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Mouthing activities in the human neonatal sucking act
Arch od
Blol. Vol. 14, pp. 1159-I 167, 1969. Pergamoa Press. Printed ia Gt. Britain.
MOUTHING ACTIVITIES IN THE HUMAN NEONATAL SUCKING ACT M. L. SCNWTGEN, L. PIERCE and H. S. BRENMAN Departments of Pediatrics and Physiology Jefferson Medical College, Philadelphia, Pennsylvania 19107, U.S.A. Summary--Mouthing activities of the act of sucking and related variables were studied in ten normal newborn infants within the first week of life. Deglutition events were monitored by a contact microphone held in place on the neck. A specially adapted standard nipple was used to record lip and tongue movement and nutrient flow rate simultaneously but independently. Respiration and heart rate were recorded with a short-latency nasal thermistor and a digital photocell plethysmograph respectively. Two chara&ristic patterns of sucking activity were noted. One pattern consisted of periods of relatively constant sucking activity with short pauses between bursts. The second pattern showed short periods of sucking activity with longer pauses between bursts. Infants exhibiti the latter pattern obtained less volume per suck. Every one or two sucking movements occurred per respiration. Swallowing occurred most often at the end of inspiration or the beginning of expiration. Heart rate increased in most infants during sucking activity. Data collected can be readily analyxed for cataloguing and could aid in early diagnosis of pathological conditions. Measurement of neural interrelationships reilected by sucking and the respiratory and swallowing complex may be helpful in evaluating the neurological state of new-born infants and may possibly establish a relationship between neonatal patterns and subsequent growth and development. INTRODUCTION
THE ACT of infant feeding involves complex neural interrelationships of many physiologic mechanisms. An attenuation of the maturation process or an induced abnormality, such as brain damage, could adversely modify the normal, sequential interrelationships between respiration, sucking and deglutition with subsequent feeding problems and failure to thrive. The sucking act and related activities have been previously investigated in humans and animals. PEIPER(1963) has conducted extensive studies on newborn infants and has described the interrelationships between swallowing and respiration, swallowing and sucking, and sucking and respiration. His work has done much to establish patterns of neural interrelationships. In addition, ARDRAN,KEMP and LIND (1958) have conducted cineradiographic studies of the sucking act in human infants and animals in order to determine the role played by mouthing activities and pressures in the sucking act. They concluded that the expression of fluid into the oral cavity is accomplished by combined action of sub-atmospheric pressure and the action of compression of the nipple by the tongue and gums. COLLEY and CREAMER (1958), on 1159
1160
M. L. SOENTGEN, L. PIERCE AND H. S.
BRENMAN
the other hand, support the aspiration theory which attributes expression of fluid to the piston-like action of the tongue as it folds backwards. With recent advances in electronics facilitating the recording of many variables, the present study was initiated to develop and adapt external sensors which, by a multiparametric approach, could simultaneously but independently record sucking pressures and movements, respiration and the act of swallowing. Analytic techniques for analysis of data have been developed to assist in identifying emerging patterns of the feeding act. METHODS
AND
MATERIALS
Ten full-term infants, 2 to 4 days old, with average weights of 3000 g and no evidence of cardio-pulmonary, bucco-oesophageal, or central nervous system disease were selected at random for use in this study. The infant was transported to a testing room in close proximity to the newborn nurseries and remained in the transportation crib throughout the procedure. A paediatrician and two registered nurses were present during the testing. Deglutition events were monitored by means of a small, highly sensitive microphone (Sonotone RE-21030) placed on the neck lateral to the thyroid cartilage and held in place by light digital pressure. The microphone signals were processed by a Grass Polygraph (Model 7) and low-level DC preamplifier (Model 7Pl) and stored on a Roberts tape recorder (Model 990s). In order to establish acoustic patterns of swallowing sounds which could be used in clinical diagnosis, sound recordings were fed into an Ampex Multichannel FM Instrumentation Recorder and were: (1) expanded by playback at tape speeds one eighth the original recording speed and were displayed on a multichannel storage oscilloscope (Tektronix Model 564), and (2) submitted to Voiceprint Laboratories of Somerville, New Jersey, for sound spectrum analysis of the acoustic energy (MACKOWIAK,BRENMAN and FRIEDMAN,1967). These two methods demonstrate the reproducibility of sounds of swallowing. Respirations were recorded with the nasal sensor (MACKOWIAK,BRENMANand FRIEDMAN,1967) developed for this study. When placed in the vicinity of the nares, this sensor indicated the respiratory envelope by responding to temperature changes in inspired and expired air flow. Signals were processed by a low-level DC preamplifier (Grass 7Pl) and Polygraph (Grass Model 7), and standardized against the pneumograph and pneumotachograph. Five per cent glucose water was ingested through a multisensor nipple (BRENMAN et al., 1969) so constructed that oral activities and nutrient flow are recorded simultaneously but independently. The nipple was attached to a flow limiting device as illustrated in Fig. 1. With the apparatus arranged so that the side-arm burette and transducer are at the level of the infant’s mouth, fluid can only flow from the burette through the rubber tubing and resistance rod into the stainless steel tubing anchored in the nipple when intraoral pressure becomes subatmospheric. Flow exerts pressure against a column of fluid on either side of the resistance rod. These pressures are conveyed to either side of a diaphragm in the differential transducer (Sanborn Model 268B). P1 and P, are processed by a differential transducer converter (Sanborn Model
htownmci
ACTIVITIESINTHEHUMAN
NEONATAL
SUCKING
ACT
1161
Polygraph
Amplifier
Amplifier
FIG. 1. Multisensor nipple apparatus. When side-arm burette and transducer are placed on the level of the infant’s mouth, nutrient flow occurs only when intraoral pressure becomes subatmospheric.
