Clinical Pediatrics http://cpj.sagepub.

com/

Postdischarge Feeding Patterns in Early- and Late-Preterm Infants

Sara B. DeMauro, Preeti R. Patel, Barbara Medoff-Cooper, Michael Posencheg and Soraya Abbasi CLIN PEDIATR 2011 50: 957 originally published online 19 August 2011 DOI: 10.1177/0009922811409028 The online version of this article can be found at: http://cpj.sagepub.com/content/50/10/957

Published by:
http://www.sagepublications.com

Additional services and information for Clinical Pediatrics can be found at: Email Alerts: http://cpj.sagepub.com/cgi/alerts Subscriptions: http://cpj.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav Citations: http://cpj.sagepub.com/content/50/10/957.refs.html

>> Version of Record - Sep 26, 2011 OnlineFirst Version of Record - Aug 19, 2011 What is This?

Downloaded from cpj.sagepub.com at Midlands State University on August 13, 2013

Postdischarge Feeding Patterns in Early- and Late-Preterm Infants

Sara B. DeMauro, MD1, Preeti R. Patel, MD1, Barbara Medoff-Cooper, PhD, RN2, Michael Posencheg, MD1, and Soraya Abbasi, MD3

Clinical Pediatrics 50(10) 957962 The Author(s) 2011 Reprints and permission: http://www. sagepub.com/journalsPermissions.nav DOI: 10.1177/0009922811409028 http://cpj.sagepub.com

Abstract Objective. To compare the incidence of postdischarge feeding dysfunction and hospital/subspecialty visits for feeding 6 6 problems during the first year of life in late (34 to 36 weeks) and early-preterm (25 to 33 weeks) infants. Methods. 7 7 In this prospective study, the authors sent questionnaires to parents of early (n = 319) and late (n = 571) preterm infants at 3, 6, and 12 months corrected age. Parents perceptions of infants feeding skills, comfort with feeding, and hospital/subspecialty visits for feeding difficulties were obtained. Results were analyzed with 2 tests and Spearmans correlations. Results. Early preterms had more oromotor dysfunction at 3 (29% vs 17%) and 12 months (7% vs 4%) and more avoidant feeding behavior at 3 months (33% vs 29%). In both groups, oromotor dysfunction and avoidant feeding behavior improved over time. Frequency of poor appetite and hospitalization/subspecialty visits were similar. Conclusion. Pediatricians should screen all preterm infants for feeding dysfunction during the first year. Keywords infant, preterm, late preterm, feeding dysfunction, feeding and eating disorders of childhood

Introduction
In the United States, 9% of all infants are born at 34 to 6 36 weeks gestation, or late preterm.1,2 The short- and 7 long-term complications of late preterm birth are a recent focus of investigation.1 Although it is well documented that extremely preterm infants have feeding problems in infancy and childhood, the incidence of feeding difficulties in late preterm infants is unknown. A strong suck and coordinated swallow begin to develop at 34 weeks.3-5 However, oral feedings are often initiated as early as 28 weeks.6-8 Oral feeding prior to the development of mature, coordinated skills can reinforce abnormal habits. On the other hand, long-term exposure to nasogastric feedings and other invasive stimuli may lead to oral sensitivity and poor feeding skills.9 Both earlyand late-preterm infants are often discharged on full oral feedings but with immature sucking and swallowing skills.10,11 Abnormal feeding behavior can persist for months or years after discharge and may lead to poor growth.12,13 Early growth is integral to long-term neurological and cognitive development.14,15 Therefore, infants at risk for

feeding dysfunction should be identified as early as possible. The rate of abnormal feeding behavior in the late preterm population is unknown. Without this information, pediatricians do not know whether late preterms should have more frequent or intensive follow-up of their feeding behavior and cannot give parents accurate anticipatory guidance about feeding behavior. This study aimed to assess parental perceptions of feeding skills and the relationship between reported feeding problems and the incidence of hospitalization or subspecialty clinic visits for feeding difficulties during 6 the first year of life in late preterm infants (34 to 36 weeks 7
The Childrens Hospital of Philadelphia and University of Pennsylvania, Philadelphia, PA, USA 2 University of Pennsylvania School of Nursing, Philadelphia, PA, USA 3 Pennsylvania Hospital and University of Pennsylvania, Philadelphia, PA, USA Corresponding Author: Sara B. DeMauro, MD, Division of Neonatology, The Childrens Hospital of Philadelphia, 34th and Civic Center Boulevard, 2nd Floor, Main Building, Philadelphia, PA 19104, USA Email: [email protected]
1

