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378 July/August 2007, Volume 61, Number 4 Bottle-Feeding Behaviors in Preterm Infants With and Without Bronchopulmonary Dysplasia KEY WORDS brochopulmonary dysplasia (BPD) feeding behaviors • pediatrics preterm infants F eeding problems are a prominent developmental issue for preterm infants (Lau & Hurst, 1999; Ross & Browne, 2002). An important aspect of nutritive feed- ing in preterm infants is coordination among the processes of suck, swallow, and respiration. Compromise of this coordination can result in suboptimal nutrition and growth. Nutritive sucking is a complex process that allows in-depth examina- tion of the integration of neonatal behavioral organization (Bu’Lock, Woolridge, & Baum, 1990; Conway, 1994). Sucking may be a sensitive indicator of central nervous system integrity, differentiating stressed from nonstressed infants even when standard neurological examinations fail to do so (Martell, Martinez, Gonza- lez, & Diaz Rossello, 1993; Medoff-Cooper, McGrath, & Bilker, 2000). Moreover, sucking rhythms are useful clinically in discriminating infants with a history of perinatal complications but with no abnormal neurological signs and infants with a benign perinatal history (Drillen, 1972). Different types of nutritive sucking have been described using the sucking rhythm as the differentiating criterion (Gewolb, Bosma, Reynolds, & Vice, 2003; Glass & Wolf, 1994; Gryboski, 1969; Medoff-Cooper, Weininger, & Zukowsky, 1989; Meier & Anderson, 1987; Palmer, 1993). Sucking patterns can be labeled as immature, transitional, and mature. The immature sucking pattern (3–5 sucks per burst) has been observed in premature infants as early as 32 weeks and 3 days (Gry- boski, 1969; Meier & Anderson, 1987). The transitional sucking pattern is described as a burst–pause pattern, with typical sucking bursts of 6–10 sucks per burst (Palmer, 1993). The mature sucking pattern is characterized by sucking bursts of 10–30 sucks per burst with only brief pauses between bursts (Medoff- Tsu-Hsin Howe, PhD, OTR, is a Postdoctoral Research Fellow, School of Occupational Therapy, College of Medicine, National Taiwan University, Taiwan. The author was affiliated with Mount Sinai Medical Center when the study was conducted. Ching-Fan Sheu, PhD, is Professor, Institute of Cogni- tive Science, National Cheng Kung University, Taiwan. Ian R. Holzman, MD, is Professor of Pediatrics, Department of Pediatrics, Division of Newborn Medicine, Mount Sinai Medical Center, 1176 Fifth Avenue, Box 1508, Klingenstein Pavilion, 3rd Floor, New York, NY 10029- 6574; [email protected]. OBJECTIVE. This study compared bottle-feeding behaviors in preterm infants with and without bron- chopulmonary dysplasia (BPD) during the initial hospitalization. METHOD. Individual sucking characteristics and feeding transitional rates were compared in 41 preterm infants (22 boys, 19 girls) with BPD and 99 infants (44 boys, 55 girls) without BPD. Observations of the first bottle feeding and observations of the last feeding before discharge were obtained from medical records of all infants retrospectively. RESULTS. On discharge, infants with BPD, unlike those without BPD, continued to have an immature suck- ing pattern and required longer hospital stays to attain full oral feeding ( p < .001). No differences were found between the BPD and non-BPD groups in time needed for feeding and use of oral support. CONCLUSION. These results suggest that feeding transitional rate, rather than sucking pattern, may be a better discharge indicator for infants with BPD. Howe, T.-H., Sheu, C.-F., & Holzman, I. R. (2007). Bottle-feeding behaviors in preterm infants with and without bronchopul- monary dysplasia. American Journal of Occupational Therapy, 61, 378–383. Tsu-Hsin Howe, Ching-Fan Sheu, Ian R. Holzman DownloadedFrom:http://ajot.aota.org/pdfaccess.ashx?url=/data/journals/ajot/930091/on09/02/2018TermsofUse:http://AOTA.org/terms

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378 July/August 2007, Volume 61, Number 4

Bottle-Feeding Behaviors in Preterm Infants With and Without Bronchopulmonary Dysplasia

KEY WORDS• brochopulmonary dysplasia (BPD)• feeding behaviors• pediatrics• preterm infants