592-300) where P, is subtracted from P,. AP is transmitted into a low-level DC preamplifier (Grass Model 7Pl) and is recorded on a polygraph (Grass Model 7) as a flow curve. Simultaneously, lip movement is recorded by means of the patent rubber tubing anchored within the intra-nipple compression chamber. When pressure is applied by lip and tongue movements, changes in intra-nipple pressure are conveyed to a differential pressure transducer (Statham Model P23AC) and into a low-level DC preamplifier (Grass Model 7Pl) and polygraph (Grass Model 7). The flow-limiting device of the multisensor nipple is a modification of a device described by KRON, STEIN and GODDARD (1963). We have substituted the Sanborn differential pressure transducer and converter for a Statham differential pressure transducer used by KRON et al. (1963). In this way, we were able to measure AP which was recorded as a fluid flow curve reflecting volume rate of flow. Flow volume can be obtained by calculating the area under the curve. The intra-nipple compression chamber is an innovation which enables simultaneous recording of oral activities as reflected by lip and tongue movements. Since the sucking complex involves both lip and tongue movements as well as intraoral pressure changes, this device makes it possible to investigate the temporal relationships between oral activities and nutrient flow. To complete the instrumentation, a digital photoelectric plethysmograph (Grass Model PTTl-7) was placed on the great toe and recorded heart rate. Signals from all the transducers were fed into a direct-writing polygraph (Grass Model 7). As indicated in Fig. 2, the infant is in no way restricted from normal activity and readily accepts the sensors. All sensors are easily sterilized by ethylene oxide gas sterilization.
1162
M. L. S~ENTGEN,L. PIERCEANDH. S. BRENMAN
FIG. 3. Polygraph recording of temporal interrelationships of the recorded variables in a 2-day old infant. Intra-nipple pressure recordings show an upward deflection when lips compress bulb of nipple and/or when pressure increases within oral cavity. Channel 2: Nutrient flow curve reflecting intraoral pressure. Plow occurs only when subatmospheric pressure is created. Channel 3: Respiration, with downward deflection of pen indicating inspiration. Channel 4: Sounds of swallowing. Arrow denotes one swallow and where it occurs in relation to other variables. Channel 5: Pulse rate as recorded by digital plethysmograph. Calibrations of intra-nipple pressure and nutrient flow are indicated on the right.
MOUTHING ACTIVITIES IN THE HUMAN NEONATAL SUCKING ACT
1163
RESULTS
Figure 3 demonstrates a portion of simultaneous ordinate recordings of intranipple pressure, nutrient flow, respiration, deglutition and pulse rate. Channel 1 represents oral activity as reflected by lip and tongue compression on the nipple and as recorded from the compression chamber within the nipple. Upward deflection indicated increased intra-nipple pressure and downward deflection indicated decreased intra-nipple pressure. When the nipple apparatus was positioned with the side-arm burette and the differential pressure transducer (Sanborn 268B) at the level of the infant’s mouth, fluid flowed only when the intraoral pressure became subatmospheric. Observation of channels 1 and 2 indicates that, as the intra-nipple pressure increased, the flow tapered off. As intra-nipple pressure decreased with cessation of lip compression, fluid flowed rapidly and was sustained for the duration of the decrease in intra-nipple pressure. The tracing on channel 1 also shows the intra-nipple pressure falling below baseline during the downward deflection when lip compression was absent. This is interpreted as representing the influence of the subatmospheric intraoral effects on that part of the compression chamber within the oral cavity. The individual effects of lip and tongue compression and intraoral pressure were demonstrated in several ways. When the flow tubing was clamped and lip and tongue activity was recorded without flow, the pen deflected upward as usual, but it returned only to baseline when compression was released. This would indicate that lip and tongue compression is responsible for the changes in intra-nipple pressures demonstrated by the deflection above baseline and the return to baseline. On the other hand, in several recordings, flow was recorded without noticeable lip activity suggesting creation of subatmospheric pressure without lip movements. In these cases, the lips were able to create the anterior seal without noticeable lip activity and flow occurred when intraoral pressure became subatmospheric. Changes in intraoral pressure were also reflected on the flow curve of channel 2 since nutrient flow could occur only with subatmospheric intraoral pressure. Channel 3 (Fig. 3) represents respiration as recorded by means of the nasal sensor which responds to temperature changes in inspiratory and expiratory air flow. Downward deflection represents inspiratory flow and upward deflection expiratory flow. Sounds of swallowing were recorded on channel 4 by means of the contact microphone held in place on the neck. The small deflections on the recording represent the swallowing sound whereas the larger deflections represent sucking noises. These noises decrease in frequency as the sucking burst becomes less active. Channel 5 represents heart rate as recorded by means of the digital plethysmograph placed on the infant’s great toe. Interrelationships between sucking movements, swallowing and respiration were determined by drawing a line through each swallow depicted on channel 4 and passing this line through all other tracings (Fig. 3). The number of sucking movements and respiratory cycles occurring between swallows was determined and ratios for sucking movements and respirations and for sucking movements and swallowing were established. Every one or two sucking movements were followed by a swallow occurring at the height of or at the end of flow. One or two sucking movements occurred per
