Early Introduction of Oral Feeding in Preterm Infants
Chanda Simpson, MD*; Richard J. Schanler, MD‡§; and Chantal Lau, PhD‡
ABSTRACT. Objective. To determine whether transi-tion from tube to all oral feeding can be accelerated by the early introduction of oral feeding in preterm infants. It is hypothesized that this shortened transition time will lead to earlier attainment of all oral feeding.
Design. Twenty-nine infants (<30 weeks’ gestation) were randomized to an intervention or control group. The intervention group (n ⴝ 13) was initiated to oral feeding 48 hours after achieving full tube feeding (120 kcal/kg/d), and the feeding progression followed a struc-tured protocol. The oral feeding management of the con-trol infants (nⴝ 16) was left to the discretion of their attending physicians. Oral feeding progress was moni-tored for achievement of selected feeding milestones: achievement of first and all successful oral feedings. Feeding performance was assessed by overall transfer (percent volume transferred during a feeding/total vol-ume offered) and rate of milk transfer (mL/min), which were measured from introduction of oral feeding to first successful oral feeding.
Results. Infants in the experimental group, when compared with their control counterparts, were intro-duced to oral feeding significantly earlier (31.1ⴞ1.3 vs 33.7 ⴞ 0.9 weeks’ postmenstrual age, respectively) and attained all oral feeding significantly earlier as well (34.5 ⴞ 1.6 vs 36.0 ⴞ 1.5 weeks’ postmenstrual age, re-spectively). The transition time from full tube feeding to all oral feeding was 26.8ⴞ12.3 days for the experimental group and 38.4 ⴞ 14.0 days for the control group. Both groups of infants demonstrated similar increase in over-all transfer and rate of milk transfer from introduction of oral feeding until achievement of first successful oral feeding.
Conclusions. Early introduction of oral feeding accel-erates the transition time from tube to all oral feeding. This not only allows earlier attainment of all oral feed-ing, but it also provides practice opportunities that en-hance the oral motor skills necessary for safe and suc-cessful feeding. Pediatrics 2002;110:517–522; nipple feeding, bottle feeding, prematurity, very low birth weight infants.
ABBREVIATION. PMA, postmenstrual age.
I
mproved survival of preterm infants born ⬍30 weeks’ gestation has brought on a new set of challenges for the clinician, especially one of pro-viding adequate nutrition and maintaining growth. This includes the challenge of assessing the infant’s ability and readiness to feed orally. When is the preterm infant able to take oral feedings and what clinical markers should be used to determine readi-ness to do so? A number of studies have addressed the development of sucking in preterm infants,1–7 but there are no data to guide clinicians on selecting the optimal time to introduce oral feeding.The sucking behavior of term infants consists of a rhythmic alternation of suction and expression.5 Suc-tion is the negative intraoral pressure exerted by the infant while drawing milk into the mouth. Expres-sion is the positive pressure believed to correspond to the stripping of the nipple between the hard palate and the tongue to eject milk into the mouth. In a study with infants born between 26 and 29 weeks’ gestation,6 it was shown that the ability to transfer milk did not require the presence of a term sucking pattern. In fact, the majority of these preterm infants demonstrated a predominant sucking pattern of ex-pression with no suction when first introduced to oral feeding. Despite the use of such an “immature” sucking pattern, these infants were able to complete their oral feeding within the allotted time of 20 min-utes without complications. With age, infants shifted to a more frequent use of the term sucking pattern.6 It is known that motor activities for suck, swallow, and breathe are functioning long before gestation is complete. For example, mouth opening has been ob-served at 7 to 8 weeks, tongue protrusion at 13 weeks, sucking at 15 weeks, swallowing of amniotic fluid at 12 to 14 weeks,8,9 and fetal breathing at 10 weeks’ gestation.10,11 Although these functions are present prenatally, we do not know the earliest time at which postnatal sucking-swallowing and breath-ing can be coordinated.
The American Academy of Pediatrics recommends that preterm infants demonstrate competent oral feeding skills before hospital discharge,12 and the latter has been correlated with the attainment of all oral feeding.13Often a delay in discharge is observed secondary to the inability of preterm infants to feed by mouth successfully and safely. Success implies the ability to take all of the prescribed volume by mouth within an allotted time and maintain a sus-tained pattern of weight gain. Safety implies proper From the *Pediatrix Medical Group of Texas, PA, Fort Worth, Texas;
‡De-partment of Pediatrics/Neonatology, Baylor College of Medicine, Houston, Texas; and §Children’s Nutrition Research Center, Houston, Texas. This work is a publication of the US Department of Agriculture/Agricul-tural Research Service Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas. The contents of this publication do not necessarily reflect the views or policies of the US Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the US government.