Downloaded from cpj.sagepub.com at Midlands State University on August 13, 2013

958 of gestation) as compared with early preterm infants (25 6 weeks of gestation). We hypothesized that when to 33 7 compared with early preterm infants, late preterm infants would have more mature feeding skills, leading to fewer difficulties with feeding and fewer visits to the hospital or subspecialty clinics.
Table 1. Feeding Questionnaire Question How is your babys appetite? Does your baby have any trouble with the following: Sucking? Swallowing? Choking? How long does it take to feed your baby? How often does your baby do the following when given food? Push food away Turn head Close mouth Gag Hold food in mouth Spit Cry Is your baby feeding enough? Are feeding times for you usually: Has your baby been hospitalized due to feeding difficulties? Has your baby been seen by a specialty clinic due to feeding difficulties? How comfortable do you feel feeding your baby?

Clinical Pediatrics 50(10)

Answer Choices Very poor, poor, average, good, very good

Methods
This prospective cohort study was conducted between 2006 and 2010 at Pennsylvania Hospital in Philadelphia, Pennsylvania. Infants of gestational age 25 to 36 weeks and without major congenital or chromosomal anomalies were eligible. Basic demographic information was collected by chart review or from a local database at the time of enrollment. The study was approved by the University of Pennsylvania Institutional Review Board. Informed consent was obtained from each patients parent or legal guardian.

Not at all, occasionally, frequently Not at all, occasionally, frequently Not at all, occasionally, frequently <35 minutes, >35 minutes

Feeding Behavior Questionnaire

Information about feeding behavior was collected at 3, 6, and 12 months corrected age by telephone interviews or mailed questionnaires. The parents were contacted by telephone when infants were eligible for follow-up. If no parent could be reached, weekly follow-up attempts were made, and then the questionnaire was mailed with a stamped return envelope. Attempts were continued until the infant was outside the time frame of eligibility. The infant feeding questionnaire was modified from a survey used by Wright et al12 to evaluate feeding practices in full-term infants (Table 1). Questions were grouped into 5 categories: appetite, oromotor dysfunction, avoidant feeding behavior, hospitalizations or subspecialty visits, and parental discomfort with feeding. Because parental report of appetite is correlated with energy intake and weight gain in term infants, the questionnaire began with an evaluation of the infants appetite.12,16 The infants appetite was rated on a 5-point scale from very poor to very good. Preterm infants have immature suck and swallow reflexes, and problems with sucking and swallowing are correlated with poor weight gain.17 Therefore, we asked 3 questions about problems with sucking, swallowing, and choking, rated on a 3-point scale, and a fourth question about duration of feeding episodes, as in the questionnaire by Wright et al.12 Then, 7 questions, also on a 3 point scale, were used to assess avoidant feeding behavior, which is associated with failure to thrive at both 12 and 24 months.12,18 On a 5-point scale, parents were asked about stress during meal time and comfort while feeding their infant. On a 3-point scale, we asked if they thought their infant was feeding enough.

Rarely, sometimes, often Rarely, sometimes, often Rarely, sometimes, often Rarely, sometimes, often Rarely, sometimes, often Rarely, sometimes, often Rarely, sometimes, often Yes, not always, no Very relaxed, relaxed, average, stressful, very stressful Yes, no Yes, no Always uncomfortable, sometimes uncomfortable, average, sometimes comfortable, always comfortable

Finally, we asked 2 questions about hospitalization or visits to subspecialty clinics for feeding difficulties.

