DOI: 10.1542/peds.111.6.1337
2003;111;1337-1342
Pediatrics
Kuhn
Melanie M. Smith, Maureen Durkin, Veronica J. Hinton, David Bellinger and Louise
Initiation of Breastfeeding Among Mothers of Very Low Birth Weight Infants
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Initiation of Breastfeeding Among Mothers of
Very Low Birth Weight Infants
Melanie M. Smith, MNS*§; Maureen Durkin, PhD, DrPH*§¶; Veronica J. Hinton, PhD*‡; David Bellinger, PhD, MSc储; and Louise Kuhn, PhD*§
ABSTRACT. Objective. To examine factors that pre-dict the initiation of expressed milk feedings and the transition to direct breastfeedings among mothers of very low birth weight (VLBW) infants.
Methods. The sample consists of 361 mother-infant pairs enrolled in a follow-up study of children aged 6 to 8 years who were born weighing <1501 g in 1 of 5
hospitals between 1991–1993. Chart review at birth pro-vided data on neonatal characteristics and demographic factors at delivery were obtained by postpartum maternal interview. Information regarding infant feeding prac-tices was obtained at follow-up.
Results. In this study, 60% of mothers initiated ex-pressed milk feedings for their VLBW infants. However, the duration of these feedings was brief with 52% of infants receiving 1 to 3 months or less of human milk feedings. Greater educational attainment, private insur-ance, and breastfeeding experience were each indepen-dently associated with the decision to provide expressed milk feedings. Only 27% of mothers reported directly breastfeeding their VLBW infants. The transition from expressed milk feedings to direct breastfeedings was positively associated with sociodemographic factors in-cluding maternal age, insurance status, and breastfeed-ing experience as well as the length of hospitalization, an indicator of infant health.
Conclusions. Sociodemographic factors were associ-ated with both the decision to initiate expressed milk feedings and the transition to direct breastfeedings. However, factors relating to infant health only influ-enced the transition to direct breastfeedings. Interven-tion programs need to consider the sociodemographic factors that influence infant feeding decisions as well as specific challenges encountered by mothers of VLBW infants. Pediatrics 2003;111:1337–1342; very low birth weight infant, breastfeeding, infant nutrition.
ABBREVIATIONS. VLBW, very low birth weight; NICU, neonatal intensive care unit.
B
reastfeeding is the optimal method of infant feeding with numerous nutritional and immu-nologic advantages.1,2 National breastfeedinggoals have been established to increase the propor-tion of mothers initiating breastfeeding to at least 75% and to maintain at least 50% of infants breast-feeding at 6 months.3,4In 1997, the American
Acad-emy of Pediatrics extended its recommendation of breastfeeding to include premature infants.5 Very
low birth weight (VLBW) infants represent a vulner-able population at increased risk of neonatal and neurodevelopmental impairments that are far less likely to receive the benefits of breastfeedings com-pared with healthy term infants.6 –9 The low
inci-dence and duration of breastfeeding among this high-risk population is unfortunate as human milk feedings convey advantages specific to the prema-ture or low birth weight infant including more rapid gastric emptying, improved fat absorption, and re-duced risk of necrotizing enterocolitis.10,11
Sociodemographic and attitudinal determinants of breastfeeding initiation and duration among mothers of healthy term infants have been investigated in numerous studies.12–17 Fewer studies have focused
on the challenges faced by mothers of VLBW in-fants.7,18,19 Most VLBW infants cannot be directly
breastfed at birth, requiring mothers to first initiate milk expression; mothers delivering prematurely are more likely to experience delivery complications; and they face significant stress regarding their fant’s health and the procedures of the neonatal in-tensive care unit (NICU).20,21 Potential institutional
barriers include inadequate or contradictory infor-mation regarding the benefits of human milk feed-ings for VLBW infants; lack of consistent advice and support from health care professionals regarding the initiation and maintenance of milk expression and the transition to direct breastfeedings; and difficulty securing appropriate equipment and supplies to ex-press milk.
