). Eight male and six female infants were recruited. At the time of study, all babies were being predominantly bottle-fed. All group 1 infants had been given tube-feeds initially, followed by bottle-feeds, although efforts were being made to establish breast-feeding in two cases. A11 group 2 and 3 infants were wholly bottle-fed. During the study the babies were fed with either Cow & Gate ‘Premium’ formula or expressed breast-milk in a standard glass bottle with a disposable teat. There was a one- to two-minute period of sucking on a sealed teat (nonnutritive sucking) at the beginning, midpoint or end of each feed to allow comparison of nutritive and non-nutritive sucking performance. The volumes of each baby’s three previous feeds were noted, and the
midpoint of the test feed was predetermined as half the mean of these volumes. The mean volumes varied from 3 0 m ~for small babies to 7 0 m ~for larger ones.
Scans The scans were performed using an ATL 20 MK300C real-time ultrasound scanner with a 7.5MH.z scanhead (Advanced Technology Labs. Inc.). The image was inverted and adjusted so that the teat always appeared on the left of the screen. Depth and contrast were adjusted for each baby t o optimise the quality of the image. The frame counter was activated at the start of each feed. All feeds were recorded on a linked VHS video-recorder. Recordings were made throughout any period when the teat was in the baby’s mouth; however, the technique did not always permit a completely continuous record. A Graseby Dynamics Apnoea Alarm was attached to the baby with elasticated adhesive tape over the anterolateral thoraco-abdominal junction. This provides reliable compression and triggering of the sensor on inspiration, whether breathing is predominantly abdominal or thoracic, thereby overcoming the problems that Selley and colleagues (1986) encountered with such a device. The output from the alarm was connected to the ECG input of the scanner via a variable KC^ resistor to produce a clear signal on the in-built ECG display facility. The device also produces a simultaneous audible ‘click’, which was recorded, together with any comments during the feed, via the microphone input onto the video record. Previous studies have shown that maximum information from a single view is obtained from the submental midline sagittal plane, so all scans were recorded from that position. Possible additional information from coronal scanning (Smith et al. 1985) was sacrificed in order to obtain near-continuous recordings of the feeds. Feeds The breath sensor was positioned and adjusted. The baby was fed in the usual position at the usual time, either by the mother, or if this was usually the case, by
a nurse. There were pauses for ‘winding’ as necessary. The babies were allowed to feed to satiety, or to their maximum milk allowance in the case of preterm babies, and feeds lasted for an average of 30 minutes. Mothers said that they did not feel that the scanning process materially affected the feeds.
Analysis Each scan was viewed several times at both normal and slow speeds. The scans were reviewed in random order, without knowledge of the infants’ maturity. A qualitative description of the type and frequency of tongue movements was noted, as were temporal relationships between the three separate eventssucking, swallowing and breathing-and any changes in these relationships during the feed. The relative proportions of time spent in nutritive and non-nutritive sucking were also noted. We were unable to obtain continuous records of every complete feeding sequence, so it was not possible to quantitate the exact proportions of feed occupied by the various sucking patterns seen. Consequently, a scoring system was used throughout each scan. A formal statistical analysis would not be appropriate for a study of this kind, in which a large proportion of observations are concerned with the nature and quality of certain activities.
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Results Interpretable scans were obtained for all infants throughout one entire feed. Although the quality of the scans varied, it was always possible to identify separately the teat, tongue and palate for most of each feed (Fig. 2). At rest, the palate is separated from the tissues adjacent to the scanhead by the air gap of the nasopharynx, so it is difficult t o identify the palate at rest or during non-nutritive sucking, except when (presumably) saliva is being swallowed. However, swallowing could also be identified by upward movement of the hyoid and anterior cervical tissues, as well as occasionally by peristaltic movements of the upper oesophagus. No infant had any external evidence of mechanical feeding difficulties, gagging
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TABLE I1
Summary of results Group I (33-34 WkS)
Group 2 (35-36 wks)
Group 3 (37-40 wks)
++ +
+ +
0 0
++
++
+++
Suck:swallow:breath ratio: 1:l:l other
++ ++
++
+ + t
Breathing abnormalities: ‘Apnoeas’ ‘Breath bursts’ Abnormalities: trend during course of feed
++
+
+/-
+/-
Increase
Some increase
Nutritive sucking Tongue movements: ‘Abnormal’ ‘Obstructive’ Suck:swallow ratio: 1:l
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2:1-4: 1
Non-nutritive sucking Tongue movements: ‘Abnormal’ ‘Obstructive’ Relationship of sucking to breathing Sucks disrupt regular ‘at rest’ breathing Breathing abnormalities: ‘Apnoeas’ ‘Breath bursts’ Abnormalities: trend during course of feed Code: 0 =none; + + + times/absent at others.
