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Acta Pñdiatr 89: 846±52. 2000

Characterization of the developmental stages of sucking in preterm infants during bottle feeding C Lau1,2,3,4, R Alagugurusamy1,3, RJ Schanler1,3,5, EO Smith1 and RJ Shulman1,2,5 Baylor College of Medicine1; Department of Pediatrics, Divisions of Gastroenterology & Nutrition2/Neonatology3; Feeding Disorders Center4, Children’s Nutrition Research Center5, Houston, TX, USA

Lau C, Alagugurusamy R, Schanler RJ, Smith EO, Shulman RJ. Characterization of the developmental stages of sucking in preterm infants during bottle feeding. Acta Pædiatr 2000; 89: 846–52. Stockholm. ISSN 0803–5253 It is acknowledged that the difficulty many preterm infants have in feeding orally results from their immature sucking skills. However, little is known regarding the development of sucking in these infants. The aim of this study was to demonstrate that the bottle-feeding performance of preterm infants is positively correlated with the developmental stage of their sucking. Infants’ oral-motor skills were followed longitudinally using a special nipple/bottle system which monitored the suction and expression/compression component of sucking. The maturational process was rated into five primary stages based on the presence/absence of suction and the rhythmicity of the two components of sucking, suction and expression/compression. This five-point scale was used to characterize the developmental stage of sucking of each infant. Outcomes of feeding performance consisted of overall transfer (percent total volume transfered/volume to be taken) and rate of transfer (ml/min). Assessments were conducted when infants were taking 1–2, 3–5 and 6–8 oral feedings per day. Significant positive correlations were observed between the five stages of sucking and postmenstrual age, the defined feeding outcomes, and the number of daily oral feedings. Overall transfer and rate of transfer were enhanced when infants reached the more mature stages of sucking. We have demonstrated that oral feeding performance improves as infants’ sucking skills mature. In addition, we propose that the present five-point sucking scale may be used to assess the developmental stages of sucking of preterm infants. Such knowledge would facilitate the management of oral feeding in these infants. Key words: Feeding performance, low birthweight infants, oral feeding, oral-motor, prematurity Chantal Lau, Department of Pediatrics/Neonatology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA, MC 5-1000 (Tel. 1 713 798 6710, fax. 1 713 798 7187, e-mail. [email protected])

Preterm infants have difficulty transitioning from tubefeeding to full oral feeding. This has been blamed on the immaturity of their sucking pattern and often results in a delayed discharge from the hospital as the latter milestone is significantly correlated with hospital discharge (1). The sucking pattern of term infants is characterized by the rhythmic alternation of suction and expression/ compression (2, 3). Suction defines the negative intraoral pressure generated as the infant draws milk into the mouth and expression/compression is believed to correspond to mouthing or the compression and/or stripping of the nipple between the tongue and the hard palate as milk is ejected into the mouth (4–6). It is unclear when the term sucking pattern appears. In a recent study, we demonstrated that preterm infants, with an immature sucking pattern consisting primarily of expression/compression, can successfully bottle feed, although they were not as efficient as infants who achieved a term sucking pattern (7). Thus, the aim of the  2000 Taylor & Francis. ISSN 0803-5253

present study was to verify the hypothesis that oral feeding performance of preterm infants is positively correlated with the maturation of sucking skills. For this purpose, we followed the development of the sucking pattern of infants, born less than 30 wk gestation, from the time they were introduced to oral feeding until they reached full oral feeding and categorized the maturational process into five primary stages of sucking. This five-point scale was used to demonstrate the relationship between the development of sucking and oral feeding performance in preterm infants.

Methods Subjects Seventy-two infants (38M, 34F), born between 26 and 29 wk gestation (27.5 1.1 wk, mean SD), with birthweight averaging 1028 173 g, and appropriate

