PEDIATRICS Vol. 120 No. 4 October 2007, pp. e1035-e1042 (doi:10.1542/peds.2006-3567)
ARTICLE |
Infants With Bronchopulmonary Dysplasia Suckle With Weak Pressures to Maintain Breathing During Feeding
Department of Pediatrics, Showa University of Medicine, Tokyo, Japan
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ABSTRACT |
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 TOP ABSTRACT PATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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OBJECTIVE. Preterm infants with bronchopulmonary dysplasia often demonstrate sucking difficulties. The aim of this study was to determine whether the severity of bronchopulmonary dysplasia affects not only coordination among suck–swallow–respiration but also sucking endurance and performance itself.
PATIENTS AND METHODS. Twenty very low birth weight infants were studied. Infants with anomalies or intraventricular hemorrhage were excluded from the evaluation. Subjects were divided into 3 groups: no bronchopulmonary dysplasia (7 infants), bronchopulmonary dysplasia without home oxygen therapy (7 infants), and bronchopulmonary dysplasia with home oxygen therapy (6 infants). In addition to sucking efficiency, pressure, frequency, duration, and duration of sucking burst, length of deglutition apnea, number of swallows per burst, and respiratory rate were also measured during bottle-feeding at 40 weeks' postmenstrual age. In addition, PCO2 and oxygen saturation were measured at rest and during bottle-feeding.
RESULTS. Infants with severe bronchopulmonary dysplasia demonstrated not only the lowest sucking pressure and sucking frequency, shortest sucking burst duration, and lowest feeding efficiency but also the lowest frequency of swallows during the run and the longest deglutition apnea. The respiratory rate was highest, and the decrease in oxygen saturation was largest, in infants with severe bronchopulmonary dysplasia.
CONCLUSIONS. Feeding problems depend on the severity of bronchopulmonary dysplasia. Infants with bronchopulmonary dysplasia demonstrated not only poor feeding coordination but also poor feeding endurance and performance.
Key Words: bronchopulmonary dysplasia • home oxygen therapy • sucking • swallowing • very low birth weight infant
Abbreviations: BPD—bronchopulmonary dysplasia • PMA—postmenstrual age • HOT—home oxygen therapy
We recently reported that preterm infants without respiratory problems such as bronchopulmonary dysplasia (BPD) demonstrate better feeding efficiency with maturation.1 At 35 weeks' postmenstrual age (PMA), it was found that preterm infants do not stop breathing because of swallowing: the most frequent swallow and respiration pattern is inspiration–swallow–expiration, which is seen in term infants at 4 to 5 days of age.2 Sucking efficiency significantly increased between 34 and 36 weeks' PMA and exceeded 7 mL/minute at 35 weeks. There were significant increases in sucking pressure between 33 and 36 weeks as well.1 In other words, preterm infants demonstrate not only more coordinated suck–swallow–breathe but also better sucking endurance and performance with maturation. Because the mean gestational age and mean birth weight of the studied infants were 30.0 weeks and 1505 g, respectively, they were not very immature infants.
Recent advances in perinatal and neonatal medicine have resulted in an increased survival rate for very premature infants. However, the prevalence of BPD in such infants has increased, and they often demonstrate sucking difficulties. Therefore, it is necessary to understand the reasons underlying the sucking difficulties of BPD to establish a suitable feeding strategy for these infants. We need to evaluate the 2 elements that affect overall feeding behavior: coordination of suck–swallow–breathe and sucking endurance and performance.
In an infant with respiratory compromise, the respiratory suppression that occurs during the continuous sucking burst may not be well tolerated or sustainable for an entire feed. Successful feeding in infants with BPD is further compromised by acute oxygen desaturation during feeding.3,4 Recent studies5,6 noted that breathing patterns during feeding in infants with BPD did not demonstrate the striking regularity seen in control term infants. Infants with BPD have a high prevalence of suck–swallow–breathe coordination difficulties.5–9 Gewolb et al10 recently studied the patterns of suckle and swallow rhythms and found that anticipated maturational patterns of suckle and swallow rhythms did not occur in infants with BPD. They also compared the integration of suck and swallow rhythms during feeding in preterm infants with and without BPD11 and presented supportive data that infants with BPD do not follow predicted maturational patterns of suck–swallow rhythmic integration.12
Although sucking endurance/performance is one of the key elements in successful oral feeding, research focusing on sucking performance (ie, the sucking pressure or frequency) of preterm infants with BPD is limited. Therefore, we do not know whether the feeding difficulties in preterm infants with BPD are related to incoordination between swallowing and breathing or sucking endurance/performance itself or both of these factors.