Received for publication May 23, 2001; accepted Jan 17, 2002.
Reprint requests to (C.L.) Department of Pediatrics/Neonatology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030. E-mail: clau@ bcm.tmc.edu
coordination of suck-swallow-breathe. Previous studies have suggested that this coordination does not occur until 33 to 34 weeks’ postmenstrual age (PMA),1–3at which time preterm infants are believed to have a sucking pattern that begins to resemble that of term infants.1 As such, the introduction of oral feeding to preterm infants is not routinely done until this time.
Because infants with immature sucking can be suc-cessful at bottle feeding,6we hypothesized that pre-term infants are capable of successfully and safely initiating oral feeding before 33 weeks’ PMA and attaining all oral feeding earlier than 37 weeks’ PMA as is commonly observed today.13
METHODS
We conducted a prospective, randomized, controlled study of preterm infants from the neonatal nurseries of Texas Children’s Hospital who were born⬍30 weeks’ gestation and were appro-priate for gestational age, as determined by obstetrical dating and clinical examination. The patients were recruited from October 1998 to December 1999. As we were interested in the most healthy, “well,” preterm infant population for this initial study, we ex-cluded infants with major congenital malformations, severe
neu-rologic problems (eg, Grade III/IV intraventricular hemor-rhage14), contraindications to enteral feeding, (eg, necrotizing
enterocolitis, no enteral feedingⱖ1 week), oxygen requirement of ⬎30%, and/or mechanical ventilation forⱖ1 week after reaching full enteral feeding. Infants were recruited before their attaining full tube feeding (120 kcal/kg/d) and randomized to either an experimental or control group. Gestational age stratification (ⱕ25, 26 –27, and 28 –29 weeks’ gestation) was balanced for both groups. Attending physicians were not blinded to the group assignment. Informed written consent was obtained from parents after consul-tation with the attending physician. This study was approved by the Baylor College of Medicine Institutional Review Boards for Human Research.
In our nurseries, enteral tube feeding is begun usually by the end of the first week of life. Once initiated, the feeding volume is advanced by small increments daily depending on feeding toler-ance,13until full tube feeding (120 kcal/kg/d) is achieved. Infants
are fed every 3 hours and receive breast milk whenever available. Formula is only provided if mothers do not pump or have insuf-ficient supply. Insofar as breastfeeding is strongly encouraged, infants were assessed for this study only at a time when their mother could not be present to breastfeed. Infants are offered the pacifier as part of their routine care. The experimental group began the early oral feeding protocol 48 hours after full tube feeding was achieved (Fig 1). If an oral feeding was successful, the infants in the experimental group were advanced by 1 oral feeding the next day and followed the protocol. An oral feeding was
considered successful if the entire prescribed volume was taken within 20 minutes without adverse events, such as oxygen desatu-ration or bradycardia. Oxygen desatudesatu-ration is defined as oxygen saturation dropping to ⱖ5% of baseline values. Bradycardia is defined as heart ratesⱕ100. If the feeding was unsuccessful, the previous day’s number of feedings was repeated until success was achieved. Oral feeding in the control group was initiated and advanced at the discretion of the attending physician.
The procedure for oral feedings began by taking the infant out of the incubator and bundling in a receiving blanket.15The infant
was held in an upright position with the head and back supported in straight alignment.15 Small volumetric bottles and standard
premature nipples stocked in our nursery were used. From initi-ation of oral feeding to their attainment of 4 oral feedings/d, the infants were fed by the same investigator (C.S.). They were not encouraged, but were allowed to feed at their own pace for a period of 20 minutes. There was continuous cardiorespiratory and pulse oximetry monitoring during the feedings to detect subtle changes that usually precede apnea and bradycardia.15If an oro/
nasogastric tube was present, it remained in place during the oral feeding,16and any volume remaining after the 20-minute feeding
period was given through the tube.