A greater understanding of the determinants of breastfeeding among mothers of VLBW infants may be achieved by examining the decision-making pro-cess as distinct stages. Mothers of VLBW infants must first decide whether to initiate expressed milk feedings. A second critical juncture occurs with the transition from expressed milk feedings to direct breastfeedings. A final decision relates to the dura-tion of human milk feedings (eg, the decision to continue milk expression or direct breastfeedings).
From the *Gertrude H. Sergievsky Center; ‡Department of Neurology, College of Physicians and Surgeons; §Division of Epidemiology, Joseph L. Mailman School of Public Health, Columbia University, New York, New York;储Harvard Medical School, Boston, Massachusetts; and ¶University of Wisconsin Medical School, Madison, Wisconsin.
Received for publication May 9, 2002; accepted Sep 16, 2002. Reprints not available.
Address correspondence to Louise Kuhn, PhD, Sergievsky Center, PH-19, Box 16, Columbia University, 630 168th St, New York, NY 10032. E-mail: lk24@columbia.edu
Studies of breastfeeding among VLBW infants have recruited small numbers of mothers from a single medical center, limiting the generalizability of the findings.7,18,19,22,23With a large sample of VLBW
fants enrolled in a multicenter study, this study in-vestigates the influence of sociodemographic and neonatal factors on the initiation of expressed milk feedings, the transition to direct breastfeedings, and the duration of human milk feedings. Identification of specific barriers may help focus efforts to help mothers who may be interested in providing human milk feedings for their VLBW infants.
METHODS
We conducted a retrospective analysis of the determinants of human milk feedings among mothers of VLBW infants participat-ing in a follow-up study designed to assess neuropsychological outcomes at age 6 to 8 years. The original cohort, a multicenter study of 1607 infants weighing⬍1501 g born between January 1991 and December 1993 in 1 of 5 hospitals in New York, New Jersey, and Massachusetts, was assembled to investigate the epi-demiology of brain injuries associated with VLBW and has been described in previous articles.24 –26Data collection is ongoing with a target sample size of 796 children. A total of 444 mothers had completed questionnaires by September 2001 and were eligible for inclusion in this analysis. After selection of a single infant for pregnancies that resulted in a multiple birth, 361 mother-infant pairs remained.
At baseline, maternal demographic and delivery information was collected from postpartum maternal interviews. Infant birth and neonatal data were abstracted from obstetric and neonatal charts. At follow-up, information regarding human milk feedings was obtained by parent questionnaires. The majority of question-naires (95%) were completed by the participant’s biological mother. Mothers reported whether their child received expressed milk feedings during hospitalization and whether their child was directly fed from the breast. The duration of human milk feedings was recorded in five categories (⬍1 week, 1– 4 weeks, 1–3 months, 4 – 6 months,⬎6 months) and mothers specified whether they had breastfed other children. Other breastfeeding experience may have included the same birth sibling (in the case of multiple births), subsequent breastfeeding of younger siblings born after the participating child or previous breastfeeding experience of older siblings. Also during the follow-up interview, mothers com-pleted the Peabody Picture Verbal Test as an estimate of verbal intelligence (IQ).27
Group comparisons were conducted withttests for continuous variables and2tests for categorical data. To examine duration of human milk feedings, expressed milk feedings were divided into 2 categories, less than or more than 4 weeks, and direct breast-feedings were dichotomized less than or more than 3 months for the univariate and multivariate analyses. Logistic regression was used to produce univariate odds ratios and 95% confidence inter-vals. Multivariate logistic regression was employed to determine
which factors were independently associated with the decision to provide expressed milk feedings and the transition to direct breastfeedings. Variables that were related to the outcome (P⬍.1) were added in a forward stepwise fashion. The final model re-tained variables that, when excluded, significantly changed the2 statistic with the relevant degrees of freedom.