Power and Analysis

Because 74.4% of all preterm infants are born late preterm, we expected to recruit late and early preterms at a ratio of 3:1.2 To detect a one-third difference in feeding difficulties with 90% power and = .05, we planned to recruit 200 early-preterm and 600 late-preterm infants.11 As in the study by Wright et al,12 results on all 5-point scales were right skewed.12 For analysis, these data were re-coded on 3-point scales. For example, appetite was recorded as normal (very good, good, average),

Downloaded from cpj.sagepub.com at Midlands State University on August 13, 2013

DeMauro et al.
6 6 Table 2. Demographic and Outcome Data for Early (25-33 weeks) and Late (34-36 weeks) Preterm Infants 7 7

959

Early Preterm, n = 319 Maternal age in years, mean (SD) Maternal obstetric history, median [IQR] Gravity Parity Maternal race, n (%) Black White Other Cesarean section, n (%) Birth weight in grams, mean (SD) Male, n (%) Admitted to neonatal intensive care unit, n (%) Length of stay in days, median [IQR] Transient tachypnea of the newborn, n (%) Respiratory distress syndrome, n (%) Sepsis, n (%) Necrotizing enterocolitis, n (%) Intraventricular hemorrhage, n (%)
Abbreviations: SD, standard deviation; IQR, interquartile range.

Late Preterm, n = 571 30 (6) 2 [1, 3] 1 [0, 1] 204 (36) 274 (48) 93 (16) 327 (57) 2539 (465) 307 (54) 311 (55) 5 [4, 8] 60 (11) 17 (3) 46 (8) 1 (0.2) 0 (0)

P Value .59 .76 .49 .36 <.001 <.001 .89 <.001 <.001 .94 <.001 .49 <.001 .02

30 (6) 2 [1, 3] 1 [0, 1] 123 (39) 154 (48) 41 (13) 248 (78) 1595 (503) 170 (53) 319 (100) 32 [19, 54] 34 (11) 123 (39) 30 (9) 20 (6) 3 (1)

borderline (poor), and low (very poor). In each of the categories that contained multiple questions, scores were combined for analysis. Summary scores for oromotor dysfunction, avoidant behavior, and parental discomfort were then coded as normal/low (0), borderline/ medium (1), and high (2). Summary scores for hospitalization/subspecialty clinic visits for feeding problems were coded as none or any (yes to either question). We compared categorical variables and frequency counts in the 2 groups with 2 tests. We compared normally and nonnormally distributed continuous data with Students t test and Mann-Whitney tests. Correlations between measures of feeding dysfunction and hospitalization or specialty clinic visits for feeding dysfunction were calculated with Bonferroni-adjusted pairwise Spearman correlations. All significance tests were 2 sided, and P < .05, adjusted where applicable, was considered significant. All analyses were performed with Stata/IC 11 (StataCorp, College Station, TX).

infants enrolled in the study (Table 2). There was no difference in maternal demographics or parenting experience, gender, or race. As expected, the late-preterm infants were less likely to be born by cesarean section, had lower rates of most neonatal morbidities, and stayed in the hospital for fewer days. Late-preterm infants admitted to the neonatal intensive care unit (NICU) were significantly smaller and stayed in the hospital longer than those who went to the term nursery.

Questionnaire Results
A total of 1975 questionnaires were completed. Parents completed 621 questionnaires at 3 months, 659 questionnaires at 6 months, and 695 questionnaires at 12 months. Of the 890 participants for whom at least 1 questionnaire was returned, 404 (45%) completed three, 277 (31%) completed two, and 209 (23%) completed only one. Results of the questionnaires are displayed in Table 3. At 3 months, parents reported more oromotor dysfunction (29% vs 17% borderline or high; P = .004) and more avoidant feeding behavior (33% vs 29% medium or high; P = .04) in early preterm infants. The most commonly reported form of oromotor dysfunction was choking and the most common avoidant feeding behavior was spitting. These differences resolved by 6 months, with improvement in both measures of feeding dysfunction in both groups. At 12 months, parents of early-preterm infants reported higher rates of oromotor dysfunction (7% vs 4% borderline or high; P = .03) and more

