The transition from gavage to nipple feeding is more difficult for preterm infants with bronchopulmonary dysplasia (BPD) compared with healthy preterm infants because of the consequences from chronic respiratory distress. The consequences may include tachypnea, intercostal muscle retractions, and chronic hypoxemia (Bancalari & Gonzalez, 2000). These consequences compromise the neurodevelopmental skills needed for nipple feeding. Infants with BPD have been reported to take 15–28 days on average to achieve full nipple feeding (Howe, Sheu, & Holzman, 2007; Pridham et al., 1998) compared with healthy preterm infants who take 5–15 days on average (Howe, Sheu, & Holzman, 2007; M cCain, Gartside, Greenberg, & Lott, 2001).
A preterm infant’s achievement of nipple feeding requires three types of neurodevelopmental capabilities: (a) coordination of sucking and swallowing with breathing, (b) organization of behavior expressed in states of wakefulness and sleep, and (c) regulation of cardiorespiratory control via the autonomic nervous system. For preterm infants with BPD, the compensatory tachypnea of hypoxemia interrupts the coordination of sucking and swallowing with breathing, causes fatigue that diminishes the infant’s ability to maintain awake behavior, and can disrupt heart rate stability (Mizuno et al., 2007). The coordination of rhythmic sucking, swallowing, and breathing patterns during feeding is disorganized in preterm infants with BPD (Craig, Lee, Freer, & Laing, 1999; Gewolb, Bosma, Reynolds, & Vice, 2003; Gewolb, Bosma, Taciak, & Vice, 2001; Gewolb & Vice, 2006). Infants with BPD have lower suck rates (Howe, Sheu, & Holzman, 2007) and take longer pauses between nutritive sucks than infants without BPD, suggesting that the infants are modifying their suck–swallow–breathe rhythm to increase their breathing time (Medoff-Cooper, McGrath, & Shults, 2002). When supplemental oxygen is required, preterm infants with BPD have lower oxygen saturations, poorer suck–swallow–breath coordination, and ingest less volume with nipple feeding compared with similar infants who do not require supplemental oxygen (Mizuno et al., 2007). Dyspnea and tachypnea with BPD can lead to fatigue with feeding, which results in sleepy behavior that places an infant at risk for choking with resulting apnea, bradycardia, or both.
The semidemand method tested in this study addressed the respiratory distress of infants with BPD by systematic use of infant behavioral cues and cardiorespiratory signs to regulate frequency, length, and volume of nipple feedings. The method is called semidemand because preterm infants <34 weeks postmenstrual age (PMA) may display feeding readiness signs such as awakening or sucking on fingers that are less robust than crying, which is used as a feeding readiness sign in demand feeding for term infants. Under conditions of less robust signs of feeding readiness, a nurse must interpret an infant’s signs appropriately and intervene accordingly. Also, with the semidemand method during the transition period when both gavage and nipple feedings are occurring, infants are fed prescribed volumes based on their caloric needs for growth. This method is in comparison to ad libitum feeding volumes allowed for term infants and for healthy preterm infants who have achieved full nipple feeding. In contrast, the standard practice for introducing nipple feeding to preterm infants <34 weeks PMA, with and without BPD, is to limit nipple feeds to preset frequencies and times. The objective of this study was to test the semidemand method for preterm infants with BPD.