+
+
++
+/-
+/-
+/-
No trend
+
+/-
0
0
+/
++
+/-
+/-
+
0
0 +/-
Some increase
No trend
0 0 No trend
+ t
+
+
0
+ + + =present (by degree); + / - =present at
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or distress during the test feeding. Major features of the scans for each group of infants are summarised in Table 11. (Full details for individual babies are available on request.) No differences in feeding behaviour were noted between babies receiving formula feeds and those receiving expressed breast-milk (cf Johnson and Salisbury 1977). Tongue movements The normal mature pattern of tongue movements during sucking (as described above) was dominant throughout the feed in all three groups. However, various ‘abnormal’ movement patterns were seen, particularly among infants in group 1 (33 to 34 weeks). These were less evident among group 2 infants (35 to 36 weeks) and virtually absent in group 3 (37 to 40 weeks). The movements took three forms:
(1) incomplete or fragmentary peristaltic
waves of motion passing along the tongue, starting from and finishing at abnormal regions of the tongue and/or progressing in a posterior-anterior direction (Fig. 3); both the direction and duration of these movements were unpredictable; (2) apparently purposeless ‘non-peristaltic’ movements, which appeared as flickering or writhing movements in the two-dimensional view; (3) twitching or tremulous movements (‘microtremors’), probably equivalent to the ‘Quiver frequency’ noted by B a h t (1948). These tongue movements were more conspicuous during nutritive than nonnutritive sucking in both group 1 and 2 infants. They lessened during the course of the feed in four infants, but increased in two others.
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8
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Fig. 2. Scan at moment of swallowing by infant of38 weeks gestation (as in 4 in Fig. I ) .
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-- ‘Tong u e “-Teat Respiratory trace Fig. 3. Scan demonstrating abnormal contraction of tongue by infant of 33 weeks gestation.
/- - - - - - - --Hard Palate
‘.
- ‘Reverberation Artefact’
--.
-Tongue
‘‘Teat
Fig. 4. Scan showing ‘teat blocking’ by infant of36 weeks gestation.
6 75
Some babies closed off the end of the teat by raising the tip or distal portion of the tongue (Fig. 4). Again, this was more common among group 1 infants and was not seen in group 3.
Co-ordination of sucking and swallowing Co-ordination of sucking and swallowing was far more consistent in babies with longer gestations. In addition, whereas four of the five infants in group 1 showed up to four sucks per swallow for much of the feed, the term infants showed a 1:1 ratio of sucks to swallows for a much higher proportion of the feed. Swallows were rarely observed during non-nutritive sucking at any gestational age. Sucking, swallowing and breathing It was readily apparent that all babies in the study achieved some periods of 1:l:l sequential linking of sucking, swallowing and breathing. The proportion of the feed in which this ratio occurred increased fairly uniformly with maturity, unlike other ratios. In the more preterm infants, sucking occasionally disrupted the regular, quiet breathing of an awake infant, but this was rarely seen in term infants. Such disruption was manifested by periods of sucking (usually associated with regular but asynchronous respiratory movements) being interrupted by a period of rapid breathing unaccompanied by sucks (‘breathing bursts’). This has also been described by Halverson (1944) and more recently by Selley et al. (1986). Similarly, term babies did not exhibit the ‘apnoeic’ pause in breathing movements during nutritive sucking which were prominent in group 1 babies and occurred occasionally in those in group 2.