We hypothesized that infants with BPD may suffer not only from poorly coordinated suck–swallow–breathe but also from poor sucking endurance and performance. The aim of this study was to determine whether the severity of BPD affects sucking performance; for example, sucking pressure, duration of sucking burst, and sucking frequency. In addition, we examined the effect of the severity of BPD on the swallowing and breathing relationship.
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PATIENTS AND METHODS |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Patients
Twenty very low birth weight infants admitted to the NICU of Chiba Children's Hospital or Showa University Hospital between January 1, 2003, and August 31, 2006, were the subjects of this study.
Infants who had anomalies or neurologic sequelae or who were ventilator dependent at the time of study were excluded from the evaluation. In addition, infants who could not be fed orally before 41 weeks' PMA were excluded from evaluation. Written informed consent was obtained before enrollment in the study. These 20 VLBW infants were divided into 3 groups according to the existence of BPD and the severity of BPD determined by the necessity of home oxygen therapy (HOT).
- Group A: Infants were not compromised with BPD.
- Group B: Infants were compromised with BPD, but did not need HOT. The mean age when oxygen support was discontinued was 33.8 weeks' PMA.
- Group C: Infants were compromised with BPD and needed HOT. At the time of study, they needed supplemental oxygen (fraction of inspired oxygen: 0.3–0.4).
- The background of these infants including the age of the first oral feed and the amount and duration of the feed under study is shown in Table 1.
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Methods
The infants were studied during bottle-feeding at 40 ± 1 weeks' PMA. Infants were evaluated during bottle-feeding of room-temperature breast milk (own mother's milk) at the regular feeding time. The feeding time was standardized (every 3 hours; 8 times per day). All infants at 40 ± 1 weeks' PMA were given 8 oral feedings per day, which is the common protocol used in Japan. Infants, especially those with chronic lung disease, were not forced to suck. Any remaining milk was given via a nasogastric tube. The evaluation was performed twice at 1 and 4 PM to confirm reproducibility. The volume fed was between 20 and 50 mL, depending on the ability to feed, because the evaluation was stopped after 20 minutes of feeding.
We used a study design that was described elsewhere.1,13–15 In brief, the infants were held in a semi-upright supine position for feeding. This position was maintained by 1 of the investigators throughout the feeding period (Fig 1). The teats, supplied by Pigeon Co, Ltd (Tokyo, Japan), were modified to measure the intraoral sucking pressures of the infants and were those routinely used in the nursery. A 1-mm inside-diameter silicone tube was inserted inside the teat and opened near the nipple hole; the other end of the tube was connected to a microsemiconductor pressure transducer (Teac/Kurite transducer; Kurite Co, Ltd, Tokyo, Japan). The pressure was amplified with an SA 58 DC amplifier (Teac Co, Ltd, Tokyo, Japan) and recorded into a DR-F3 digital recorder (Teac Co, Ltd).
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To record the pharyngeal pressure, an open-ended 4F or 5F silicone catheter was introduced transnasally with the tip at the oropharynx; it was then connected to a pressure transducer. The length between the oropharynx and the mouth was measured with a routine chest radiographic examination. Catheter insertion occasionally caused a sneeze, but once in place, the catheter had no apparent effect. A sensor on the foot was used to record oxygen saturation, and heart rate was recorded with a pulse oximeter (Nellcor N3000, Pleasanton, CA). A transcutaneous PO2/PCO2 electrode (OKV 7301; Nippon Coden, Tokyo, Japan) was used to measure the PCO2 values. Before the evaluation, any nasogastric tubing that was in place for feeding was removed if the feeding tube was in place. The size of the catheter used for the swallowing measurement was the same as or smaller than the nasogastric tube. As such, we assumed that the silicone catheter affected the respiratory condition of the studied infants minimally, if at all.