Results
Of the 1083 infants eligible for the study, 83 refused or were not approached and 1000 (92.3%) were enrolled. Of those who gave consent, 110 were not included in analysis because of death (2), transfer to another facility (11), or loss to follow-up (97). Thus, 890 infants (89.0%) were included in the analysis. 6 There were 319 early-preterm (25-33 weeks gesta7 6 tion) and 571 late-preterm (34-36 weeks gestation) 7

Downloaded from cpj.sagepub.com at Midlands State University on August 13, 2013

960
Table 3. Preterm Infant Feeding Questionnaire Results 3 Months Appetite Oromotor dysfunction Normal Borderline Low Normal Borderline High Avoidant Low behavior Medium High Maternal Low feeding Medium anxiety High Hospitalization None or specialty Any clinic 6 Months

Clinical Pediatrics 50(10)

12 Months

<34 Weeks, 34-37 Weeks, P <34 Weeks, 34-37 Weeks, P <34 Weeks, 34-37 Weeks, P n = 220 n = 401 Value n = 261 n = 398 Value n = 244 n = 451 Value 96 (44) 96 (44) 28 (13) 158 (72) 41 (19) 21 (10) 146 (66) 58 (26) 16 (7) 135 (61) 83 (38) 2 (1) 183 (83) 37 (17) 207 (52) 143 (36) 51 (13) 331 (83) 52 (13) 18 (4) 285 (71) 104 (26) 12 (3) 274 (68) 122 (30) 5 (1) 352 (88) 49 (12) 134 (51) 96 (37) .12 31 (12) 234 (90) 19 (7) .004 8 (3) 215 (82) 39 (15) .04 7 (3) 185 (71) 74 (28) .18 2 (1) 228 (87) .11 33 (13) 229 (58) 119 (30) 50 (13) 367 (92) 25 (6) 6 (2) 319 (80) 65 (16) 14 (4) 296 (74) 101 (25) 1 (0.2) 349 (88) 49 (12) 139 (57) 71 (29) 34 (14) 227 (93) 14 (6) 3 (1) 209 (86) 28 (11) 7 (3) 154 (63) 90 (37) 0 (0) 203 (83) 41 (17) 245 (54) 143 (32) 63 (14) 434 (96) 17 (4) 0 (0) 395 (88) 45 (10) 11 (2) 329 (73) 120 (27) 2 (0.4) 396 (88) 55 (12) .76 .03 .77 .01 .09

.18

.34

.73

.43 .90

Note: All results are displayed as n (%).

discomfort with feeding their children (37% vs 27% medium or high; P = .01). The only difference between late-preterm infants who were admitted to the NICU and those admitted to the term nursery was that those admitted to the NICU were twice as likely to require hospitalization or specialty care before 3 months (16% vs 8%; P = .009). The rates of oromotor dysfunction and avoidant feeding behavior decreased over time in both groups (linear trend P < .001). All 4 forms of oromotor dysfunction decreased over time in both groups. The decrease in avoidant feeding behavior over time is predominantly explained by significantly decreased rates of spitting, gagging, and crying. Rates of borderline or poor appetite, parental discomfort with feeding, and hospitalization or specialty clinic visits for feeding dysfunction stayed constant over time in both groups (linear trend P > .2).

infants, avoidant feeding behavior at 3 and 6 months was correlated with medical attention for feeding by 12 months (correlation coefficients, 0.24-0.25; P < .05). Parental discomfort with feeding was correlated with nearly all types of feeding dysfunction but was inconsistently correlated with later subspecialty care or hospitalization in both groups (correlation coefficients, 0.11-0.29). None of the questionnaire measures were strong or consistent predictors of medical attention resulting from feeding dysfunction.