Oral feeding progress was monitored for the achievement of selected feeding milestones: 1) age at introduction of oral feeding, 2) age at first, 4, and 8 (all) successful oral feedings per day, 3) time from introduction of oral feeding until first successful oral feed-ing, 4) time from first successful oral feeding until all oral feedfeed-ing, and 5) time from all oral feeding until discharge. Overall transfer (percent volume transferred per total volume ordered) and rate of milk transfer (volume transferred per unit time, mL/min) were assessed in both groups from introduction of oral feeding until attainment of the first successful oral feeding. The following clin-ical measures were obtained during each oral feeding session: duration of feeding, episodes of oxygen desaturations, and bra-dycardia. Medical diagnoses, daily weight gain, age at discharge to home, and reasons for hospital stay⬎7 days after achieving all oral feeding were recorded.
Data Analyses
Independent ttest was used to compare the achievement of selected feeding milestones between the 2 groups. The Kaplan-Meier survival technique was applied to the PMA when all oral feeding was achieved. Paired t test was used to examine the change in overall transfer and rate of milk transfer from introduc-tion of oral feeding until the day before the first successful oral feeding within each group of infants. Differences in these 2 out-comes at introduction and first successful oral feeding between groups were assessed using the independentttest.
RESULTS
Thirty-three infants were enrolled in the study. Thirteen infants in the experimental group com-pleted the study. Three infants were dropped from the study because 1 infant received a nonstandard concentrated milk preparation that was difficult to pass through the orifice of the nipple, 1 infant was not fed daily secondary to investigator error, which violated study protocol, and 1 infant was discharged from the hospital while tube feeding and therefore, the study could not be completed. Sixteen infants in the control group completed the study. One infant was dropped secondary to⬎7 days of interruptions in feeding schedule. The subjects were similar in gestational age, birth weight, gender, race distribu-tion, and clinical history (Table 1).
The infants began tube feeding and attained full tube feeding at similar postnatal and PMAs (Table 2). The transition time from full tube feeding to all oral feeding was significantly shorter in the experimental than control group (Table 2).
Oral feeding was introduced⬃2.6 weeks earlier in the experimental group (Table 2). The experimental
infants were successful at 1, 4, and all oral feedings per day at a significantly earlier time than their con-trol counterparts (Table 2). Once both groups were introduced to oral feeding, the control group achieved their first successful oral feeding in signif-icantly fewer days than the experimental group. However, after achieving their first successful feed-ing, both groups attained all oral feedings within the same time interval.
The experimental group had a significantly greater percentage of subjects achieving all oral feeding at an earlier PMA when compared with the control group (Table 2). The percent infants who attained all oral feeding at each postmenstrual week monitored showed a similar pattern of achievement between the 2 groups (Fig 2). However, the pattern was shifted to the left, ie, occurred at an earlier age in the experimental group than in the control group. At 33 weeks’ PMA, 54% of the experimental group had achieved all oral feedings, and only 12.5% of the control group had achieved this goal.
There was a significant increase in overall transfer and rate of milk transfer within groups from intro-duction of oral feeding until achievement of first successful oral feeding (P ⱕ .03). These 2 measures were similar between experimental and control in-fants at introduction of oral feeding as well as at attainment of all oral feeding.
Weight gains and discharge weight for both groups were similar throughout the hospital course. The experimental and control groups were dis-charged respectively at 57 ⫾ 18 days (36.0 ⫾ 2.1 weeks’ PMA) and 67 ⫾ 17 days (37.0 ⫾ 1.8 weeks’ PMA). This difference was not statistically different (Table 2). Reasons, as stated in the medical records, for hospital discharge greater than 1 week after achieving all oral feeding are listed in Table 3.
DISCUSSION
Approximately 40% percent of infants who expe-rience oral feeding difficulties are born premature-ly.17 This is believed to arise primarily from their immaturity. Preterm infants are expected by their clinical caretakers to have attained a term-like pat-tern of sucking when first introduced to oral feeding opportunities. Previous studies have shown that in-fants given the opportunity to feed orally, at 33 to 34
TABLE 1. Infant Characteristics
Experimental n⫽13
Control n⫽16
P Value
Gestational age (wk) 27.8⫾1.3 27.6⫾1.4 0.58
Birth weight (g) 1205⫾303 1033⫾177 .09
% Male 69 63
White:Black:Hispanic 6:6:1 8:7:1
Oxygen therapy (d) 15.5⫾20.7 27.4⫾24.2 .17
Mechanical ventilator 6.1⫾3.2 6.9⫾4.9 .61
Nasal continuous positive airway pressure (d)
24.6⫾13.1 28.9⫾12.4 .37
Introduction to tube-feeding
Postnatal age (d) 8.5⫾3.2 7.6⫾3.7 .45
PMA (wk) 29.1⫾1.2 28.6⫾12.6 .40
Feedings withheld (d) 0.6⫾1.0 1.6⫾2.3 .15
Mean⫾standard deviation.