To record the small changes in air flow associated with respiration, a miniaturized pneumotachograph, connected to a pressure transducer, was inserted into 1 nostril.16 The flow head consisted of a plastic tube that was 5 mm in diameter and 12 mm long. The distal end carries a 100-mesh stainless steel gauze, held in place by an end cap. The measured pressure drop across the mesh varied linearly with flow up to 15 mL/seconds. The resistance for inspiration was 0.1 mmH2O/mL per second and 10% higher for expiration. We confirmed that the effects on respiration were small by comparing the SpO2 and PCO2 values before and after attachment of the apparatus.
Sucking Variables
The sucking pressure, frequency, and duration were obtained by measuring the sucking waves. Feeding efficiency was determined as the amount of volume/total feeding time (mL/minute). A suck or swallow burst is defined as 
3 events with interevent intervals of 
2 seconds.10 The length of sucking burst is one of the sucking variables.
Swallowing Variables
Swallowing events were recorded by the method described by Pickens et al.17 Swallows were identified by a characteristic peak of the pharyngeal pressure, which rises rapidly and remains elevated for 0.5 seconds.18 Other events associated with increased pharyngeal pressure, for example, emesis or forced expiration (as in coughing or sneezing), were identified by visual observation. The number of swallows during a swallow burst was measured throughout feeding.
Respiration Variables
The amplitude of the most recent series of uninterrupted breaths was used as the baseline, and movement of 20% of this amplitude was considered a valid breath.19 The duration of deglutition apnea (ie, the duration of 0 nasal airflow associated with each swallow) and respiratory rate during feeding were evaluated throughout the feeding.
Statistical Analysis
To determine whether there was a difference in sucking variables among the 3 groups, we performed an analysis of variance (using Microsoft [Redmond, WA] Excel for statistics). When there was a significant difference, we performed a posthoc Fisher's probable least-squares difference test to obtain where the difference lied. Values were expressed as mean ± SD, and P < .05 was considered significant.
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RESULTS |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Seven infants were not diagnosed as having BPD (group A), 7 infants were diagnosed as having BPD, but they did not need oxygen at the time of the study (group B), and 6 infants needed HOT because of severe BPD (group C).
Mean gestational age and mean birth weight of each group was: 28.8 ± 2.2 weeks and 1117 ± 286 g (group A; n = 7); 27.7 ± 0.8 weeks and 970 ± 282 g (group B; n = 7); and 26.7 ± 2.6 weeks and 783 ± 234 g (group C; n = 6), respectively (Table 1). There were no significant differences in gestational age and birth weight. The reasons for the severe BPD were intrauterine infection in 4 infants and respiratory distress syndrome in 2 infants. In terms of sucking efficiency, there were significant differences (P < .01) in sucking efficiency between all groups. Group A showed the highest efficiency (9.0 ± 0.5 mL/minute), group B was 6.6 ± 1.9, and group C was the lowest (1.9 ± 0.5). The feed amount and feed time for each infant are shown in Table 1.
Sucking Variables (Table 2)
Sucking Pressure
Sucking pressures were –92.2 ± 16, –69.6 ± 16, and –26.5 ± 8 mmHg in groups A, B, and C, respectively. There were significant differences between all 3 pairs (P < .01).
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Sucking Frequency
Sucking frequencies were 72.0 ± 4.9, 57.9 ± 9.8, and 21.8 ± 2.9 sucks per minute in groups A, B, and C, respectively. There were significant differences between all 3 pairs (P < .01).
In terms of sucking waveform, the infants in group B demonstrated a sucking-pressure waveform that was smaller and less consistent compared with infants in group A (Figs 2 and 3). The infants in group C demonstrated the weakest negative pressure and the lowest sucking frequency (Fig 4).
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Duration for Each Suck
Durations for each suck were 0.79 ± 0.1, 0.75 ± 0.1, and 0.42 ± 0.03 seconds in groups A, B, and C, respectively. There was no significant difference between groups A and B, but group C showed significantly shorter duration in comparison (P < .01).
Duration of Sucking Burst
Group C demonstrated significantly shorter sucking burst (5.3 ± 0.6 seconds) compared with that of group A (10.4 ± 3.3; P < .01). There was also a significant difference between groups A and B (7.4 ± 1.4; P < .05).