Discussion
Contrary to our hypothesis, we found that parents of early- and late-preterm infants reported fairly similar rates and patterns of feeding dysfunction in the first year of life. Both groups reported oromotor dysfunction and avoidant feeding behavior that improved over time. Over the first year of life, about one half of caregivers reported borderline to poor appetite in their infants, and about one third reported discomfort when feeding their infants. These measures of feeding dysfunction were not strongly correlated with later need for hospitalization or subspecialty visits for feeding problems. Multiple studies have explored early feeding behaviors in very preterm infants, but there is little literature about the late-preterm population.5,19,20 One study found that late-preterm infants had more immature feeding

Correlations
We used Spearman correlation coefficients to compare early questionnaire results with later reports of subspecialty visits or hospitalizations to determine if measures of feeding dysfunction could be used to predict later need for medical attention. In early preterm infants, only poor appetite at 3 months was correlated with medical attention for feeding by 12 months (correlation coefficient 0.25, Bonferroni-adjusted P value <.05). In late-preterm

Downloaded from cpj.sagepub.com at Midlands State University on August 13, 2013

DeMauro et al. behaviors at 35 to 36 weeks postmenstrual age than early preterm infants and suggested that increased experience with oral feeding led to more mature skills in the earlypreterm cohort.4 Hawdon et al21 sent questionnaires to parents of infants born at 23 to 41 weeks gestation at 6 and 12 months. Parents reported disorganized feeding including coughing, vomiting, and food refusalin 39% at 6 months and 37% at 12 months. All infants with disorganized feeding were born <30 weeks of gestation. On the other hand, 23% of infants who presented for multidisciplinary feeding evaluation were born late preterm, and 12% were born early preterm.22 This is consistent with our finding that feeding dysfunction was not limited to infants born at younger gestational ages. Escobar demonstrated that 15.8% of preterm infants discharged from the NICU were rehospitalized with feeding difficulties.23 Similarly, 17% of early- and 12% of latepreterm infants in our study required medical attention for feeding problems by 1 year of age. There was no significant difference between rates of hospitalization/ specialty clinic visits for feeding dysfunction in earlyand late-preterm infants at any time point. Parental reports of feeding dysfunction did not predict which infants would eventually require hospitalization or subspecialty care. The current study has several strengths, including the high consent rate, large sample size, duration of follow-up, and low attrition. At least 2 questionnaires were completed by more than 75% of participants. However, our study also has several limitations. There is likely bias in regard to which families agreed to participate in the study and completed the questionnaires. Feeding difficulties were based on parental report, and we do not have information about the type of feeding, duration of nasogastric feedings, or parental mental health. Although a similar questionnaire was predictive of weight gain in term infants, this tool has never before been used or validated in a preterm population.12 Finally, because full-term infants had already been studied by Wright et al12 in 2006, we did not include them as a comparison group.12 Feeding difficulties, particularly oral motor difficulties, persist in infants with extremely low birth weight until at least 6 years of age, causing distress to both the children and their families.13,23 Our study shows that feeding difficulties in the first year of life are nearly as common in latepreterm infants as in early-preterm infants. Parents of infants in both groups may benefit from increased anticipatory guidance about feeding dysfunction prior to hospital discharge. Pediatricians should screen for parental discomfort with infant feeding and discuss adaptation to caring for a premature infant. Finally, pediatricians should take detailed feeding histories to identify signs of feeding dysfunction and know when to refer at-risk patients for feeding or speech therapy. Acknowledgments