Feeding problems are a prominent developmental issue for preterm infants (Lau& Hurst, 1999; Ross & Browne, 2002). An important aspect of nutritive feed-

ing in preterm infants is coordination among the processes of suck, swallow, andrespiration. Compromise of this coordination can result in suboptimal nutritionand growth. Nutritive sucking is a complex process that allows in-depth examina-tion of the integration of neonatal behavioral organization (Bu’Lock, Woolridge,& Baum, 1990; Conway, 1994). Sucking may be a sensitive indicator of centralnervous system integrity, differentiating stressed from nonstressed infants evenwhen standard neurological examinations fail to do so (Martell, Martinez, Gonza-lez, & Diaz Rossello, 1993; Medoff-Cooper, McGrath, & Bilker, 2000). Moreover,sucking rhythms are useful clinically in discriminating infants with a history ofperinatal complications but with no abnormal neurological signs and infants witha benign perinatal history (Drillen, 1972).

Different types of nutritive sucking have been described using the suckingrhythm as the differentiating criterion (Gewolb, Bosma, Reynolds, & Vice, 2003;Glass & Wolf, 1994; Gryboski, 1969; Medoff-Cooper, Weininger, & Zukowsky,1989; Meier & Anderson, 1987; Palmer, 1993). Sucking patterns can be labeled asimmature, transitional, and mature. The immature sucking pattern (3–5 sucks perburst) has been observed in premature infants as early as 32 weeks and 3 days (Gry-boski, 1969; Meier & Anderson, 1987). The transitional sucking pattern isdescribed as a burst–pause pattern, with typical sucking bursts of 6–10 sucks perburst (Palmer, 1993). The mature sucking pattern is characterized by suckingbursts of 10–30 sucks per burst with only brief pauses between bursts (Medoff-

Tsu-Hsin Howe, PhD, OTR, is a Postdoctoral ResearchFellow, School of Occupational Therapy, College ofMedicine, National Taiwan University, Taiwan. The authorwas affiliated with Mount Sinai Medical Center when thestudy was conducted.

Ching-Fan Sheu, PhD, is Professor, Institute of Cogni-tive Science, National Cheng Kung University, Taiwan.

Ian R. Holzman, MD, is Professor of Pediatrics,Department of Pediatrics, Division of Newborn Medicine,Mount Sinai Medical Center, 1176 Fifth Avenue, Box 1508,Klingenstein Pavilion, 3rd Floor, New York, NY 10029-6574; [email protected].

OBJECTIVE. This study compared bottle-feeding behaviors in preterm infants with and without bron-chopulmonary dysplasia (BPD) during the initial hospitalization.

METHOD. Individual sucking characteristics and feeding transitional rates were compared in 41 preterminfants (22 boys, 19 girls) with BPD and 99 infants (44 boys, 55 girls) without BPD. Observations of the firstbottle feeding and observations of the last feeding before discharge were obtained from medical records of allinfants retrospectively.

RESULTS. On discharge, infants with BPD, unlike those without BPD, continued to have an immature suck-ing pattern and required longer hospital stays to attain full oral feeding (p < .001). No differences were foundbetween the BPD and non-BPD groups in time needed for feeding and use of oral support.

CONCLUSION. These results suggest that feeding transitional rate, rather than sucking pattern, may be abetter discharge indicator for infants with BPD.

Howe, T.-H., Sheu, C.-F., & Holzman, I. R. (2007). Bottle-feeding behaviors in preterm infants with and without bronchopul-monary dysplasia. American Journal of Occupational Therapy, 61, 378–383.

Tsu-Hsin Howe, Ching-Fan Sheu, Ian R. Holzman

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Cooper et al., 1989). The mature sucking pattern is usuallyobserved in infants after 40 weeks’ gestational age and hasbeen used as one of the criteria to assess an infant’s oral–motor skills. An infant’s failure to demonstrate maturesucking after a certain age is considered a soft neurologicalsign (Palmer & Heyman, 1999).

Infants with bronchopulmonary dysplasia (BPD) havedifficulty achieving coordinated suckle feeding (Gewolb etal., 2003) and demonstrate irregular breathing patternsduring feeding (Craig, Lee, Freer, & Laing, 1999). Suc-cessful feeding is further compromised by acute oxygendesaturation during feeding (Garg, Kurzner, Bautista, &Keens, 1988; Singer et al., 1992). The goal of the presentstudy was to compare the differences in bottle-feedingbehaviors in infants with and without BPD during the ini-tial hospitalization. We examined the feeding history of asample of preterm infants through medical chart review.We hypothesized that infants with BPD would show lessmature sucking patterns and would require more time andfeeding assistance to finish their feedings compared toinfants without BPD.