1164
M. L. S~ENTGEN, L. PIERCE
AND
H. S.
BRENMAN
respiration. Sucking rate appeared to pace respiration. Swallowing occurred most frequently at the end of inspiration or the beginning of expiration. Heart rate was counted by the number of pulsations prior to sucking activity and during sucking activity. In all infants, heart rate increased IO-30 beats per min during sucking. These findings are in general agreement with those reported by PEIPER(1963). Graphic representation of the temporal interrelationships are shown in Fig. 4. The first bar graph represents intra-nipple pressure. The break in the bar indicates the end of one sucking movement and the beginning of the next. Upward oblique lines
I
Intronipple
pressure
2 Nutrient
flow
3 Respiration
4
q
Deglutition
Pulse
5 rate
I
’
I
q I
I
I
FIG.4. Bar graph representation of temporal relationships between intranipple pressure, nutrient flow, respiration, deglutition and pulse rate. The blank spaces on the bar graphs represent the end of one movement and the beginning of the next. Upward oblique lines on bars 1 and 2 represent increasing intranipple pressure due to increased lip compression and flow respectively. Downward oblique lines represent decreasing pressure and flow. Downward oblique lines on bar 3 represent inspiration shown as a downward pen deflection on Fig. 3. Upward oblique lines denote expiration. Each vertical line on bar 5 represent a pulse beat. The first swallow occurred as intranipple pressure began to increase at the end of flow and during respiration. There was one sucking movement per swallow and one swallow per respiration. The heart rate was 188 beats per min. indicate increasing intra-nipple pressure created by lip and tongue activity and downward oblique lines indicate decreasing pressure as the lip and tongue compression is released. The second bar graph represents nutrient flow. The breaks in the bar indicate the end of one flow curve and the beginning of the next. Upward oblique lines indicate increasing flow and downward oblique lines indicate decreasing flow. The third bar graph represents respiration. The break in the bar indicates the end of one respiratory cycle and the beginning of the next. Downward oblique lines indicate inspiration and upward oblique lines represent expiration. The two small squares on the fourth bar area represent swallows. The single line markings on the fifth bar represent pulse rate. The 1.6 set time period is associated with the portion of the recording on Fig. 3 indicated by the arrow. In this sequence, the first swallow (as indicated by the arrow) occurred with the initial increase of intraoral pressure at the end
MOUTHING
ACTIVITIES
IN THE HUMAN
NEONATAL
SUCKING
ACT
1165
of nutrient flow and during the expiratory phase of respiration. There is one sucking movement per swallow and one swallow during each respiratory cycle. The heart rate is approximately 188 beats per min representing an increase of approximately 30 beats per min caused by the sucking complex. In the ten series of recordings made, two patterns of sucking activity repeated themselves. One pattern, a portion of which is illustrated in Fig. 3, consisted of periods of relatively constant sucking activity of 15 set or longer and with short pauses of 5-10 set between bursts. A burst of sucking activity is defined as a series of continuous sucking movements without a pause. When a pause in the activity occurred, the burst was considered as ended. The average number of sucking movements per set in this pattern was greater than one but less than two. The second pattern of activity consisted of periods of shorter bursts of sucking activity lasting approximately 10-l 5 set with longer pauses (greater than 10 set). DISCUSSION
According to descriptions by ARDRAN,KEMPand LIND (1958) and PEIPER(1963), lip movements are initiated, at least in part, by the presence of the nipple on the lips. These movements position the nipple in the oral cavity and cease with the creation of an air seal. At the same time the rear of the oral cavity is sealed by apposition of the posterior tongue and soft palate. The lower jaw is raised and moved forward, the neck of the nipple is compressed between the maxillary ridge and tip of tongue covering the mandibular ridge. The movement of the tip of the tongue upward and backward expresses some of the nutrient into the mouth. The lower jaw drops, creating an increased intraoral volume which brings about a decrease in intraoral pressure. At this time the nipple is drawn into the oral cavity and flow occurs. Our data also demonstrated lip compression occurring prior to flow. This would correspond to the manipulation of the nipple and the raised lower jaw which moves forward. The role of expression of the nutrient by the tip of the tongue moving backward cannot occur with the multi-nipple apparatus as described, since flow can occur only with subatmospheric intraoral pressure. When the lip compression ceased, the intraoral pressure fell below atmospheric pressure and flow occurred. This action was indicated on both channels 1 and 2. The decreased intraoral pressure is indicated by a downward deflection on channel 1 and by increased flow on channel 2 (Fig. 3). This description of the sucking act and our findings emphasize the relationship of lip actions and intraoral pressure in expressing nutrient fluids. We feel that the multisensor nipple provided a means of establishing temporal relationships between these two variables in such a manner than they can be recorded during routine feeding. Deviations from normal patterns could be detected early. In this study, swallows occurred at the height of flow or end of flow. The posterior seal is maintained until sufficient fluid is present in the mouth. The tip of the tongue moves upward and backward and the posterior seal is lost. The fluid is propelled into the mesopharynx and the involuntary stages of swallowing occur. During the time of the swallowing events, other related activities cease. This is demonstrated in Fig. 3. During the swallowing event, a plateau occurred in the intra-nipple pressure as seen on
1166
M. L. SOENTGEN, L. PIERCE ANDH. S. BRENMAN
channel 1. A small deflection of the pen indicated this event on the flow curve of channel 2. Respiratory air flow ceased for a short interval as indicated by the pause in the expiratory flow which we designate as the swallowing inhibitory pause produced by the modification of respiration by the swallow. This would indicate that respirations can be dominated by the swallowing centre. These relationships have been noted by other investigators including PEIPER (1963). The temporal sequence between sucking movements and swallows and sucking movements and respiration suggest that sucking movements pace swallowing events and respirations. Every one or two sucking movements were followed by a swallow. PEIPER(1963) proposes that the sucking centre begins to function when a nipple-like object is placed in the infant’s mouth but that the swallowing centre is excited to produce a regular rhythm only when food is obtained. He also proposes that buccooesophageal swallowing depends for its rhythm upon sucking movements and may really represent a continuation of them. Our findings would confirm this supposition although it will be noted that in some cases more than one sucking movement occurred per swallow. This may indicate the necessity for a volume threshold to trigger a swallow. The respiratory rate also seems to depend upon the sucking movements for its rhythm. When sucking movements began, the respiratory rate increased and became irregular. As indicated in Fig. 3, when the sucking activity became less intense, swallowing became less frequent and the respiratory rate became more regular and slower. The fact that there is a locus of inhibition in respiration created by the swallowing events also lends support to PEIPER’S(1963) conclusion that the sucking centre dominates the respiratory centre. We can, therefore, conclude that the external sensors developed for this study provide the means for studying temporal neural interrelationships between sucking, deglutition and respiration. The sensors are non-restrictive, easily sterilized and accepted by the infants. They can be employed with standard recording instruments and contribute data that can be easily analyzed. Time expansion and sound spectrum analysis provide a means of establishing the reproducibility of swallows and characteristic sound patterns for normal and abnormal swallows. We feel that the establishment of a library of normal sound patterns could be an aid in early diagnosis of pathological conditions reflected in the feeding act. GE~ELL(1945) has used sucking as one criterion for evaluating neurological development in infants. We believe that measurement of neural interrelationships as reflected by the sucking, respiratory and swallowing complex could be helpful in evaluating not only the neurological state of the newborn infant, but also possibly in establishing a relationship between neonatal patterns and subsequent growth and development. Rkme--Les activites buccales au cows de la suction et ainsi, que les activitb annexes sont Btudikes chez dix enfants nouveau-n& normaux pendant la premiere semaine de vie. La deglutition est enregistree par I’intermddiaire d’un microphone de contact place au niveau de la nuque. Un biberon standard, spkcialement adapte, est utihse pour enregistrer simultanement, mais independemment, les mouvements de la fangue et des levres, ainsi que la vitesse d’kcoulement du liquide nuttitif. Les frequences respiratoire et cardiaque sont enregistrees respectivement ?I l’aide d’un thermistor nasal et d’un pletysmographe a cellule phototlectrique.