BPD was described first in 1967 as injury to the infant lung resulting from mechanical ventilation and oxygen therapy for treatment of acute respiratory distress syndrome (Northway, Rosan, & Porter, 1967). By 1979, the diagnostic criteria for BPD were oxygen requirement and radiographic evidence of airway injury, inflammation, and fibrosis at 28 days of life (National Institutes of Health, 1979). Beginning in the late 1980s and early 1990s, the use of exogenous surfactant replacement, antenatal glucocorticoids, and improved ventilation strategies resulted in less severe lung injury in older preterm infants and increased survival of extremely preterm neonates (Bancalari & Claure, 2006; Jobe & Bancalari, 2001). Today, in the postexogenous surfactant era, the new pathology of BPD is characterized by alveolar hypoplasia, minimal lung fibrosis, and decreased pulmonary microvascular development (Bancalari & Claure, 2006; Husain, Siddiqui, & Stocker, 1998). A workshop of the National Institute of Child Health and Human Development, the National Heart, Lung and Blood Institute, and the Office of Rare Diseases, convened in 2000, defined diagnostic criteria for the new BPD as treatment with oxygen >21% for at least 28 days of life (Jobe & Bancalari, 2001). The prolonged need (sometimes weeks or months) of infants with BPD for mechanical ventilation and supplemental oxygen has consequences (Bancalari & Gonzalez, 2000). Tachypnea, dyspnea, intercostal muscle retractions, and wheezing signal the development of chronic respiratory distress. The growth of infants with BPD is less than their gestational age peers without BPD, very likely due to chronic hypoxemia and increased energy expenditure (Bancalari & Gonzalez, 2000; de Meer et al., 1997; Huysman et al., 2003).
The incidence of BPD was 23% for all infants with birth weights of <1,500 g but was reported at 52% for infants with birth weights of 501–750 g (Lemons et al., 2001). Male infants have a 60% rate of BPD compared with a 40% rate in female infants (Kaempf et al., 2008; Klinger, Sirota, Lusky, Reichman, & Israel Neonatal Network, 2006). The cost of hospitalization after birth for infants born at 500–700 g is $224,400, compared with a cost of $1,000 for infants weighing >3,000 g (Gilbert, Nesbitt, & Danielson, 2003). This increased cost is related to longer hospitalizations for preterm infants, especially those with BPD. In a sample of 139 preterm infants with BPD (gestational ages, 24–32 weeks), discharge from hospital was delayed by 2 weeks compared with preterm infants without BPD related to meeting the criteria of full nipple feeding, maintenance of body temperature, and being weaned from supplemental oxygen (Bakewell-Sachs, Medoff-Cooper, Escobar, Silber, & Lorch, 2009). Howe, Sheu, and Holzman (2007) also reported that preterm infants with BPD (n = 41) required longer hospital stays to accomplish full nipple feeding compared with infants without BPD (n = 99).
In a retrospective, medical record review from two Midwestern nurseries, infants with BPD in the postexogenous surfactant era (n = 21) took an average of 15.3 ± 8.1 days to transition from gavage to nipple feeding. Infants with BPD took 7 more days on average to achieve full nipple feeding compared with infants without BPD (n = 15; Pridham et al., 1998). The average age at which nipple feeding was started was 34.6 ± 2.3 weeks PMA for infants with BPD. Transition time was not affected by gender, number of days on a ventilator, or number of days on supplemental oxygen. In more recent studies, infants with BPD (n = 41) were older at an average of 38.5 weeks PMA when they attained full feeding compared with infants without BPD (n = 99) who were on average 35.5 weeks PMA (Howe, Sheu, & Holzman, 2007). Preterm infants with BPD (n = 139) attained nipple feeding at a median PMA of 36.6 weeks compared with preterm infants without BPD (n = 726), who reached full nipple feeding at a median PMA of 34 weeks. There were no differences related to gender and attainment of nipple feeding. (Bakewell-Sachs et al., 2009). Age at the start of feeding and the number of days to attain nipple feeding were not reported in these recent studies.
The standard practice for introducing nipple feeding is to limit nipple feeds to preset frequencies and times. In contrast, the semidemand method tested in this study provides for offering nipple feedings at times and frequencies in response to an infant’s readiness (e.g., awake behavior, sucking on fingers) and tolerance of nipple feeding (e.g., infant initiated and sustained sucking without cardiorespiratory distress). The semidemand method is guided by Barnard’s (1978) model of reciprocal interaction between caregiver and infant. The interaction occurs as the infant expresses behavioral cues and physiological signs to which the caregiver responds. The caregiver, correctly interpreting the infant’s cues and signs, responds in a way to maximize the feeding experience for the infant.