MethodsThis retrospective study was conducted at Mount SinaiMedical Center in New York City with the approval of theof the hospital’s institutional review board. We reviewed allmedical charts in the neonatal intensive care unit (NICU)from July 2001 to July 2003. Infants who met all of the fol-lowing criteria were included in this study: Infants (a) wereborn at a gestational age of less than or equal to 34 weeks;(b) were free from any major cardiac, gastrointestinal, orcongenital impairment; (c) had received occupational ther-apy services during their NICU stay; and (d) were fed bybottle with or without breast feeding experience during thehospital stay. Bronchopulmonary dysplasia was defined as anoxygen requirement at more than 28 days of life. Infantswho had a tracheotomy or who were discharged home witha nasogastric tube were excluded from this study.

The data were originally collected for a longitudinalstudy to examine the factors related to bottle feeding inpreterm infants (Howe, 2004). Thirty-four infants with abirthweight greater than 1,500 g who had been excludedfrom the previous data set were included in the present study.

Each infant’s medical chart was reviewed for informa-tion at two time points. The first observation occurredshortly after bottle feeding was initiated (between 1 and 5days) and the second just before discharge (within 5 days).We obtained data from a detailed review of occupationaltherapy progress reports included in the medical records.The variables we examined included sucking patterns, suck-

ing characteristics, transitional rate, oral feeding assistance,and duration of hospital stay, among other factors. Thetransitional rate was calculated by the ratio of feeding intake(ml ) to the feeding duration (min). The volume of milkwas the amount of milk that the infant had consumed viabottle at observed feed. The time was measured as soon asthe bottle was introduced and sucking began. Any inter-ruptions, such as burping, and allowance for breathing dur-ing feeding were included as part of feeding. The time wasrecorded when the infant finished his or her requiredamount or stopped sucking for more than 2 min. Oral feed-ing assistance was defined as any external assistance appliedby a feeder to an infant during bottle feeding to facilitateperformance. In this study, oral feeding assistance includedoral support and external pacing.

The Neonatal Oral Motor Assessment Scale (NOMAS;see Figure 1) was included as part of the feeding assessmentin the occupational therapy progress report (Braun &Palmer, 1986; Palmer, Crawley, & Blanco 1993), and writ-ten permission was obtain from Ms. Palmer.

In line with hospital protocol, an occupational thera-pist routinely monitored each infant when the infant wasmedically stable and when his or her feeding deliverymethod had progressed from continuous feeding (thedefault method for infants weighing less than 1,250 g) tobolus feeding. A single occupational therapist (the firstauthor) implemented the feeding assessment and interven-tion for all infants in the NICU.

ResultsWe reviewed the records of 140 premature infants (66 boys,74 girls), 41 in the BPD group and 99 in the non-BPDgroup. Characteristics of infants in the BPD and non-BPDcohorts are given in Table 1. Infants in the BPD grouptended to be of lower birthweight and lower gestational agethan those in the non-BPD group. Both groups started oralfeeding at a similar age and weight. Consequently, the post-natal age (days of life) at time of first observation was sig-nificantly higher in the group with BPD (p < .001).

We compared the infants’ feeding behaviors on dis-charge using records of the last feeding observation. Table 2allows comparison of the BPD and non-BPD group. Ondischarge, the majority of infants in both groups did notdemonstrate a mature sucking pattern (85% in the non-BPD group and 93% in the BPD group). Seventy percentof infants in the non-BPD group and 54% of infants in theBPD group demonstrated the transitional sucking pattern.When we examined developmental sucking patterns, wefound that infants with BPD who demonstrated the transi-tional sucking pattern on discharge were significantly older

The American Journal of Occupational Therapy 379

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than those in the non-BPD group (37.5 weeks vs. 35.6weeks; p < .001). In addition, infants with BPD achievedfull oral feeding significantly later than their counterparts(38.5 weeks vs. 35.5 weeks). No significant differences werefound in the areas of feeding assistance and practice.