weeks’ PMA, complete their oral feeding with imma-ture sucking patterns.6 Therefore, using term-like sucking patterns as a goal for preterm infants may not be the appropriate standard for the assessment of readiness to feed orally. Many caretakers believe that by giving these infants time to grow and mature, they will attain all oral feeding. However, an alter-native approach is to allow preterm infants the early opportunity to exercise their innate skills or to stim-ulate the development of these skills. If attainment of all oral feeding can be achieved at an earlier time than currently observed, earlier hospital discharge may be envisaged thereby reducing financial burden and allowing for earlier mother-infant reunion. There is continuing debate on whether the matura-tion of suck-swallow-breathe coordinamatura-tion is related to PMA and/or experience.18 –20 The results of this study support the latter notion inasmuch as infants offered early oral feeding opportunities were able to
attain oral feeding milestones, ie, 1, 4, and all oral feedings per day at significantly earlier times than their control counterparts.
In the present study, preterm infants born ⬍30 weeks’ gestation were introduced to oral feeding around 31 compared with 33 weeks’ PMA for control subjects. The following observations are made from the results obtained. At this early age, although the skills involved for successful oral feeding may not be coordinated fully, episodes of feeding related oxygen desaturations and bradycardia were similar in both the experimental and the control group. At introduc-tion of oral feeding until first successful oral feeding, the younger experimental group performed just as well as its older control counterpart, although the time to achieve their first successful oral feeding was longer for the younger infants. Despite the latter, the experimental group achieved all oral feeding signif-icantly sooner than the control group; the time from
Fig 2. PMA when subjects (experimental, ; control, ---●---) achieved all oral feeding, Kaplan Meier;P⬍.001.
TABLE 2. Oral Feeding Milestones
Experimental Control PValue
Full tubefeeding
Postnatal age (d) 19.5⫾4.7 20.4⫾7.6 .72
PMA (wk) 30.6⫾1.2 30.5⫾1.7 .77
Transition from tube to all oral feeding (d) 26.8⫾12.3 38.4⫾14.0 ⬍.05 Introduction to oral feeding
Postnatal age (d) 22.9⫾5.0 42.8⫾11.2 ⬍.001
PMA (wk) 31.1⫾1.3 33.7⫾0.9 ⬍.001
First successful oral feeding
Postnatal age (d) 32.1⫾9.9 46.9⫾10.9 ⬍.001
PMA (wk) 32.4⫾1.0 34.3⫾0.9 ⬍.001
4 Successful oral feedings
Postnatal age (d) 43.6⫾13.7 54.4⫾12.6 ⬍.05
PMA (wk) 34.1⫾1.7 35.3⫾1.4 ⬍.05
All oral feeding
Postnatal age (d) 46.4⫾13.9 58.7⫾14.5 ⬍.05
PMA (wk) 34.5⫾1.6 36.0⫾1.5 ⬍.05
Introduction of oral feeding to first successful oral feeding (d)
9.3⫾7.7 3.7⫾3.5 ⬍.05
First successful oral feeding to all oral feeding (d)
13.8⫾8.8 11.9⫾6.4 .51
Hospital discharge
Postnatal age (d) 57.0⫾17.7 67.0⫾16.6 .13
PMA (wk) 36.0⫾2.1 37.1⫾1.8 .13
first successful oral feeding until the attainment of all oral feeding being similar for both groups. Taking these 2 observations into consideration, it is ad-vanced that PMA may not be the only accurate de-terminant of successful oral feeding. It is speculated that the longer period of time the younger infants needed from introduction to oral feeding until the first successful oral feeding offered them “practice/ training opportunities.” This is supported by the fact that once successful at oral feeding, they were able to attain all oral feeding as rapidly as their older coun-terparts. The notion of experience is not a new con-cept. Healthy term infants, when introduced to oral feeding, encounter oxygen desaturations and epi-sodes of deglutition apnea similar to those experi-enced by preterm infants.21–24 These events are be-lieved to be secondary to the incoordination of swallowing and breathing that subsides with greater feeding experience and maturation.