The semidemand method tested in this study provides for offering nipple feedings at times and frequencies in response to an infant’s readiness and tolerance of nipple feeding.
In two experimental studies with healthy, preterm infants of 32–34 weeks PMA, nipple feedings were offered based on infants’ behavioral and physiological responses (Anderson et al., 1990; McCain et al., 2001). The results were that the infants reached full nipple feeding sooner (McCain et al., 2001) and gained more weight (Anderson et al., 1990) compared with control infants receiving standard care. In a study of mothers feeding their healthy preterm infants of 34 weeks PMA, infant success with feeding was related to infant readiness to feed and not jiggling the nipple to force infant sucking (Thoyre & Brown, 2004).
Preterm infants who are in awake states at the beginning of nipple feedings are more successful at ingesting their feeding volumes (Anderson et al., 1990; McCain, 1997; Pickler, Higgins, & Crummette, 1993). In addition, preterm infants who were successful at ingesting their feeding volumes spent more time in awake states compared with infants who were unsuccessful with feeding (McCain, 1997).
In descriptive studies with healthy preterm infants, an association has been shown between feeding experience and attainment of nipple feeding (Howe, Sheu, Hinojosa, Lin, & Holzman, 2007; Medoff-Cooper et al., 2002; Pickler, Best, & Crosson, 2009). In addition, the results of two experimental studies with healthy preterm infants were that increased feeding experience was associated with a shorter time to attain nipple feeding compared with control infants who were given fewer opportunities for feeding (McCain et al., 2001; Simpson, Schanler, & Lau, 2002).
The semidemand method includes offering the infant a pacifier before feeding to help bring the infant to an awake, alert state. The practice of offering a pacifier to healthy, preterm infants before beginning nipple feeding brings infants to an awake state (Gill, Behnke, Conlon, & Anderson, 1992; McCain, 1992) and decreases the length of feeding time (Hill, 2005). However, no effect from nonnutritive sucking on nipple feeding success also has been reported (Pickler & Reyna, 2004).
The primary hypothesis for this study was that experimental infants who received the semidemand feeding protocol would achieve full nipple feeding in fewer days than control infants who received the standard care for making the transition from gavage to nipple feeding. It was also hypothesized that the experimental infants would be discharged from the hospital sooner than control infants.
Setting and Sample
A randomized, two-group, experiment was conducted in the Neonatal Intensive Care Unit at the University of Miami/Jackson Memorial Hospital in Miami, Florida (Figure 1).
The study was approved by the University’s Institutional Review Board, and written informed consent was obtained from parents of the infants in the study. Preterm infants born at <34 weeks gestation with BPD were eligible for the study. A diagnosis of BPD was based on the continued need for treatment with oxygen >21% for >28 days of life (Jobe & Bancalari, 2001). Exclusion criteria were infants with major congenital anomalies, gastrointestinal disorders (e.g., necrotizing enterocolitis), congenital infections, and major neurological conditions (e.g., cerebral palsy, seizures, Grades III–IV intracranial hemorrhage, periventricular leukomalacia). A sample size estimation was calculated to use 80% power, alpha = .05, improvement (in time to transition from gavage to nipple feeding) = 50%, and six covariables (gender, race [Black, Hispanic, White], birth gestational age, PMA on study enrollment, birth type [singleton, twin, triplet/quadruplet], and respiratory status [breathing room air or supplemental oxygen]). The group size needed was 86 total subjects (43 per group). Infants were identified as meeting criteria for recruitment if they had received supplemental oxygen at >21% for 28 days or more, and their respiratory status was evaluated as stable enough to begin nipple feeding by the attending neonatologist. Nipple feedings were not begun until infants were started on either the control or experimental protocols.