Discussion

In our study, most infants in both groups did not demon-strate a mature sucking pattern (i.e., continuous suckingbursts) when they were discharged from the NICU. This

380 July/August 2007, Volume 61, Number 4

Figure 1. Neonatal Oral Motor Assessment Scale.

Source: Neonatal Oral-Motor Assessment Scale, by Marjorie Meyer Palmer, 1990, San Juan Bautista, CA: Author.Copyright © 1990 by Marjorie Meyer Palmer. Reprinted with permission.

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finding is not surprising, because neither group had reacheda gestational age of 40 weeks when discharged from the hos-pital. With further examination, we found that infants withBPD demonstrated a lower sucking rate and showed slowerprogression through sucking patterns. These results confirmother findings that infants with BPD do not follow pre-dicted maturational patterns of suck–swallow rhythmicintegration (Gewolb et al., 2003; Gewolb, Bosma, Taciak,

& Vice, 2001). Researchers have used sucking rhythms asan indicator of maturation in neurobehaviors in preterminfants (e.g., Medoff-Cooper et al., 2000). In our study,infants with BPD failed to demonstrate age-appropriatesucking patterns, indicating signs of immaturity comparedwith their counterparts.

Oral support was reported to be effective in improvingpreterm infants’ sucking efficiency (Einarsson-Backes,

The American Journal of Occupational Therapy 381

Table 1. Infant Characteristics (N = 140)Characteristic Infants Without BPD Infants With BPD p

Gestational age (weeks) < .001Mean (SD) 30.3 (2.0) 27.1 (1.8)Range 25.0–34.0 24.0–30.6

Birthweight (g) < .001Mean (SD) 1,308.0 (304.6) 866.5 (283.9)Range 610–2,570 471–1,490

Gender 44 boys, 55 girls 22 boys, 19 girlsGestational age at first observation (weeks) < .050

Mean (SD) 33.4 (1.4) 34.4 (2.1)Range 29.4–37.6 30.7–40.1

Gestational age at last observation (weeks) < .001Mean (SD) 35.5 (1.7) 38.5 (2.8)Range 31.7–43.3 33.7–46.1

Weight at first observation (g) nsMean (SD) 1,577.0 (272.6) 1,554.0 (266.4)Range 1,180.0–2,320.0 1,235.0–2,330.0

Weight at last observation (g) < .001Mean (SD) 2,046.1 (325.7) 2,367.6 (469.5)Range 1,360.0–2,970.0 1,340.0–3,930.0

Postnatal age at first observation (days) < .001Mean (SD) 18.6 (11.3) 51.0 (19.0)Range 3–62 10–87

Postnatal age at last observation (days) < .001Mean (SD) 33.6 (16.6) 79.4 (23.3)Range 5–81 32–120

Note. BPD = bronchopulmonary dysplasia; ns = not significant.

Table 2. Infant Feeding Characteristics by Sucking Pattern on Discharge From Hospital (at Last Observation) Infants Without BPD Infants With BPD

Characteristic (n = 99) (n = 41) p

Immature sucking patterna

Postmenstrual age (SD) 35.6(2.8) 39.9 (3.4) < .001Transitional rate (ml/min) 2.6 2.7 ns Number of infants needing oral support/total infants

in immature sucking pattern 10/15 (67%) 9/16 (56%) ns

Transitional sucking patternb

Postmenstrual age (SD) 35.6 (1.51) 37.5(1.40) < .001Transitional rate (ml/min) 3.4 3.5 ns Number of infants needing oral support/total infants

in transitional sucking pattern 23/69 (33%) 5/22 (23%) ns

Mature sucking patternc

Postmenstrual age (SD) 35.3 (1.3) 38.1 (3.9) nsTransitional rate (ml/min) 4.5 7.6 nsNumber of infants needing oral support/total infants

in mature sucking pattern 2/15 (13%) 0/3 (0%) ns

Note. BPD = bronchopulmonary dysplasia; ns = not significant. Postmenstrual age = gestational age + postnatal days of life/7.a3–5 sucks in each sucking burst; n = 31.b6–10 sucks in each sucking burst; n = 91.c >10 sucks in each sucking burst; n = 18.

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Deitz, Price, Glass, & Hays, 1994). In our study, we foundthat techniques used to assist oral feeding, such as oral sup-port and external pacing, were similar for healthy prema-ture infants and infants with BPD. Infants with BPD didnot require more feeding assistance, as we had originallyhypothesized. Thus, prematurity, rather than chronic lungproblems, appeared to be the reason for needing oral sup-port during feeding, as BPD was not a contributing factor.