Discussion
676
The co-ordination of the intrinsic muscles of the tongue to produce fully-formed rhythmic, rolling movements seems t o be, at least in part, a product of gestational maturity. This is suggested by the fact that the preterm babies had more poorly co-ordinated tongue movements, despite being ‘older’ in ex utero age than the term babies at the time of the study. The synchronised co-ordination of sucking, swallowing and breathing to produce a ratio of 1:l:l during feeding
appears to be the preferred (and therefore presumably optimal) mode of feeding of term infants. This agrees with observations in other studies (Halverson 1944, B a h t 1948, Wolff 1968, Weber et al. 1986). The sequential linkage of sucking to swallowing and of swallowing to breathing also appears to approach the 1:1:1 ratio more often with increasing gestational maturity. This seems to require the simultaneous mastery of successful intrinsic tongue movements (providing a bolus of milk sufficient to initiate a swallow) and protection of the airway while maintaining regular breathing. In our small series, the linkage of sucking and swallowing with breathing appeared to be achieved consistently only by infants of more than 37 weeks postconceptional age. The linkage of sucking to swallowing usually is well established by 32 weeks, which is not surprising since swallowing can occur in utero from about 11 weeks gestation (Miller 1982). Preterm babies are notably less efficient at ‘safe’ feeding than term babies (Gryboski 1969). In this study we have viewed the mechanisms of their ‘failures’ and their ‘alternative’ efforts to protect the airway. This appears to be achieved by alternation of periods of apnoea during vigorous feeding with ‘breathing bursts’, during which feeding is suspended, and by blocking the teat with the tongue (see Fig. 4). These ‘alternative’ patterns were not seen in infants with consistent 1:1: 1 feeding. As a group, the infants with uncoordinated tongue movements had fewer coordinated 1 :1 :1 sequences than those who did not. However, there was no obvious, absolute relationship between the frequency of the abnormal tongue movements and the frequency of 1:1:1 sequences. Moreover, the number of infants in this study was insufficient to determine whether tongue co-ordination and suck-swallow-breath co-ordination develop independently or in parallel. Relatively few immature infants were studied. Since only those judged by nursing staff to be ‘safe to feed’ were included, it is not possible to state definitely that the abnormalities observed are representative of all preterm infants or clinically uncoordinated feeders. However, our experi-
ence with non-nutritive sucking by very preterm infants with gestations of 28 to 32 weeks (not part of this study) suggests that the movements are representative. The movements appear to progress from bizarre writhings of the tongue (e.g. around the endotracheal tube or inserted finger-tip), including occasional overt sucks, to the mixed pattern seen in our least mature study infants. Such movements can also be observed in utero at similar gestations. This suggests, as do the results above, that such developmental progression depends more on physiological neuromuscular maturity than on any particular extraneous stimulus. Abnormal feeding movements are also seen occasionally in term infants. A variety of patterns was seen in a separate series of term babies with identified feeding problems studied by the same method (unpublished data). Some patterns were almost identical to those seen in the preterm infants in the present study. Although many were due to developmental abnormalities, some of the abnormal feeding patterns could be explained by the novel ways the baby used to keep the airway open during feeding having become habitual. Thus the persistence of preterm feeding patterns can consistitute feeding ‘habits’, and can be due, in part, t o adverse early experience (e.g. breathing difficulties during feeding). While we would not consider abnormal tongue movements at
the ‘appropriate’ gestational age to be pathological, they may become so if they are inadvertently reinforced. Further studies may provide a clearer understanding of the mechanisms underlying feeding abnormalities in term and preterm infants. Real-time ultrasound studies, linked to respiratory monitoring, have provided new information about the development of feeding co-ordination in preterm infants. They suggest that their feeding failure is caused more by neuromuscular immaturity than by lack of experience. Assessment of feeding function by this technique allows comparison with the performance ‘expected’ at a particular gestational age, and may be helpful in prognosis.
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Accepted for publication 3rd October 1989. Acknowledgements We are grateful to Dr. A. J. Wilkinson, Consultant Paediatrician, Neonatal Unit, John Radcliffe Maternity Hospital, for permission to study his patients; to the parents and nursing staff for their co-operation; and to Lewis Woolf Griptight Ltd. for partial funding of this project. M.W.W. is also funded by a grant from The Health Promotion Research Trust (Grant No. 163) and from Birthright (Royal College of Obstetricians and Gynaecologists No. B1/87). Authors’ Appointments *Frances Bu’Lock, M.A., M.R.C.P.; M. W. Woolridge, B.Sc., D.Phil.; J . D. Baum, M.D., F.R.C.P.; Institute of Child Health, University of Bristol, Royal Hospital for Sick Children, St. Michael’s Hill, Bristol BS2 8BJ. ‘Correspondence lo first author.