In addition to concerns over suck-swallow-breathe incoordination, clinicians also believe that oral feed-ing in preterm infants causes poor weight gain. The present study demonstrated similar daily weight gain between the experimental and control infants throughout their hospital course. An average weight gain of 15 to 20 g/d was maintained by both groups. Thus, the provision of a caloric intake of 120 kcal/ kg/d was sufficient to compensate for the energy expenditure infants encountered during their oral feeding sessions be they introduced at 31 or 33 weeks’ PMA.
A previous study conducted on 171 preterm in-fants bornⱕ30 weeks’ gestation13has shown a cor-relation between time to attainment of all oral feed-ing and discharge to home. We found no such correlation in this study, although our experimental group was discharged 10 days earlier than their con-trol counterpart. The lack of significance in duration of hospitalization may be explained by our small sample size and/or by the fact that our discharge planning criteria did not include plans for the smaller infant who has achieved successfully the milestone of all oral feeding. Guidelines for hospital discharge of preterm infants are detailed in a policy statement from the American Academy of Pediat-rics.12As stated in the guidelines, discharge planning should begin when recovery of the infant is certain. Several medical milestones must be achieved before discharge. Competent oral feeding is one of these milestones. Other milestones include a sustained pat-tern of weight gain of sufficient duration, appropri-ate thermoregulation in an open bed, and
physio-logic mature and stable cardiorespiratory function.12 Although there is no longer a weight criterion for discharge, it is used as a milestone by a number of clinicians. Indeed, the discharge was delayed for 50% of the experimental subjects secondary to weight⬍2 kg, despite achieving all other discharge criteria. The present observation raises 2 important consider-ations. If earlier attainment of all oral feeding is correlated with earlier discharge as substantiated by larger studies,13then the implementation of a proto-col such as described in this study would lead to significant cost savings along with earlier mother-infant reunion.
CONCLUSION
We have shown that initiation of oral feeding be-fore 33 weeks’ PMA is not only feasible for preterm infants, but also allows for earlier attainment of all oral feeding than currently observed. We did not identify a specific PMA in which these infants were ready to take nipple feedings. Instead, we chose to identify a common milestone, achievement of full tube feeding, based on the medical stability of the infant in which to initiate oral feedings. This allowed us to disregard the subjective criteria (ie, specific PMAs or specific weights) for introducing oral feed-ing in preterm infants that bias most caretakers. It is advanced that earlier initiation of oral feeding, in providing greater practice opportunities, helps pre-term infants improve their oral motor skills and co-ordination of suck-swallow-breathe. This, in turn, allowed them to achieve all oral feeding at an earlier PMA. This intervention was not deleterious to the infants, inasmuch as occurrences of oxygen desatu-rations, bradycardia, and daily weight gain were similar between the experimental and control group. Finally, this study provided a structured feeding protocol that can be used to assist clinicians in the management of oral feeding in preterm infants. The protocol eliminated bias based on weight and age criteria for initiating oral feeding. It also provided criteria in which to advance oral feeding. It should be emphasized that this study addressed oral feeding in the healthy preterm infant. It would be beneficial to address these same issues in those preterm infants with more chronic illnesses, such as those with chronic lung disease or neurologic insult. Oral feed-ing in preterm infants is a challenge for clinicians. This study provides some guidelines for initiation, advancement, and improvement of oral feeding skills.
ACKNOWLEDGMENTS
This work was supported by the National Institute of Child Health and Human Development (RO-1-HD-28140). Partial fund-ing was provided from the US Department of Agriculture/Agri-cultural Research Service.
We wish to express their gratitude to E. O. Smith and J. K. Fraley for statistical assistance. We thank the nursing staff and all the infants that helped make this work possible.
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Reasons Experimental Control
Weight⬍2 kg 4 1
Oxygen weaning 1 2
Developed viral illness 1 1
Prolonged discharge planning 2 2
Eye surgery for retinopathy of prematurity
0 1
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Meier B.New York Times.April 23, 2002
DOI: 10.1542/peds.110.3.517
2002;110;517
Pediatrics
Chanda Simpson, Richard J. Schanler and Chantal Lau
Early Introduction of Oral Feeding in Preterm Infants
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Chanda Simpson, Richard J. Schanler and Chantal Lau
Early Introduction of Oral Feeding in Preterm Infants
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