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for gestational age as determined by maternal dates and antenatal ultrasonography, were recruited from the nurseries at Texas Children’s Hospital. These subjects were “healthy” preterm infants whose discharge from the hospital was primarily dependent upon their ability to reach full oral feeding. Infants with any of the following conditions were excluded from the study: intraventricular hemorrhage grades III and IV (8), necrotizing enterocolitis, hydrocephalus, major congenital abnormalities, and persistent oxygen requirement for more than a month. Infants were treated prophylactically with caffeine citrate until they demonstrated mature control of breathing, usually around 35 wk postmenstrual age. The infants were introduced to oral feeding at 34.2 1.7 wk postmenstrual age, when their respiratory rate was 1.5 sec delineated the beginning and end of a sucking burst. The first 5 min of an oral motor recording was used because we assumed that fatigue would be minimal at the start of a session. To reduce the potential of fatigue, the infants were not handled for at least 30 min prior to each monitored session. Because the fatigue factor was reduced, it is presumed that the sucking pattern observed during that time would reflect the true sucking skills of the subject rather than his/her overall feeding ability. Indeed, it is expected that the level of endurance of an infant would affect more likely his/her overall performance than the initial 5 min of a feeding. Oral feeding outcomes Feeding performance was assessed with the following outcome measures: overall transfer, the percent volume taken during a feeding divided by the volume to be taken, and rate of transfer (ml/min), the rate at which the entire feeding was taken. Volume taken was determined by comparing the amount of milk remaining in the graduated reservoir at the end of a feeding. Milk lost from drooling was measured by weighing a bib before and after each feeding,with 1 ml approximating 1 g. For full-term infants, only rate of transfer was calculated, as they were fed ad libitum, and overall transfer was always 100%. Data analyses In order to assess the reliability of using the scores of only one observer in the identification of the five stages of the proposed sucking scale, two observers, blind to the age and number of oral feedings per day of the infants, independently scored 50 of 208 (24%) oralfeeding tracings selected at random across the five stages of sucking. The percentage agreement between observers was calculated. Inasmuch as the infants born at 26 wk gestation are less mature than those born at 29 wk, a regression analysis of the defined outcome measures versus gestational age was conducted in order to determine

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Fig. 1. Actual sample tracings and corresponding range of amplitudes (mmHg) measured at each stage of sucking.

whether maturity plays a significant role in the performance of the infants. Gender was analyzed by analysis of variance (ANOVA). Correlations between the stages of sucking and postmenstrual age, overall transfer, rate of transfer, and the number of oral feedings per day were assessed using regression analyses which accounted for repeated measures on individuals. ANOVA for repeated measures was used to assess the difference between stages of sucking with respect to the above measures. Post-hoc Fisher’s LSD modified t-test

was used, when approppriate. An independent t-test was used to compare the rates of transfer and postmenstrual ages between preterm and full-term subjects.

Results Stages of sucking Fig. 1 shows a composite of actual sample tracings, corresponding range of amplitudes (mmHg) and a


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Fig. 2. Postmenstrual age versus stages of sucking (boxplot). * = mean; horizontal bar (dashed) = median; dotted vertical bars = max, min; dot box (white) = quartiles 1 and 3; solid box (slant) = 95% confidence interval. p value: Repeated measures ANOVA of the differences between stages. **Post-hoc Fisher’s LSD versus stage 1: p < 0.001.

description of the suction and expression/compression components which typify the five stages of sucking. As the stages advance, the amplitude of the expression/ compression component does not change, ranging between 0.2 and 1 mmHg, whereas those of suction gradually increase along with the duration of the sucking bursts. Stage 1 consisted of sucking patterns where arrhythmic expression/compression was present with very infrequent suction of low amplitude. Stage 2 included rhythmic expression/compression with the appearance of arrhythmic suction of larger amplitude than those observed during stage 1. Stage 3 comprised rhythmic expression/compression alone, as well as the emergence of not yet rhythmic alternation of suction and expression. In stages 4 and 5 the infants used only the rhythmic alternation of suction and expression/ compression. Amplitude and the duration of sucking burst primarily differentiated the latter two stages.

Observers’ reliability On a five-point scale and based on 50 bottle-feeding assessments, there was a 58% (29/50) exact agreement between the two observers, 40% (20/50) when scoring differed by 1 unit, and 2% (1/50) when scoring differed by 2 units. With 98% of the differences between observers (49/50) falling within 1 unit, we were confident that the use of only one observer was adequate. Thus, subsequent data analyses were based on the scoring made by only one observer who was blind to the infants’ postmenstrual age and oral-feeding status. In addition, tracings from all the infants were mixed, such that all the tracings from any particular subject were never scored sequentially.

Fig. 3. A. Overall transfer versus stages of sucking. B. Rate of transfer versus stages of sucking (boxplot). * = mean; horizontal bar (dashed) = median; dotted vertical bars = max, min; dot box (white) = quartiles 1 and 3; solid box (slant) = 95% confidence interval. p value: Repeated measures ANOVA of the differences between stages. *Post-hoc Fisher’s LSD versus stage 1: p < 0.01; **posthoc Fisher’s LSD versus stage 1: p < 0.001.