SUMMARY Fourteen newborn babies of different gestational ages (33 to 40 weeks) but similar postnatal age (four to 19 days) were studied during bottle-feeding using real-time ultrasonography, combined with respiratory monitoring. Previously undescribed tongue movements and graded changes in the temporal relationships between tongue movements, swallowing and breathing were observed among infants of differing maturity. These were most marked in the least mature infants, but were occasionally seen in term infants. The results suggest that adequate neuromuscular co-ordination is more a function of gestational maturity than of postnatal sucking experience. The pattern of intraoral events for infants of differing maturity described in this study provides a framework for the study of feeding problems of term and preterm infants. RESUME Developpement de la coordination, de la succion, de la deglutition et de la respiration chez les nourrissons nes a terme et chez les prematures Quatorze nouveaux-nes d’8ges differents de gestation (33 a 40 semaines) mais d’8ges post-nataux semblables (quatre a 19 jours) ont ete etudies durant I’alimentation au biberon en utilisant une echographie en temps reel combinee avec un contrBle respiratoire. Des mouvements de langue non decrits anterieurement et des modifications graduees dans les relations temporelles entre les mouvements de langue, la deglutition et la respiration ont ete observes chez les nourrissons de differentes maturites. 11s etaient au plus eleve chez les moins matures des enfants etudies mais observes occasionnellement chez les nourrissons a terme. Les resultats suggerent que la coordination neuro-musculaire adequate est plus une fonction de la maturite de gestation que de l’experience postnatale de succion. La distribution des evenements intra-oraux pour les nourrissons de differentes
677
maturites decrites dans cette etude fournit une base de travail pour I’etude des problemes d’alimentation chez les nourrissons a terme et prematures.
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ZUSAMMENFASSUNG
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Koordinationsentwicklung von Saugen, Schlucken und Atmen bei reif- und friihgeborenen Kindern Bei 14 Neugeborenen mit verschiedenem Gestationsalter (33 bis 40 Wochen), aber etwa gleichern Lebensalter (vier bis 19 Tage) wurden wahrend der Flaschenfiitterung Real-Zeit Ultraschalluntersuchungen mit gleichzeitigen Aufzeichnungen der Atmung durchgefuhrt. Es wurden bisher nicht beschriebene Zungenbewegungen und abgestufte Veranderungen in der zeitlichen Relation zwischen Zungenbewegungen, Schlucken und Atmen bei Kindern mit unterschiedlichem Reifegrad festgestellt. Diese waren bei den unreifsten Kindern a m ausgepragtesten, wurden aber auch bei einigen reifen Kindern beobachtet. Die Ergebnisse zeigen, daR eine richtige neuromuskulare Koordination eher eine Funktion der Gestationsreife als der postnataleri Saugerfahrung ist. Die Muster intra-oraler Ablaufe bei Kindern unterschiedlicher Reife, die in dieser Studie beschrieben werden, bilden die Basis fur Untersuchungen von Fiitterungsproblemen bei reif- und friihgeborenen Kindern.
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RESUMEN Desarrollo d e la coordinacion d e la succion, deglucion y respiracion en lactantes a termino y pretermino Catorce recien nacidos de diferentes edades gestacionales (33 a 4 0 semanas) pero de edad postnatal similar (de cuatro a 19 dias) fueron estudiados durante la toma del biberon usando una ultrasonografia a tiempo real en combinacibn con la monitorizacion de la respiracion. Entre 10s lactantes con diferente madurez se observaron movimientos de lengua no descritos previamente, asi como cambios graduales en las relaciones temporales entre 10s movimientos de la lengua, la deglucion y la respiracion. Esto era marcado sobre todo en 10s lactantes menos maduros mientras que se observaron raramente en 10s lactantes a termino. Los resultados sugieren que la adecuada coordinacion neuromuscular es mas una funcion de la maduracion gestacional que de la experiencia succional postnatal. El esquema de 10s acontecimientos intraorales en lactantes de diferente madurez descritos en este estudio proporciona un marco para el estudio de 10s problemas de alimentacion de lactantes a termino y a pretermino. References Ardran. G. M.. Kemu, F. H.. Lind. J . (1958a) ‘A cineradiographic stbdy of bottle feeding.’ British Journal of Radiology, 31, 11-22. _ _ _ (1958b) ‘A cineradiographic study of breast feeding.’ British Journal of Radiology, 31, 156- 162.