961

The authors thank Rosemary Dworanczyk, Toni Mancini, and Emidio Sivieri for their assistance with this research. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. Funding The author(s) received no financial support for the research, authorship, and/or publication of this article. References
1. Ramachandrappa A, Jain L. Health issues of the late preterm infant. Pediatr Clin North Am. 2009;56:565-577; table of contents. 2. Davidoff MJ, Dias T, Damus K, et al. Changes in the gestational age distribution among U.S. singleton births: impact on rates of late preterm birth, 1992 to 2002. Semin Perinatol. 2006;30:8-15. 3. Mizuno K, Ueda A. The maturation and coordination of sucking, swallowing, and respiration in preterm infants. J Pediatr. 2003;142:36-40. 4. Medoff-Cooper B, Bilker W, Kaplan J. Suckling behavior as a function of gestational age: a cross-sectional study. Infant Behav Dev. 2001;24:83-94. 5. Medoff-Cooper B, McGrath JM, Shults J. Feeding patterns of full-term and preterm infants at forty weeks postconceptional age. J Dev Behav Pediatr. 2002;23: 231-236. 6. Dodrill P, Donovan T, Cleghorn G, McMahon S, Davies PS. Attainment of early feeding milestones in preterm neonates. J Perinatol. 2008;28:549-555. 7. Simpson C, Schanler RJ, Lau C. Early introduction of oral feeding in preterm infants. Pediatrics. 2002;110: 517-522. 8. Nyqvist KH. Early attainment of breastfeeding competence in very preterm infants. Acta Paediatr . 2008;97: 776-781. 9. Dodrill P, McMahon S, Ward E, Weir K, Donovan T, Riddle B. Long-term oral sensitivity and feeding skills of low-risk pre-term infants. Early Hum Dev. 2004;76: 23-37. 10. Thoyre SM, Carlson J. Occurrence of oxygen desaturation events during preterm infant bottle feeding near discharge. Early Hum Dev. 2003;72:25-36. 11. Cleaveland K. Feeding challenges in the late preterm infant. Neonatal Netw. 2010;29:37-41. 12. Wright CM, Parkinson KN, Drewett RF. How does maternal and child feeding behavior relate to weight gain and failure

Downloaded from cpj.sagepub.com at Midlands State University on August 13, 2013

962
to thrive? Data from a prospective birth cohort. Pediatrics. 2006;117:1262-1269. 13. Samara M, Johnson S, Lamberts K, Marlow N, Wolke D. Eating problems at age 6 years in a whole population sample of extremely preterm children. Dev Med Child Neurol. 2010;52:e16-e22. 14. Ehrenkranz RA, Dusick AM, Vohr BR, Wright LL, Wrage LA, Poole WK. Growth in the neonatal intensive care unit influences neurodevelopmental and growth outcomes of extremely low birth weight infants. Pediatrics. 2006;117:1253-1261. 15. Kelleher KJ, Casey PH, Bradley RH, et al. Risk factors and outcomes for failure to thrive in low birth weight preterm infants. Pediatrics. 1993;91:941-948. 16. Brown KH, Peerson JM, Lopez de Romana G, de Kanashiro HC, Black RE. Validity and epidemiology of reported poor appetite among Peruvian infants from a lowincome, periurban community. Am J Clin Nutr. 1995;61: 26-32. 17. Wright C, Birks E. Risk factors for failure to thrive: a population-based survey. Child Care Health Dev. 2000; 26: 5-16.

Clinical Pediatrics 50(10)

18. Wilensky DS, Ginsberg G, Altman M, Tulchinsky TH, Ben Yishay F, Auerbach J. A community based study of failure to thrive in Israel. Arch Dis Child. 1996;75:145-148. 19. Lau C, Smith EO, Schanler RJ. Coordination of suckswallow and swallow respiration in preterm infants. Acta Paediatr. 2003;92:721-727. 20. Gewolb IH, Bosma JF, Reynolds EW, Vice FL. Integration of suck and swallow rhythms during feeding in preterm infants with and without bronchopulmonary dysplasia. Dev Med Child Neurol. 2003;45:344-348. Hawdon JM, Beauregard N, Slattery J, Kennedy G. 21. Identification of neonates at risk of developing feeding problems in infancy. Dev Med Child Neurol. 2000;42: 235-239. 22. Rommel N, De Meyer AM, Feenstra L, Veereman-Wauters G. The complexity of feeding problems in 700 infants and young children presenting to a tertiary care institution. J Pediatr Gastroenterol Nutr. 2003;37:75-84. 23. Escobar GJ, Joffe S, Gardner MN, Armstrong MA, Folck BF, Carpenter DM. Rehospitalization in the first two weeks after discharge from the neonatal intensive care unit. Pediatrics. 1999;104:e2.

Downloaded from cpj.sagepub.com at Midlands State University on August 13, 2013