MOUTHINGAClTVtTIESIN THEHUMANNEONATAL SUCKING
ACT
1167
Deux modes de suction caractCristiques ont CtCnotes. L’un des types comporte des p&odes de suction relativement constante avec des repos courts entre les suctions. Le second type comprend des periodes de suction courtes, &par&s par des intervalles longs. Les enfants, utilisant ce demier mode, obtiemrent moins de volume liquidien par suction. Un ou deux mouvements de suction se produisent au tours d’un cycle respiratoire. La deglutition suit generalement la fin de l’inspiration ou le debut de l’expiration. La frequence cardiaque augmente chez la plupart des enfants pendant la suction. Les resultats obtenus pourraient servir dans le diagnostic de conditions pathologiques. La mesure des rapports nerveux entrant dans le complexe de suction, respiration et deglutition, peut etre utile pour tester l’dtat neurologique des nouveau-t&. Zusannnenfassung-Bei 10 gesunden neugeborenen Kindem wurden innerhalb der ersten Lebenswoche die Aktivitaten des Saugaktes und damit zusammenhangende Variable untersucht. Der Schluckakt wurde mit Hilfe eines Kontaktmikrophons am Hals aufgezeichnet. Urn die Lippen- und Zungenbewegungen sowie die Fliel3rate de Nahrung gleichzeitig, jedoch unabhlngig voneinander zu registrieren, wurde ein speziell adaptierter Standardnippel beniitzt. Atemfrequenz und Herzpuls wurden mit einem nasalen Thermistor bzw. mit einem Photozell-Plethysmographen aufgezeichnet. Zwei charackteristische Bilder der Saugaktivitlt wurden beobachtet. Das eine Bild umfagt Perioden relativ konstanter Saugaktivitlt mit kurzen eingestreuten Pausen. Das zweite Bild war durch kurze Perioden der Saugaktivitat mit langeren, dazwischenliegenden Pausen charakterisiert. Kinder, die diese letztere Art der Saugaktivitlt entwickelten, nahmen weniger Volumen pro Saugvorgang zu sich. Pro Einatmung kamen ein oder zwei Saugbewegungen vor. Geschluckt wurde am haufigsten am Ende der Einatmung oder zu Beginn der Ausatmung. Bei den meisten Kindem steig der Herzpuls wahrend des Saugens an. Die gesammelten Daten kiinnen leicht zum Katalogisieren analysiert werden und zur Frtihdiagnose pathologischer Zustlnde beitragen. Die Messung neuraler Beziehungen, die sich im Komplex des Saugaktes, der Atmung und des Schluckens wiederspiegeln, dtirfte gee&net sein, den neurologischen Status neugeborener Kinder festzulegen. Ebenso dtirften solche Messungen miiglicherweise eine Beziehung zwischen dem Status Neugeborener und darauffolgender Wachstums- und Entwicklungsstufen herbeifiihren lassen. REFERENCES ARDRAN, G. M., KEMP, F. H. and LIND, M. B. 1958. A cineradiographic study of bottle feeding. J. Rud. 31, 11-22. BRENMAN,H., PIERCE, L., MACKOWIAK,R. and FRIEDMAN,M. H. F. Multisensor nipple for recording oral parameters. J. appl. Physiol. in press. COLLEY,J. R. T. and CREAMER,B. 1958. Sucking and swallowing in infants. Br. Med. J. 2,422-423. GESELL,A. 1945. The Embryology ofBehavior. Chap. 10, p. 114. Harper Brothers, New York. KRON, R., STE~V,M. and GODDARD,K. 1963. A method of measuring sucking behavior of newborn infants. Psychosomatic Med. 25, 181-191. MACKOWIAK,R., BRENMAN,H. and FRIEDMAN,M. H. F. 1967. Acoustic profile of deglutition. Proc. Sot. exp. Biol. Med. 125, 1149-l 152. MACKOWIAK,R., BRENMAN,H. and FRIEDMAN,M. H. F. 1967. Inexpensive respiratory sensor constructed from miniature incandescent bulb. J. uppl. Physiol. 22, 1022-1023. PEIPER,A. 1963. Cerebral Function in Infancy and Childhood (Translation of third edition) Chap. 9, pp. 403-404, 42@446. Consultants Bureau, New York.
PLATE 1 OVERLEAF
A.O.B.