Swallowing and Respiration (Table 3)
Swallowing in a Run
Group C (4.7 ± 1.5 swallows/burst) demonstrated significantly less sucking in each swallowing run compared with that in group A (13.7 ± 2.1) or B (12.3 ± 2.4; P < .001)
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Respiration
There were significant differences (P < .001) in respiratory rate between groups A (38.9 ± 5.4 per minute) and B (50.7 ± 5.0 per minute) or C (52.8 ± 8.3 per minute). There was no significant difference between groups B and C.
Deglutition Apnea
Infants in group C demonstrated significantly (P < .001) longer deglutition apnea (1721.7 ± 157.5 milliseconds) compared with that of group A (524.3 ± 80.9) or group B (800 ± 163.4). Group B showed significantly (P < .01) longer deglutition apnea than group A.
CO2 Level and Oxygen Saturation
PCO2 Values
The baseline CO2 values were 42.7 ± 2.0, 45.3 ± 2.6, and 52.5 ± 2.3 mmHg in groups A, B, and C, respectively. There were significant differences between groups: P < .05 for group A versus B, and P < .001 for group A versus C and group B versus C. The CO2 values during feeding were 43.7 ± 2.1, 45.9 ± 2.9, and 53.5 ± 2.4 mmHg in groups A, B, and C, respectively. There were significant differences between group C and group A or B (P < .001) but no differences between group A and B.
The percentage of time during the feeding that PCO2 values were >50 mmHg in group C (76.4%) was significantly longer compared with groups A (1.1%) and B (7.7%). There was no significant difference between groups A and B.
SpO2 Values
The mean baseline oxygen saturation was 98.3 ± 0.9, 98.2 ± 0.8, and 97.9 ± 0.8% in groups A, B, and C, respectively. There were no significant differences between groups. The mean oxygen saturation during feeding was 94.6 ± 1.0, 91.4 ± 1.4, and 87.9 ± 1.8% in groups A, B, and C, respectively. There were significant differences between groups (P < .01 for all possible pairs). Group C (58.6 ± 5.0%) showed significantly longer duration of SpO2 below 90% compared with groups A (3.5 ± 1.0%) and B (9.2 ± 1.2%). There was no significant difference between groups A and B. Although the infants in group C were given oxygen supplements of 0.3 to 0.4 fraction of inspired oxygen (oxygen concentration was not increased during feeding), they demonstrated the lowest oxygen saturation during feeding. There were significant differences in SpO2 values between baseline and during feeding in all 3 groups.
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DISCUSSION |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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It is well known that sucking endurance and performance and/or coordination of suck–swallow–breathe are 2 important elements that can affect the overall feeding ability of an infant. Because previous studies did not differentiate between these issues, we evaluated sucking endurance and performance as well as coordination of suck–swallow–breathe in very low birth weight infants during oral feeding.
The study results reveal that BPD results not only in poor suck–swallow–breathe coordination but also in poor sucking endurance and performance. Although infants with severe BPD needed to breathe more frequently compared with infants without BPD or with mild to moderate BPD, they stop breathing for a longer period while they swallow (deglutition apnea). The less frequent sucking with weak pressure in infants with severe BPD resulted in less swallowing when compared with infants without BPD or with mild to moderate BPD. The weak sucking effort could result in avoiding longer deglutition apnea and may, therefore, be advantageous in maintaining breathing.
The other reason for (or factor in) disorganized feeding is neurologic impairment. Poor feeding abilities and pattern of suction/expression pressure are predictors of neurologic development.14 Gewolb et al10 found that a delay in the attainment of stable suckle and swallow rhythms in preterm infants, especially after 35weeks' PMA, may predict subsequent feeding and neurologic problems. We do not know the long-term neurologic outcome of these infants with BPD; at the time of the study, they had no neurologic abnormality. They are currently >6 months' PMA, and their development is concurrent with that for their corrected age. Therefore, the poor coordination observed in this study results mainly from their respiratory problems. In terms of maturation of sucking pattern, Lau et al20 found that expression appears first and is then followed by the suction component. The infants in this study had already demonstrated sucking pressure and, thus, had achieved expression/suction coordination at the time of study. Considering that feeding maturation is related to BPD severity, it is of interest to evaluate the relationship between expression/compression and suction longitudinally from earlier PMA.