RESULTS
The majority of mothers of VLBW infants in this cohort initiated human milk feedings. Of the 361 mother-infant pairs, 215 women (60%) provided ex-pressed milk feedings for their VLBW infants (Fig 1). Less than half (43%) of the women who initiated milk expression progressed to direct breastfeedings. Two infants were directly breastfed without first receiving expressed milk feedings and 2 mothers who directly breastfed their infants were uncertain whether ex-pressed milk feedings were given during hospital-ization. A total of 97 mothers (27% of cohort) pro-vided direct breastfeedings for their VLBW infants.
Although more than half of the VLBW infants received human milk, these feedings were brief. Thirty percent of infants received human milk feed-ings for 1 month or less (Table 1). The duration of human milk feedings was markedly shorter among infants who received only expressed milk feedings compared with infants who transitioned to direct breastfeedings. After 4 months postpartum, ex-pressed milk feedings were received by ⬍10% of infants while breastfeedings continued for 72% of infants who progressed to direct breastfeedings. In total, 47 infants (22%) received either expressed milk feedings or direct breastfeedings beyond 6 months. There were 228 women who reported having
chil-Fig 1. Pattern of expressed milk and direct breastfeed-ings among 361 mothers of VLBW infants recruited from 5 hospitals in New York, New Jersey, and Massa-chusetts during 1991–1993.
TABLE 1. Duration of Human Milk Feedings Among 218 Mothers Who Provided Expressed Milk Feedings or Direct Breast-feedings for Their VLBW Infant Recruited From 5 Hospitals in New York, New Jersey, and Massachusetts During 1991–1993
Length
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dren other than the study participant and 60% of these mothers reported breastfeeding at least 1 other child.
Decision to Provide Expressed Milk Feedings
Factors associated with socioeconomic advantage were positively associated with the decision to initi-ate expressed milk feedings (Table 2). Mothers who provided expressed milk feedings for their VLBW infants tended to be older, white, married, nonsmok-ers, high school graduates, and to have higher verbal IQs and private insurance. Other breastfeeding expe-rience was strongly associated with the decision to provide expressed milk feedings. Sixty-three percent of women who breastfed other children provided expressed milk feedings for their VLBW infants com-pared with 22% of women who did not breastfeed other children. Factors relating to delivery or neona-tal health, eg, mode of delivery, gender, multiple birth, birth weight, or gestational age, were not sig-nificantly associated with the decision to provide expressed milk. None of the infant factors were as-sociated with the initiation of milk expression includ-ing gender, birth weight, or gestational age. In the multivariate model, maternal education, other breastfeeding experience, and presence of private insurance were each independently associated with the initiation of expressed milk feedings (Table 2).
Transition to Direct Breastfeedings
Many of the same sociodemographic characteris-tics associated with the decision to provide ex-pressed milk feedings also influenced the transition from expressed milk feedings to direct breastfeed-ings in the univariate analysis (Table 3). Maternal age, education, verbal IQ, marital status, and pres-ence of insurance were also positively associated with direct breastfeedings. Mothers who were non-white, smokers, and lacked other breastfeeding ex-perience were less likely to transition their infants to direct breastfeedings.
Additionally, the transition to direct breastfeed-ings was influenced by the hospital center and the health status of the infant. A lower proportion of mothers delivering at hospital center C initiated ex-pressed milk feedings and significantly fewer infants received direct breastfeedings. Infants who pro-gressed to direct breastfeedings had higher birth weights, more advanced gestational ages and shorter hospital stays. Infants who received direct breast-feedings spent an average of 51 days in the hospital compared with 69 days for infants who received only expressed milk feedings.