14/10-c
MOUTHlNG
ACTIVITIES
IN THE HUMAN
NEONATAL
SUCKING
ACT
FIG. 2. Nasal sensor placed in vicinity of nares, microphone held lightly on neck, nip[ de placed in mouth. Sensors are readily accepted by infant and are non-restrictive.
PL.ATE
1
A.O.B. f.p. 1168
Blol. Vol. 14, pp. 1159-I 167, 1969. Pergamoa Press. Printed ia Gt. Britain.
MOUTHING ACTIVITIES IN THE HUMAN NEONATAL SUCKING ACT M. L. SCNWTGEN, L. PIERCE and H. S. BRENMAN Departments of Pediatrics and Physiology Jefferson Medical College, Philadelphia, Pennsylvania 19107, U.S.A. Summary--Mouthing activities of the act of sucking and related variables were studied in ten normal newborn infants within the first week of life. Deglutition events were monitored by a contact microphone held in place on the neck. A specially adapted standard nipple was used to record lip and tongue movement and nutrient flow rate simultaneously but independently. Respiration and heart rate were recorded with a short-latency nasal thermistor and a digital photocell plethysmograph respectively. Two chara&ristic patterns of sucking activity were noted. One pattern consisted of periods of relatively constant sucking activity with short pauses between bursts. The second pattern showed short periods of sucking activity with longer pauses between bursts. Infants exhibiti the latter pattern obtained less volume per suck. Every one or two sucking movements occurred per respiration. Swallowing occurred most often at the end of inspiration or the beginning of expiration. Heart rate increased in most infants during sucking activity. Data collected can be readily analyxed for cataloguing and could aid in early diagnosis of pathological conditions. Measurement of neural interrelationships reilected by sucking and the respiratory and swallowing complex may be helpful in evaluating the neurological state of new-born infants and may possibly establish a relationship between neonatal patterns and subsequent growth and development. INTRODUCTION
THE ACT of infant feeding involves complex neural interrelationships of many physiologic mechanisms. An attenuation of the maturation process or an induced abnormality, such as brain damage, could adversely modify the normal, sequential interrelationships between respiration, sucking and deglutition with subsequent feeding problems and failure to thrive. The sucking act and related activities have been previously investigated in humans and animals. PEIPER(1963) has conducted extensive studies on newborn infants and has described the interrelationships between swallowing and respiration, swallowing and sucking, and sucking and respiration. His work has done much to establish patterns of neural interrelationships. In addition, ARDRAN,KEMP and LIND (1958) have conducted cineradiographic studies of the sucking act in human infants and animals in order to determine the role played by mouthing activities and pressures in the sucking act. They concluded that the expression of fluid into the oral cavity is accomplished by combined action of sub-atmospheric pressure and the action of compression of the nipple by the tongue and gums. COLLEY and CREAMER (1958), on 1159
1160
M. L. SOENTGEN, L. PIERCE AND H. S.
BRENMAN
the other hand, support the aspiration theory which attributes expression of fluid to the piston-like action of the tongue as it folds backwards. With recent advances in electronics facilitating the recording of many variables, the present study was initiated to develop and adapt external sensors which, by a multiparametric approach, could simultaneously but independently record sucking pressures and movements, respiration and the act of swallowing. Analytic techniques for analysis of data have been developed to assist in identifying emerging patterns of the feeding act. METHODS
AND
MATERIALS
Ten full-term infants, 2 to 4 days old, with average weights of 3000 g and no evidence of cardio-pulmonary, bucco-oesophageal, or central nervous system disease were selected at random for use in this study. The infant was transported to a testing room in close proximity to the newborn nurseries and remained in the transportation crib throughout the procedure. A paediatrician and two registered nurses were present during the testing. Deglutition events were monitored by means of a small, highly sensitive microphone (Sonotone RE-21030) placed on the neck lateral to the thyroid cartilage and held in place by light digital pressure. The microphone signals were processed by a Grass Polygraph (Model 7) and low-level DC preamplifier (Model 7Pl) and stored on a Roberts tape recorder (Model 990s). In order to establish acoustic patterns of swallowing sounds which could be used in clinical diagnosis, sound recordings were fed into an Ampex Multichannel FM Instrumentation Recorder and were: (1) expanded by playback at tape speeds one eighth the original recording speed and were displayed on a multichannel storage oscilloscope (Tektronix Model 564), and (2) submitted to Voiceprint Laboratories of Somerville, New Jersey, for sound spectrum analysis of the acoustic energy (MACKOWIAK,BRENMAN and FRIEDMAN,1967). These two methods demonstrate the reproducibility of sounds of swallowing. Respirations were recorded with the nasal sensor (MACKOWIAK,BRENMANand FRIEDMAN,1967) developed for this study. When placed in the vicinity of the nares, this sensor indicated the respiratory envelope by responding to temperature changes in inspired and expired air flow. Signals were processed by a low-level DC preamplifier (Grass 7Pl) and Polygraph (Grass Model 7), and standardized against the pneumograph and pneumotachograph. Five per cent glucose water was ingested through a multisensor nipple (BRENMAN et al., 1969) so constructed that oral activities and nutrient flow are recorded simultaneously but independently. The nipple was attached to a flow limiting device as illustrated in Fig. 1. With the apparatus arranged so that the side-arm burette and transducer are at the level of the infant’s mouth, fluid can only flow from the burette through the rubber tubing and resistance rod into the stainless steel tubing anchored in the nipple when intraoral pressure becomes subatmospheric. Flow exerts pressure against a column of fluid on either side of the resistance rod. These pressures are conveyed to either side of a diaphragm in the differential transducer (Sanborn Model 268B). P1 and P, are processed by a differential transducer converter (Sanborn Model
htownmci
ACTIVITIESINTHEHUMAN
NEONATAL
SUCKING
ACT
1161
Polygraph
Amplifier
Amplifier
FIG. 1. Multisensor nipple apparatus. When side-arm burette and transducer are placed on the level of the infant’s mouth, nutrient flow occurs only when intraoral pressure becomes subatmospheric.