After informed consent was obtained, infants were randomized to the control or experimental groups. Randomization was done using the technique of minimization and included stratifying for birth weight (<1,000 g and 1,000–2,000 g), birth gestational age (<28 weeks and ≥28–34 weeks), gender, and race (White, Black, Hispanic, other; Conlon & Anderson, 1990; Pocock & Simon, 1975). The procedure produced two study groups matched on these characteristics (Table 1).
Infants began the feeding protocols at the start of first nipple feedings and continued on their respective protocols until they achieved full nipple feeding without the need for supplemental gavage. Days to nipple feeding was operationalized as the number of days from the day of the first nipple feeding to the day when all feedings were nippled in entirety without the need for any gavage. Infants in both study groups had indwelling nasogastric tubes in place that allowed for them to receive any volume that they were unable to ingest during a nipple feeding. All infants were nipple fed with standard nipples on 30-ml volume containers. Infants were fed fortified human milk or commercial formula at 24 cal/oz based on 105–130 kcal/kg/day as prescribed by the attending neonatologist (Committee on Nutrition, American Academy of Pediatrics, 1998). The infants were swaddled with their hands free and were held in an upright position for feedings. Infants were fed at 3-hour intervals. Data collection began in March 2006 and was completed in March 2009.
The control infants received the standard care for transitioning from gavage to nipple feeding with gradual increases in the number of nipple to gavage feedings per day. The number of nipple feedings was increased based on an infant being able to ingest the prescribed volume without cardiorespiratory distress and gain weight. The nipple/gavage ratios for advancing control infants were 1 nipple:7 gavage feedings on Day 1, 3 nipple:5 gavage on Day 2, 4 nipple:4 gavage on Days 3 and 4, 6 nipple:2 gavage on Day 5, and 8 nipple feedings on Day 6.
The experimental infants on the semidemand protocol were offered nipple feedings in response to their behavioral and cardiorespiratory responses, which were used to regulate frequency, length, and volume of nipple feedings. That is, experimental infants were offered nipple feedings at 3-hour intervals if they were in an awake behavioral state. Experimental infants were offered a pacifier before feeding to bring them to an awake state. Nurses assigned to the experimental protocol were taught to assess awake behavior with a modified Anderson Behavioral State Scale (Gill et al., 1992). Interrater reliability was maintained at >90% throughout data collection. Nurses were taught the behavioral scale assessment. Initially, a study staff member and each nurse did six behavioral assessments at the same time but scored independently of each other. The independent assessment scores from the study staff member and nurse were correlated for percent agreement. If the percent agreement was <90%, the study staff member continued assessments with a nurse until 90% agreement was reached. The reliability checks continued on a weekly basis for the first 3 months of data collection and then were done monthly for the remainder of the data collection period.
The pacifier was offered during prefeeding care that included vital signs and a diaper change (approximately 5 minutes). If an infant did not come to an awake state, the feeding was given by gavage. Infants were nipple fed to their tolerance, so feedings were stopped when an infant ingested the entire amount of feeding volume, refused to suck any longer, fell asleep, or had a distress event (e.g., choking, apnea, bradycardia). Nurses were assigned exclusively to the control or experimental condition. The nurses received group instruction about their assigned protocols at the start of infant enrollment, and this instruction was repeated at the midpoint of the data collection period. In addition, the respective study protocols were provided at the bedside and reviewed with each assigned nurse on a daily basis.
The semidemand method tested previously with healthy infants was modified in this study for preterm infants with BPD (McCain et al., 2001). Those healthy preterm infants were permitted up to 3.5 hours between feedings if they did not awaken after 3 hours, and they were allowed ad libitum volume after reaching full nipple feeding. In this study of preterm infants with BPD, the infants were fed at 3-hour intervals because of their caloric needs, and they were not fed ad libitum volumes on attaining full nipple feeding because of the prevalence of reflux in these infants. The decision not to allow ad libitum feedings for infants with BPD also was supported by the findings of Pridham et al. (1999) that preterm infants (including some with BPD) fed ad libitum while transitioning to nipple feedings had lower caloric intakes compared with infants fed a prescribed caloric intake.