Gestational age and gender versus stage of sucking, overall transfer, rate of transfer, number of oral feedings per day There was no significant correlation between any of the above outcome measures and the gestational age or gender of the infants. As such, gestational age and gender were pooled for the subsequent analyses. Stage of sucking versus postmenstrual age As shown in Fig. 2, there is a significant positive correlation between postmenstrual age and stage of sucking (p < 0.001). Post-hoc analyses showed that stages 3 through 5 occurred at significantly older postmenstrual ages than stage 1 (p < 0.001). Stage of sucking versus feeding performance outcomes Overall transfer (Fig. 3A) and rate of transfer (Fig. 3B) were positively correlated with stage of sucking

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Table 1. Postmenstrual age and oral feeding rate of transfer (mean SD) of preterm infants at stage 5 and term infants at 1st, 2nd and 3rd postnatal weeks. Infants Premature Term (1st week) Term (2nd week) Term (3rd week)

n

Postmenstrual age (wk)

Rate of transfer (ml/min)

8 9 10 7

36.9 2.5 40.4 1.3** 41.8 1.2*** 43.4 0.7***

4.27 2.48 6.59 2.34 8.26 3.17** 9.03 5.24*

Independent t-test versus preterm infants: *p 0.05; **p 0.01, ***p 0.001.

(p < 0.001). Post-hoc analyses showed that overall transfer at stages 3 to 4 and rate of transfer at stages 3 to 5 were significantly enhanced over those at stage 1 (p < 0.01 and p < 0.001), respectively. Table 1. shows that preterm infants can reach a stage 5 prior to full-term corrected age (p < 0.01). However, their rate of transfer was significantly lower than that of their full-term counterparts at 2 and 3 wk postnatal age (p < 0.01 and p < 0.05, respectively). Stage of sucking versus number of oral feedings per day There was a significant correlation between the stage of sucking and the number of oral feedings per day (p < 0.001, Fig. 4), with significant differences observed between stages 3–5 and 1 (p < 0.001). Oral-feeding assessments were tolerated well by all the infants. Any episodes of desaturation, apnea or bradycardia were self-corrected, did not require addi-

Fig. 4. Number of oral feedings per day versus stages of sucking (boxplot). * = mean; horizontal bar (dashed) = median; dotted vertical bars = max, min; dot box (white) = quartiles 1 and 3; solid box (slant) = 95% confidence interval. p value: Repeated measures ANOVA of the differences between stages. **Post-hoc Fisher’s LSD versus stage 1: p < 0.001.

tional support, and did not affect the oral motor assessment.

Discussion At present, clinicians and therapists alike have not been able to establish criteria for assessing the ability of infants to feed orally. The postmenstrual age of 33 to 34 postmenstrual weeks has been used as the most appropriate time to initiate oral feeding, but there is no evidence that this is the earliest time at which it can be done. It is evident that factors, such as endurance, proper coordination of suck-swallow-breathe, are important determining factors of infants’ success at oral feeding. However, knowledge of the developmental stage of sucking of an infant may assist clinicians in the initiation and progression of oral feeding. For this purpose, we characterized five primary stages of sucking in order to assess the relationship existing between the development of sucking and oral-feeding performance in preterm infants (26 to 29 wk gestation). To our knowledge, this is the first developmental sucking scale which has been developed for preterm infants. The development of sucking, indeed, is progressive and quantification of its maturation is difficult. However, inasmuch as the term sucking pattern is composed of the rhythmic alternation of suction and expression/compression, we selected the two components of sucking and rhythmicity as primary criteria to assess the stages of sucking. Suction amplitude was used to differentiate the more mature stages 4 and 5. Thus, early on, advancement of the stages of sucking consisted of the appearance and rhythmic establishment of the expression/compression component. This was followed by the appearance of suction and the progressive establishment of the rhythmic alternation of suction and expression/compression. As suction matured, its amplitude gradually increased. This was accompanied also with an increase in the duration of sucking bursts. The lack of correlation existing between gestational age and the stage of sucking, oral feeding outcomes and advancement of oral feedings would suggest that there is no significant in utero maturation of sucking occurring between 26 and 29 wk gestation or insufficient power to detect a difference over this developmental period. The positive correlation between the stages of sucking and postmenstrual age supports the notion that sucking ability improves as the infant matures. The correlations between stages of sucking and overall transfer and rate of transfer suggest that the maturation of this skill played a significant role in improving oral-feeding performance. Although the data demonstrated that the level of oralmotor skills advanced with age, there was a wide variation in these skills between subjects at any given postmenstrual age. This was not due to the subjects’ maturity at birth as mentioned above. It is unclear why