592-300) where P, is subtracted from P,. AP is transmitted into a low-level DC preamplifier (Grass Model 7Pl) and is recorded on a polygraph (Grass Model 7) as a flow curve. Simultaneously, lip movement is recorded by means of the patent rubber tubing anchored within the intra-nipple compression chamber. When pressure is applied by lip and tongue movements, changes in intra-nipple pressure are conveyed to a differential pressure transducer (Statham Model P23AC) and into a low-level DC preamplifier (Grass Model 7Pl) and polygraph (Grass Model 7). The flow-limiting device of the multisensor nipple is a modification of a device described by KRON, STEIN and GODDARD (1963). We have substituted the Sanborn differential pressure transducer and converter for a Statham differential pressure transducer used by KRON et al. (1963). In this way, we were able to measure AP which was recorded as a fluid flow curve reflecting volume rate of flow. Flow volume can be obtained by calculating the area under the curve. The intra-nipple compression chamber is an innovation which enables simultaneous recording of oral activities as reflected by lip and tongue movements. Since the sucking complex involves both lip and tongue movements as well as intraoral pressure changes, this device makes it possible to investigate the temporal relationships between oral activities and nutrient flow. To complete the instrumentation, a digital photoelectric plethysmograph (Grass Model PTTl-7) was placed on the great toe and recorded heart rate. Signals from all the transducers were fed into a direct-writing polygraph (Grass Model 7). As indicated in Fig. 2, the infant is in no way restricted from normal activity and readily accepts the sensors. All sensors are easily sterilized by ethylene oxide gas sterilization.
1162
M. L. S~ENTGEN,L. PIERCEANDH. S. BRENMAN
FIG. 3. Polygraph recording of temporal interrelationships of the recorded variables in a 2-day old infant. Intra-nipple pressure recordings show an upward deflection when lips compress bulb of nipple and/or when pressure increases within oral cavity. Channel 2: Nutrient flow curve reflecting intraoral pressure. Plow occurs only when subatmospheric pressure is created. Channel 3: Respiration, with downward deflection of pen indicating inspiration. Channel 4: Sounds of swallowing. Arrow denotes one swallow and where it occurs in relation to other variables. Channel 5: Pulse rate as recorded by digital plethysmograph. Calibrations of intra-nipple pressure and nutrient flow are indicated on the right.
MOUTHING ACTIVITIES IN THE HUMAN NEONATAL SUCKING ACT
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RESULTS
Figure 3 demonstrates a portion of simultaneous ordinate recordings of intranipple pressure, nutrient flow, respiration, deglutition and pulse rate. Channel 1 represents oral activity as reflected by lip and tongue compression on the nipple and as recorded from the compression chamber within the nipple. Upward deflection indicated increased intra-nipple pressure and downward deflection indicated decreased intra-nipple pressure. When the nipple apparatus was positioned with the side-arm burette and the differential pressure transducer (Sanborn 268B) at the level of the infant’s mouth, fluid flowed only when the intraoral pressure became subatmospheric. Observation of channels 1 and 2 indicates that, as the intra-nipple pressure increased, the flow tapered off. As intra-nipple pressure decreased with cessation of lip compression, fluid flowed rapidly and was sustained for the duration of the decrease in intra-nipple pressure. The tracing on channel 1 also shows the intra-nipple pressure falling below baseline during the downward deflection when lip compression was absent. This is interpreted as representing the influence of the subatmospheric intraoral effects on that part of the compression chamber within the oral cavity. The individual effects of lip and tongue compression and intraoral pressure were demonstrated in several ways. When the flow tubing was clamped and lip and tongue activity was recorded without flow, the pen deflected upward as usual, but it returned only to baseline when compression was released. This would indicate that lip and tongue compression is responsible for the changes in intra-nipple pressures demonstrated by the deflection above baseline and the return to baseline. On the other hand, in several recordings, flow was recorded without noticeable lip activity suggesting creation of subatmospheric pressure without lip movements. In these cases, the lips were able to create the anterior seal without noticeable lip activity and flow occurred when intraoral pressure became subatmospheric. Changes in intraoral pressure were also reflected on the flow curve of channel 2 since nutrient flow could occur only with subatmospheric intraoral pressure. Channel 3 (Fig. 3) represents respiration as recorded by means of the nasal sensor which responds to temperature changes in inspiratory and expiratory air flow. Downward deflection represents inspiratory flow and upward deflection expiratory flow. Sounds of swallowing were recorded on channel 4 by means of the contact microphone held in place on the neck. The small deflections on the recording represent the swallowing sound whereas the larger deflections represent sucking noises. These noises decrease in frequency as the sucking burst becomes less active. Channel 5 represents heart rate as recorded by means of the digital plethysmograph placed on the infant’s great toe. Interrelationships between sucking movements, swallowing and respiration were determined by drawing a line through each swallow depicted on channel 4 and passing this line through all other tracings (Fig. 3). The number of sucking movements and respiratory cycles occurring between swallows was determined and ratios for sucking movements and respirations and for sucking movements and swallowing were established. Every one or two sucking movements were followed by a swallow occurring at the height of or at the end of flow. One or two sucking movements occurred per
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respiration. Sucking rate appeared to pace respiration. Swallowing occurred most frequently at the end of inspiration or the beginning of expiration. Heart rate was counted by the number of pulsations prior to sucking activity and during sucking activity. In all infants, heart rate increased IO-30 beats per min during sucking. These findings are in general agreement with those reported by PEIPER(1963). Graphic representation of the temporal interrelationships are shown in Fig. 4. The first bar graph represents intra-nipple pressure. The break in the bar indicates the end of one sucking movement and the beginning of the next. Upward oblique lines
I
Intronipple
pressure
2 Nutrient
flow
3 Respiration
4
q
Deglutition
Pulse
5 rate
I
’
I
q I
I
I
FIG.4. Bar graph representation of temporal relationships between intranipple pressure, nutrient flow, respiration, deglutition and pulse rate. The blank spaces on the bar graphs represent the end of one movement and the beginning of the next. Upward oblique lines on bars 1 and 2 represent increasing intranipple pressure due to increased lip compression and flow respectively. Downward oblique lines represent decreasing pressure and flow. Downward oblique lines on bar 3 represent inspiration shown as a downward pen deflection on Fig. 3. Upward oblique lines denote expiration. Each vertical line on bar 5 represent a pulse beat. The first swallow occurred as intranipple pressure began to increase at the end of flow and during respiration. There was one sucking movement per swallow and one swallow per respiration. The heart rate was 188 beats per min. indicate increasing intra-nipple pressure created by lip and tongue activity and downward oblique lines indicate decreasing pressure as the lip and tongue compression is released. The second bar graph represents nutrient flow. The breaks in the bar indicate the end of one flow curve and the beginning of the next. Upward oblique lines indicate increasing flow and downward oblique lines indicate decreasing flow. The third bar graph represents respiration. The break in the bar indicates the end of one respiratory cycle and the beginning of the next. Downward oblique lines indicate inspiration and upward oblique lines represent expiration. The two small squares on the fourth bar area represent swallows. The single line markings on the fifth bar represent pulse rate. The 1.6 set time period is associated with the portion of the recording on Fig. 3 indicated by the arrow. In this sequence, the first swallow (as indicated by the arrow) occurred with the initial increase of intraoral pressure at the end