Because infants with BPD show irregular respiration and longer deglutition apnea, which interfere with the establishment of longer suck–swallow runs,6 it is expected that feeding efficiency will depend on the severity of BPD. The results of this study reveal that even among infants with BPD, the feeding efficiency and number of swallows during a burst significantly differed between infants with mild BPD and those with severe BPD. This could result from the difference in sucking endurance and performance according to the severity of BPD because sucking pressure and frequency in infants with mild to moderate BPD were significantly larger than those in infants with severe.
To improve sucking endurance and performance, jaw and chin support (eg, the Dancer hand position) might be helpful to support the weak intraoral pressure. However, an increase in swallowing frequency and swallowing volume with the application of positive pressure inside the bottle results in a decrease in minute ventilation even in term infants.21 Given this, the rate of flow from the teat should be paced or slowed to improve feeding coordination and efficiency22,23 rather than use artificial teats that provide greater milk flow. The easiest feeding method for these infants is at the breast. Breastfeeding infants demonstrate improved suck–breathe patterns and oxygen saturations.24 Infants with BPD who were breastfed were found to have higher oxygen saturations during feeding than bottle-fed infants.25 In addition, preterm infants demonstrated more frequently interrupted breathing during bottle-feeding compared with during breastfeeding. When infants with BPD are fed with bottles, more frequent breaks, rest periods, and close SpO2/heart-rate monitoring are required. An increase in the supplemental oxygen concentration when feeding may also reduce the risk of desaturations with feeds and may be helpful in minimizing hypoxemia-induced respiratory depression.26,27 In our study, infants with severe BPD were given supplemental oxygen yet demonstrated the lowest oxygen saturation during feeding. The respiratory compromise associated with sucking bursts was evident in the lower oxygen saturations that were recorded for preterm infants with BPD. As such, they needed higher oxygen supplementation during oral feeding.
In our study, infants with severe BPD demonstrated higher PCO2 levels compared with infants without BPD or with mild to moderate BPD. The higher PCO2 level might have disadvantageous effects on sucking endurance/performance. Timm et al28 showed that preterm infants who were fed while breathing a mixture of 40% oxygen and 7% carbon dioxide had decreased suck and swallow frequency compared with a comparison group breathing 40% oxygen. Acute hypercapnia results in decreased sucking and swallowing frequency during oral feeding, but the infants in our study maintained high CO2 levels because of severe BPD. Although we do not know how significantly the chronic hypercapnia shown in our infants resulted in disadvantageous effects on sucking endurance and performance, it is evident that the respiratory demands play an important role in determining the sucking endurance/performance and that the degree of respiratory problems relates to the efficiency of sucking behavior. Craig et al5 noted that breathing becomes less stable in infants with BPD during feeding; they did not specifically assess the impact of BPD on suck rhythms, but did note that 4 of their 6 infants with BPD sucked significantly slower than they breathed during 1 test session.5 Maintaining ventilation is the most important issue during oral feeding in infants with respiratory compromise. Although additional studies are necessary to draw a conclusion, the weak sucking pressure and less frequent swallowing could be advantageous in maintaining respiration. We recommend that health care providers understand that, for infants to obtain a sufficient amount of milk orally, the total feeding time, including rest periods, may be lengthy.
Although we tried to minimize the effects of the pharyngeal catheter and pneumotachograph inserted into the nostrils on respiration by removing the nasogastric tube and inserting a pharyngeal catheter of the same size, the nasal passages remained partly occluded. Because of this nasal passage occlusion, the sucking problem may not be as severe as our data indicates.
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CONCLUSIONS |
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TOPABSTRACTPATIENTS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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The severity of BPD results not only in poor sucking endurance and performance but also in less coordinated feeding. Although more research is required to confirm this, the weak and less frequent sucking and swallowing in infants with severe BPD seems to compensate for their poor coordination of suck–swallow–breathe during feeding.
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ACKNOWLEDGMENTS |
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We thank Noriko Mizuno, RNM, IBCLC, for technical support.
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FOOTNOTES |
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Accepted Mar 14, 2007.
Address correspondence to Katsumi Mizuno, MD, PhD, Showa University of Medicine, Department of Pediatrics, 1-5-8 Hatanodai, Shinagawa-ku, Tokyo 142-8666, Japan. E-mail: katsuorobi{at}aol.com
The authors have indicated they have no financial relationships relevant to this article to disclose.
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