oral-motor skills developed more rapidly in some infants than others, when the population examined consisted of preterm infants without clinical conditions believed to hinder oral-feeding performance. It is well acknowledged that fatigue and/or coordination of suckswallow-breathe are two elements which can affect the overall feeding performance of the infant (9–12). The specific impact of these two factors will require additional studies. Other variations, such as behavioral characteristics of each subject (13), may also come into play. However, despite this wide variation, it is important to note that the defined stages of sucking correlated directly with the measures of feeding performance defined in this study. Post-hoc analyses which demonstrated a significant difference between stages 3–5 and 1 and the observation that, from stage 3 to 5, the suction component became more prominent, i.e., alternating rhythmically with the expression/compression component and increasing in amplitude, lends support to earlier reports suggesting that a sucking pattern with the rhythmic alternation of suction and expression/compression is more efficient than one without rhythmicity and/or with only the expression/ compression component (7, 9, 14). It is important, however, to note that, albeit less efficacious, the use of the expression/compression component alone, as seen in stages 1 and 2, still allows for successful and safe oral feedings in preterm infants (7). Unlike the increases in suction amplitude which occurred as the infants advanced in their oral feeding skills, the pressure recorded from the expression/ compression component reached a plateau rapidly. This likely resulted from the limitation of the monitoring system used, because the threshold corresponding to full compression of the catheter was reached very early. We are in the process of modifying our nipple/bottle system in order to circumvent this limitation, so as to monitor the actual expression/compression pressure generated by the infant. Of interest is that this technical limitation parallels the situation observed in the preterm infants. The use of expression/compression alone is of limited efficacy. Indeed, the maximal volume of milk that can be obtained when only the expression/compression component is used, is limited to the volume of milk contained between the initial point of compression of the nipple and the nipple hole. As such, although milk can be obtained when only expression/compression is utilized, it cannot be as efficient as when the suction component is present. With the latter, a continuous flow of milk can be generated as long as a negative intraoral pressure is applied. In addition, the greater the suction amplitude and duration, the greater the flow and volume out of the nipple, respectively. It should be remembered, however, that the size of the nipple hole will determine the maximum flow rate that can be obtained (5, 15). Preterm infants, who reached stage 5, were at a significantly younger postmenstrual age than the full-

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term neonates studied. Despite having developed similar oral-motor skills by virtue of achieving stage 5 sucking, they demonstrated lower rates of transfer than their full-term counterparts. It is probable that additional factors related to maturation come into play, as suggested by Pollitt et al. (16). Indeed, noting that 30-dold full-term infants ingested the same milk volume faster than 2-d-old counterparts, those authors concluded that the enhanced rate of transfer in the older infants was likely multifactorial. For example, intake can be increased by altering variables such as amplitude, frequency of suction- expression/compression, duration of sucking burst and/or endurance. In addition to facilitating the monitoring of the developmental progress of oral feeding in infants, the present scale would also help identify oral motor dysfunction(s) in infants who demonstrate feeding difficulties. This study supports the notion that sucking ability does not need to be at a mature level, i.e., stages 3 or higher, before preterm infants are introduced to oral feeding. Perhaps, just as importantly, the initiation of oral feeding at the earlier stages (e.g., stages 1 to 2), potentially provides increased opportunity for training to the infant. Safe oral feeding, in these circumstances, may be facilitated by using interventions such as the self-paced system which allows the infant to control milk flow more effectively (7, 17). As training often improves one’s ability at performing a specific task, we speculate that increased practice may enhance the oralfeeding skills of infants, leading to an accelerated progression of their oral feeding. As the benefits of breastfeeding and mother’s milk are widely recognized (18), the technique used in the present study is being adapted to study breastfeeding infants. In summary, using a five-point scale which describes the development of sucking in preterm infants during bottle feeding, we have demonstrated a significant correlation between the level of maturity of infant’s sucking and postmenstrual age, feeding performance (i.e., overall transfer and rate of transfer), and progression of oral feeding. In addition, we are advancing that the use of developmental scales, such as the present one, may be useful clinically for the identification/characterization of the oral-motor skills of preterm infants at any given time point as they progress in their oral feeding schedule. Acknowledgements.—The authors express their gratitude to P. Burns, C. Bryant, E. Newton-Novato, L. Schwartz for their assistance in this study. This work was supported by grants from the National Institutes of Child Health and Human Development (R01-HD28140), the General Clinical Research Center, Baylor College of Medicine/Texas Children’s Hospital Clinical Research Center (M01-RR-00188), National Institute of Health. Partial funding also was provided from the USDA/ARS, Children’s Nutrition Research Center, and the Department of Pediatrics, Baylor College of Medicine, Texas Children’s Hospital, Houston, TX. The contents of this publication do not necessarily reflect the views or policies of the USDA, nor does mention of trade names, commercial products, or organizations imply endorsement by the US government.

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Received Sept. 3, 1999; revision received Jan. 20, 2000; accepted Jan. 25, 2000