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of nutrient flow and during the expiratory phase of respiration. There is one sucking movement per swallow and one swallow during each respiratory cycle. The heart rate is approximately 188 beats per min representing an increase of approximately 30 beats per min caused by the sucking complex. In the ten series of recordings made, two patterns of sucking activity repeated themselves. One pattern, a portion of which is illustrated in Fig. 3, consisted of periods of relatively constant sucking activity of 15 set or longer and with short pauses of 5-10 set between bursts. A burst of sucking activity is defined as a series of continuous sucking movements without a pause. When a pause in the activity occurred, the burst was considered as ended. The average number of sucking movements per set in this pattern was greater than one but less than two. The second pattern of activity consisted of periods of shorter bursts of sucking activity lasting approximately 10-l 5 set with longer pauses (greater than 10 set). DISCUSSION
According to descriptions by ARDRAN,KEMPand LIND (1958) and PEIPER(1963), lip movements are initiated, at least in part, by the presence of the nipple on the lips. These movements position the nipple in the oral cavity and cease with the creation of an air seal. At the same time the rear of the oral cavity is sealed by apposition of the posterior tongue and soft palate. The lower jaw is raised and moved forward, the neck of the nipple is compressed between the maxillary ridge and tip of tongue covering the mandibular ridge. The movement of the tip of the tongue upward and backward expresses some of the nutrient into the mouth. The lower jaw drops, creating an increased intraoral volume which brings about a decrease in intraoral pressure. At this time the nipple is drawn into the oral cavity and flow occurs. Our data also demonstrated lip compression occurring prior to flow. This would correspond to the manipulation of the nipple and the raised lower jaw which moves forward. The role of expression of the nutrient by the tip of the tongue moving backward cannot occur with the multi-nipple apparatus as described, since flow can occur only with subatmospheric intraoral pressure. When the lip compression ceased, the intraoral pressure fell below atmospheric pressure and flow occurred. This action was indicated on both channels 1 and 2. The decreased intraoral pressure is indicated by a downward deflection on channel 1 and by increased flow on channel 2 (Fig. 3). This description of the sucking act and our findings emphasize the relationship of lip actions and intraoral pressure in expressing nutrient fluids. We feel that the multisensor nipple provided a means of establishing temporal relationships between these two variables in such a manner than they can be recorded during routine feeding. Deviations from normal patterns could be detected early. In this study, swallows occurred at the height of flow or end of flow. The posterior seal is maintained until sufficient fluid is present in the mouth. The tip of the tongue moves upward and backward and the posterior seal is lost. The fluid is propelled into the mesopharynx and the involuntary stages of swallowing occur. During the time of the swallowing events, other related activities cease. This is demonstrated in Fig. 3. During the swallowing event, a plateau occurred in the intra-nipple pressure as seen on
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channel 1. A small deflection of the pen indicated this event on the flow curve of channel 2. Respiratory air flow ceased for a short interval as indicated by the pause in the expiratory flow which we designate as the swallowing inhibitory pause produced by the modification of respiration by the swallow. This would indicate that respirations can be dominated by the swallowing centre. These relationships have been noted by other investigators including PEIPER (1963). The temporal sequence between sucking movements and swallows and sucking movements and respiration suggest that sucking movements pace swallowing events and respirations. Every one or two sucking movements were followed by a swallow. PEIPER(1963) proposes that the sucking centre begins to function when a nipple-like object is placed in the infant’s mouth but that the swallowing centre is excited to produce a regular rhythm only when food is obtained. He also proposes that buccooesophageal swallowing depends for its rhythm upon sucking movements and may really represent a continuation of them. Our findings would confirm this supposition although it will be noted that in some cases more than one sucking movement occurred per swallow. This may indicate the necessity for a volume threshold to trigger a swallow. The respiratory rate also seems to depend upon the sucking movements for its rhythm. When sucking movements began, the respiratory rate increased and became irregular. As indicated in Fig. 3, when the sucking activity became less intense, swallowing became less frequent and the respiratory rate became more regular and slower. The fact that there is a locus of inhibition in respiration created by the swallowing events also lends support to PEIPER’S(1963) conclusion that the sucking centre dominates the respiratory centre. We can, therefore, conclude that the external sensors developed for this study provide the means for studying temporal neural interrelationships between sucking, deglutition and respiration. The sensors are non-restrictive, easily sterilized and accepted by the infants. They can be employed with standard recording instruments and contribute data that can be easily analyzed. Time expansion and sound spectrum analysis provide a means of establishing the reproducibility of swallows and characteristic sound patterns for normal and abnormal swallows. We feel that the establishment of a library of normal sound patterns could be an aid in early diagnosis of pathological conditions reflected in the feeding act. GE~ELL(1945) has used sucking as one criterion for evaluating neurological development in infants. We believe that measurement of neural interrelationships as reflected by the sucking, respiratory and swallowing complex could be helpful in evaluating not only the neurological state of the newborn infant, but also possibly in establishing a relationship between neonatal patterns and subsequent growth and development. Rkme--Les activites buccales au cows de la suction et ainsi, que les activitb annexes sont Btudikes chez dix enfants nouveau-n& normaux pendant la premiere semaine de vie. La deglutition est enregistree par I’intermddiaire d’un microphone de contact place au niveau de la nuque. Un biberon standard, spkcialement adapte, est utihse pour enregistrer simultanement, mais independemment, les mouvements de la fangue et des levres, ainsi que la vitesse d’kcoulement du liquide nuttitif. Les frequences respiratoire et cardiaque sont enregistrees respectivement ?I l’aide d’un thermistor nasal et d’un pletysmographe a cellule phototlectrique.