Characteristics of the infants were compared with chi-square tests for categorical data and independent Student’s t tests for interval-level data. The number of days to achieve full nipple feeding and length of hospital stay between study groups was analyzed with generalized linear model procedures using the six covariables.
A total of 96 preterm infants with BPD were enrolled on the study protocols, and 86 completed the protocols (Figure 1). Six control infants were withdrawn from the study due to feeding intolerance (n = 3), sepsis (n = 1), pneumonia (n = 1), and mother’s request (n = 1). Four experimental infants were withdrawn due to feeding intolerance (n = 1), sepsis (n = 1), persistent tachypnea (n = 1), and mother’s request (n = 1). The characteristics of the sample are illustrated in Table 1. There were no differences in demographic or medical characteristics between the control and experimental groups, except that only the experimental group had triplet/quadruplet infants.
The experimental infants took a shorter time to achieve full nipple feeding compared with the control infants and achieved nipple feeding 50% sooner than control infants (Table 2). Female infants achieved nipple feeding sooner than male infants. Infants who were breathing room air achieved nipple feeding sooner than infants receiving supplemental oxygen. The other covariables of gestational age, PMA on study enrollment, race, and singleton or multiple birth had no effect on days to achieve nipple feeding. Length of hospital stay was not significantly different between the study groups. The experimental infants were hospitalized for an average of 106.9 ± 27.6 days and the control infants for 115.9 ± 39.4 days.
The period of 5.9 days to achieve nipple feeding for the experimental infants is an improvement over the period of 15–28 days to achieve nipple feeding reported in the literature for infants with BPD (Howe, Sheu, & Holzman, 2007; Pridham et al., 1998). The period of 12.3 days to achieve nipple feeding for the control infants also is better than the time period reported in the literature. This may be because the control group infants were all advanced in the same way on a daily basis. In actual standard clinical care, feeding advancement differs by clinician and may not be systematic on a daily basis or from one infant to another.
These results mirror the findings from a previous study to test the semidemand method with healthy preterm infants (McCain et al., 2001). The healthy preterm infants who received the semidemand method achieved full nipple feeding in 5 days on average compared with control infants who received standard care and took 10 days on average. The healthy preterm infants and the preterm infants with BPD who were transitioned to nipple feeding with the semidemand protocol had the same 50% reduction in time to reach full nipple feeding compared with control infants who received standard care. This same percentage improvement occurred despite older PMA and the presence of chronic respiratory disease at the onset of nipple feeding for the infants with BPD. The healthy preterm infants in the previous study were started on nipple feeding when they were 32 weeks PMA compared with the infants with BPD who started nipple feeding on average at 36 weeks PMA. It took the preterm infants with BPD in this study a longer time to achieve nipple feeding than the healthy preterm infants in the previous study despite their more mature age at onset of nipple feedings. The extended time it takes preterm infants with BPD to achieve nipple feeding relates to their chronic respiratory distress. That is, the integration of sucking and swallowing with breathing is disorganized (Craig et al., 1999) because the infants compensate for chronic hypoxemia with longer pauses for breathing (Medoff-Cooper et al., 2002).