We compared characteristics of feeding behaviors listedin the NOMAS between groups. None of the behavioralindicators (e.g., arrhythmic tongue or jaw movements) werefound to be significantly different between BPD and non-BPD groups. This finding does not support Perlman andVolpe’s (1989) observations of abnormal tongue and jawmovements in 10 preterm infants with BPD during feed-ing. Further research should map out feeding behaviors as afunction of age.

This study had two limitations. First, the data collec-tion was limited to the time of infants’ initial hospitaliza-tion; therefore, examination of feeding performance afterdischarge was not possible. Future research should comparethe feeding performance of BPD and non-BPD groups inlong-term follow-up. Second, infants who had severe feed-ing problems were not included in this study. The infants inour sample thus may not be representative of all prematureinfants, especially those who need a nasogastric tube fornutrient supplement at the time of discharge.

As a general policy at our institution, to be consideredas functional feeders and to be discharged home with fulloral feeding, infants are required to finish all feedingswithin 30 min without any cardiorespiratory compromises.We found that infants with BPD required a longer hospitalstay to attain full oral feeding.

On the basis of these data, we suggest that a clinicaldecision to discharge infants with BPD home without alter-native feeding intervention (i.e., nasogastric tube place-ment) should rely more on feeding transitional rate thansucking pattern. The ability to consume the requiredamount of milk within a reasonable time is a stronger indi-cator of function.

Findings from this research are important to cliniciansworking in NICUs. The development of effective strategiesto ensure an infant’s ability to consume the requiredamount of milk within a reasonable time is critical in thefacilitation of discharge plans. This goal is commonlyachieved in two ways in clinical practice. First, an infant’sfeeding time can be shortened by decreasing the requiredamount of milk per intake. For example, the caloric den-sity for breast milk and infant formulas, unless specificallynoted, is 20 kcal/30 ml. A total requirement of 120kcal/kg/day for a 2,000 g infant (240 kcal) can be reached

with 60 ml of formula per feeding (40 kcal) every 4 hr (6feedings). By increasing the caloric density to 24 kcal/30ml, the infant needs to take only 50 ml per feeding to reachthe same caloric requirement (240 kcal/6 feedings/24 kcal× 30 ml). The amount of milk per intake can be manipu-lated accordingly. However, therapists must work closelywith medical teams, including dieticians, to maintain aninfant’s caloric intake and fluid requirements whiledecreasing the amount of milk per feeding. Each infantshould be assessed individually to achieve a balancebetween volume intake per feeding and feeding time needsbefore discharge.

Second, a nipple with a higher flow can shorten aninfant’s feeding time. Increased free flow of formulathrough the nipple can increase ingestion rate, and usingnipples designed for premature infants may encourage vol-ume intake (Medoff-Cooper et al., 1989; Schrank, Al-Sayed, Beahm, & Thach, 1998). However, therapists needto exercise caution with nipple selection. An infant’s abilityto handle milk flow, behavior state during feeding, andindividual feeding style must be considered during theselection process (Lau & Schanler, 2000).

ConclusionIn the NICU setting, occupational therapists play animportant role in supporting the normal development offeeding and providing parent education (Caretto, Topolski,Linkous, Lowman, & Murphy, 2000; Matthews, 1994).Therapists should not only assess an infant’s sucking abili-ties but also provide feedback on feeding strategies to pri-mary caregivers, including medical staff and parents. Treat-ment sessions should involve parent and caregivereducation and hands-on practice. Therapists who choose touse milk transitional rate as a functional guide in choosingfeeding strategies should educate parents about this conceptto ensure postdischarge follow-through.

To formulate a functional treatment plan, occupationaltherapists directing the care team in decision making aboutappropriate and effective feeding strategies for each infantshould incorporate feeding-related input from all teammembers. They also should promote primary caregivers’understanding of the reasons for specific feeding strategies.In so doing, they will contribute to greater compliance withstrategies after discharge and thus ensure a safer and moresuccessful discharge plan. ▲

AcknowledgmentsWe thank Tara Wilhelm Forstrom for her editorialassistance.

382 July/August 2007, Volume 61, Number 4

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