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Deux modes de suction caractCristiques ont CtCnotes. L’un des types comporte des p&odes de suction relativement constante avec des repos courts entre les suctions. Le second type comprend des periodes de suction courtes, &par&s par des intervalles longs. Les enfants, utilisant ce demier mode, obtiemrent moins de volume liquidien par suction. Un ou deux mouvements de suction se produisent au tours d’un cycle respiratoire. La deglutition suit generalement la fin de l’inspiration ou le debut de l’expiration. La frequence cardiaque augmente chez la plupart des enfants pendant la suction. Les resultats obtenus pourraient servir dans le diagnostic de conditions pathologiques. La mesure des rapports nerveux entrant dans le complexe de suction, respiration et deglutition, peut etre utile pour tester l’dtat neurologique des nouveau-t&. Zusannnenfassung-Bei 10 gesunden neugeborenen Kindem wurden innerhalb der ersten Lebenswoche die Aktivitaten des Saugaktes und damit zusammenhangende Variable untersucht. Der Schluckakt wurde mit Hilfe eines Kontaktmikrophons am Hals aufgezeichnet. Urn die Lippen- und Zungenbewegungen sowie die Fliel3rate de Nahrung gleichzeitig, jedoch unabhlngig voneinander zu registrieren, wurde ein speziell adaptierter Standardnippel beniitzt. Atemfrequenz und Herzpuls wurden mit einem nasalen Thermistor bzw. mit einem Photozell-Plethysmographen aufgezeichnet. Zwei charackteristische Bilder der Saugaktivitlt wurden beobachtet. Das eine Bild umfagt Perioden relativ konstanter Saugaktivitlt mit kurzen eingestreuten Pausen. Das zweite Bild war durch kurze Perioden der Saugaktivitat mit langeren, dazwischenliegenden Pausen charakterisiert. Kinder, die diese letztere Art der Saugaktivitlt entwickelten, nahmen weniger Volumen pro Saugvorgang zu sich. Pro Einatmung kamen ein oder zwei Saugbewegungen vor. Geschluckt wurde am haufigsten am Ende der Einatmung oder zu Beginn der Ausatmung. Bei den meisten Kindem steig der Herzpuls wahrend des Saugens an. Die gesammelten Daten kiinnen leicht zum Katalogisieren analysiert werden und zur Frtihdiagnose pathologischer Zustlnde beitragen. Die Messung neuraler Beziehungen, die sich im Komplex des Saugaktes, der Atmung und des Schluckens wiederspiegeln, dtirfte gee&net sein, den neurologischen Status neugeborener Kinder festzulegen. Ebenso dtirften solche Messungen miiglicherweise eine Beziehung zwischen dem Status Neugeborener und darauffolgender Wachstums- und Entwicklungsstufen herbeifiihren lassen. REFERENCES ARDRAN, G. M., KEMP, F. H. and LIND, M. B. 1958. A cineradiographic study of bottle feeding. J. Rud. 31, 11-22. BRENMAN,H., PIERCE, L., MACKOWIAK,R. and FRIEDMAN,M. H. F. Multisensor nipple for recording oral parameters. J. appl. Physiol. in press. COLLEY,J. R. T. and CREAMER,B. 1958. Sucking and swallowing in infants. Br. Med. J. 2,422-423. GESELL,A. 1945. The Embryology ofBehavior. Chap. 10, p. 114. Harper Brothers, New York. KRON, R., STE~V,M. and GODDARD,K. 1963. A method of measuring sucking behavior of newborn infants. Psychosomatic Med. 25, 181-191. MACKOWIAK,R., BRENMAN,H. and FRIEDMAN,M. H. F. 1967. Acoustic profile of deglutition. Proc. Sot. exp. Biol. Med. 125, 1149-l 152. MACKOWIAK,R., BRENMAN,H. and FRIEDMAN,M. H. F. 1967. Inexpensive respiratory sensor constructed from miniature incandescent bulb. J. uppl. Physiol. 22, 1022-1023. PEIPER,A. 1963. Cerebral Function in Infancy and Childhood (Translation of third edition) Chap. 9, pp. 403-404, 42@446. Consultants Bureau, New York.
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FIG. 2. Nasal sensor placed in vicinity of nares, microphone held lightly on neck, nip[ de placed in mouth. Sensors are readily accepted by infant and are non-restrictive.
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