Using the semidemand method, the nurses assessed the infants for signs of feeding tolerance or intolerance and continued or discontinued the nipple feeding as appropriate. This allowed for feedings to be led by the infant, rather than by the nurse. In standard practice, when an infant is prescribed a limited number of nipple feedings per day, nurses may feel pressured to make the infants take their nipple feedings. This is because attainment of nipple feeding is usually the last criterion that infants must meet before hospital discharge, and nurses are vested in helping infants achieve readiness for hospital discharge. Also, the prescribed nipple feedings may not always be timed with an infant’s optimal behavior and cardiorespiratory status. For example, a sleepy infant who is coaxed to feed may choke. In contrast, the responsive approach to feeding with the semidemand method allows the infants to practice coordinating sucking and swallowing with breathing only when they are in an optimal state to do so, and the nurses to respond to the infants’ cues to allow the feeding to progress or not. Feedings that are offered in response to infants’ signs of tolerance or intolerance result in safer and less stressful feedings, which is uniquely important for preterm infants with BPD who have altered suck-swallow-breath patterns. As Howe, Sheu, and Holzman (2007) reported, infants with BPD have lower suck rates and immature sucking patterns. It may be that the ability to ingest the necessary nutrient volume for growth requirements is a stronger indicator of discharge readiness than sucking organization. Offering a pacifier to experimental infants before feeding also may have given them an advantage related to helping them awaken before feeding (Gill et al., 1992; McCain, 1992) and shorten the length of feeding (Hill, 2005).
Female infants achieved feeding sooner than male infants. Others have reported no gender effect on feeding achievement for preterm infants with BPD (Bakewell-Sachs et al., 2009; Pridham et al., 1998). Fewer female infants are diagnosed with BPD (40%) compared with male infants (60%), so there may be some overall female advantage related to less BPD (Kaempf et al., 2008; Klinger et al., 2006). However, in the current sample there were equal numbers of male and female infants with BPD.
It was not unexpected that the infants receiving supplemental oxygen would require a longer time to achieve nipple feeding compared with the infants who had been weaned to breathing room air. This may have occurred because infants who need supplemental oxygen to maintain adequate oxygen saturation are taxed further by the work of feeding. This compounds the disorganized coordination of sucking and swallowing with respiration that accompanies BPD in general. This finding supports the work by Mizuno et al. (2007), who reported poor feeding outcomes in preterm infants with BPD who required supplemental oxygen compared with similar infants without a supplemental oxygen requirement.
Infants who received the semidemand method were hospitalized on average 9 days less than the control infants, but this was not a significant difference. The feeding study affected only the time period during hospitalization when the infants were transitioning from gavage to nipple feeding, a small portion of the hospital stay. Other factors also affected overall length of hospitalization, including maintenance of body temperature and the need for supplemental oxygen (Bakewell-Sachs et al., 2009). Some infants in the current study were being weaned from heated incubators, and 31 infants still needed supplemental oxygen after completing the study. The need for a heated incubator environment and supplemental oxygen extended the need for hospitalization for some of the infants. Despite no significant difference in the overall length of hospitalization, an average of 9 fewer days for the infants receiving the semidemand method is important to parents who have been waiting months to take their infants home into their full-time care. Being able to have their infant at home allows the family to resume a measure of family normalcy, which is disrupted during an infant’s extended stay in a Neonatal Intensive Care Unit. Preterm infants with BPD have significant neonatal costs from their initial hospitalization compared with term neonates (Gilbert et al., 2003). Having BPD doubles the length of hospital stay compared with infants without BPD, and so length of stay has a direct effect on hospital costs (Gilbert et al., 2003). Shortening the length of hospital stay for infants with BPD contributes to cost savings.
Strengths and Limitations
The major limitation was that the experiment could not be blinded, and the validity concern was that the two study protocols would not be maintained as designed. Nurses assigned to the control protocol adhered to it generally without prompting because it was standard care, and they did not have to change their practice. Assuring adherence to the experimental protocol required daily review of the feeding plan with the assigned nurses. The strength of the study was that the semidemand intervention was tested using a randomized, experimental design.
In summary, the use of the semidemand method for preterm infants with BPD shortens the time for transition from gavage to nipple feeding compared with the standard care. The semidemand method considers the immaturity of preterm infants’ suck–swallow–breathing coordination and cardiorespiratory control, as well as the respiratory compromise associated with BPD, so the transition from gavage to nipple is more responsive to the infants than standard care.
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