B a h t , M. (1948) ‘Individual differences of behavior in early infancy, and an objective method for recording them. 11: Results and conclusions.’ Journal of Genetic Psychology, 13, 8 1-1 17. Colley, J. R. T., Creamer, B. (1958) ‘Sucking and swallowing in infants.’ British Medical Journal, 2, 422-423.
Daniels, H., Casaer, P., Devlieger, H., Eggermont, E. (1986) ‘Mechanisms of feeding efficiency in preterm infants.’ Journal of Pediatric Gastroenterology and Nutrition, 5, 593-596. Darwin, C. (1877) ‘A biographical sketch of an infant.’ Mind, 285-294. (Reprinted 1971 as Supplement No. 24 to Developmental Medicine and Child Neurology.) Doty, R. W. (1968) ‘Neural organization of deglutition.’ In Code, C. F. (Ed.) Handbook of Physiology, Vol. 6, Part I V: Alimentary Canal. Washington, D.C.: American Physiological Society, pp. 1861-1902. Farriaux, J . P., Milbled, G. (1967) ‘Deglutition in the newborn.’ Medical and Biological Illustration,
17, 191-197. Grvboski. J . 11969) ‘Suck and swallow in the premature infant.; Pediatrics, 43, 96-102. Hack, M., Estabrook, M. M., Robertson, S. S. (1985) ‘Development of sucking rhythm in preterm infants.’ Early Human Development, 11, 133-140.
Halverson, H. M. (1944) ‘Mechanisms of early infant feeding.’ Journal of Genetic Psychology,
64, 185-223.
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Johnson, P., Salisbury, D. M. (1977) ‘Preliminary studies on feeding and breathing in the newborn. In Weiffenbach, J . M. (Ed.) Taste and Development: the Genesis of Sweet Preference. Department of Health, Education, and Welfare,
Publication No. (NIHJ77-1068. Bethesda, MD: National Institutes of Health. Kron, R . E., Stein, M., Goddard, K . E. (1963) ‘A method of measuring sucking behaviour in newborn infants.’ Psychosomatic Medicine, 25, 181-191.
Logan, W. J., Bosma, J. F. (1967) ‘Oral and pharyngeal dysphagia in infancy.’ Pediatric Clinics of North America, 14, 47-61. Meier, P., Anderson, G. C. (1987) ‘Responses of small preterm infants to bottle- and breastfeeding. American Journal of Maternal and Child Nursing, 12, 97-105. Miller, A. J. (1982) ‘Deglutition.’ Physiological Review, 62, 129-183. Peiper, A. (1963) Cerebral Function in Infancy and Childhood. (Translation of: Die Eigenart der Kindlichen Hirntatigkeit, 3rd edn, 1961.) New York: Consultants Bureau. Selley, W. G., Ellis, R. E., Flack, F. C., Curtis, H., Callon, M. (1986) ‘Ultrasonographic study of sucking and swallowing by newborn infants. Developmental Medicine and Child Neurology, 28, 820-823. (Letter.) Smith, W. L., Erenburg, A,, Nowak, A., Franken, E. A. (1985) ‘Physiology of sucking in the normal term infant using real-time US.’ Radiology, 156, 379-381.
Weber, F., Woolridge, M. W., Baum, J . D. (1986) ‘An ultrasonographic study of the organisation of sucking and swallowing by newborn infants.’ Developmental Medicine and Child Neurology,
28, 19-24.
Wolff, P. H . (1968) ‘The serial organization of sucking in the young infant.’ Pediatrics, 42, 943-956.
Woolridge, M. W. (1986) ‘The ‘anatomy’ of infant sucking.’ Midwifery, 2, 164-171. - Drewett, R. F. (1986) ‘Sucking rates of human babies on the breast: a study using direct observation and intra-oral pressure measurements.’ Journal of Reproductive and Infant Psychology, 4, 69-75.