In the multivariate model, maternal age, insurance status, breastfeeding experience, and length of hos-pital stay were each independently associated with
TABLE 2. Factors Associated With the Decision to Initiate Expressed Milk Feedings Among 361 Mothers of Very Low Birth Weight Infants Recruited From 5 Hospitals in New York, New Jersey, and Massachusetts During 1991–1993
Characteristic Child Received Expressed Milk Feedings
Odds Ratio (95% Confidence Interval)
No (n⫽130) Yes (n⫽215) Univariate† Final Model‡
Maternal age (y) 29.3⫾5.6 31.4⫾5.4* 1.9 (1.3,2.9)§
Maternal verbal IQ 94.3⫾12.0 99.5⫾16.0* 1.2 (1.1,1.5)㛳
Marital status (% married) 54.8 73.8* 2.4 (1.5,3.8)
Maternal education (%ⱖhigh school) 46.8 72.0* 2.9 (1.8,4.6) 1.8 (1.0,3.4) Ethnicity of mother (%)
White 42.4 56.3* 1.0
Black 29.6 16.5 0.4 (0.2,0.7)
Hispanic 27.3 18.0 0.5 (0.3,0.9)
Other 4.0 9.1 1.1 (0.8,1.3)
Smoking (% smokers) 29.0 18.0* 0.6 (0.3,0.9)
Breastfeeding experience (%)
No other children 21.4 20.3* 3.7 (2.0,7.0) 2.8 (1.4,5.5)
Did not breastfeed other children 56.4 16.4 1.0
Breastfed other children 22.2 63.3 9.4 (5.4,16.6) 7.9 (4.3,14.6)
% With private insurance or health maintenance organization
60.2 79.5* 2.7 (1.6,4.3) 1.9 (1.0,3.7)
Hospital center (%)
A 36.2 42.5 1.0
B 26.8 24.6 0.8 (0.5,1.3)
C 16.5 10.3 0.5 (0.3,1.1)
D 20.5 22.2 0.9 (0.5,1.8)
Birth weight (g) 997.3⫾236.9 1016.2⫾237.4 1.1 (0.9,1.7)
Gestational age (wk) 27.6⫾2.3 27.8⫾2.3 1.1 (0.9,1.3)
Multiple birth (% singleton) 74.0 76.0 1.0 (0.9,1.1)
Gender (% male) 47.7 50.3 1.0 (0.9,1.2)
Mode of delivery (% cesarean section) 38.2 37.0 .99 (.92,1.1)
Information regarding expressed milk feedings was unknown or missing in 16 cases. Values are mean⫾standard deviation for maternal age, verbal IQ, birth weight and gestational age.
*p⬍.05.
† Univariate model provides odds ratio and 95% confidence interval for each characteristic.
‡ Final model included maternal education, breastfeeding experience and insurance status. The odds ratio and 95% confidence interval for each characteristic are adjusted for the other variables in the final model.
the transition to direct breastfeedings. Adjusting for maternal age, insurance status, and breastfeeding experience, each additional week of hospitalization reduced the odds of an infant transitioning to direct breastfeeding by 14%.
Duration of Human Milk Feedings
There were no consistent differences in any of the sociodemographic or neonatal factors between women who discontinued milk expression within 4 weeks compared with women who continued to pro-vide expressed milk feedings beyond the first month. Similarly, no differences were observed between the mother-infant dyads who were breastfeeding for less than or more than 3 months (data not shown). The statistical power to detect differences was limited because of small numbers in each category. Further, the categorization of the original data and the result-ing cut-offs distresult-inguishresult-ing short and long duration for expressed milk feedings and direct breastfeed-ings may obscure differences if present.
DISCUSSION
The majority of mothers of VLBW infants in this cohort initiated human milk feedings. A higher pro-portion of women initiated expressed milk feedings
(60%) in this study compared with the proportion of mothers delivering at a midwestern hospital (47%)18
but comparison of breastfeeding rates across studies is problematic because of variation across geographic location and time. In a 1995 nationwide survey, 60% of mothers reported breastfeeding their term infants and 48% of mothers of LBW infants initiated breast-feeding.6 Women who reside in New England are
more likely to initiate breastfeeding than women from southern states and the highest prevalence of breastfeeding is reported among women from west-ern states.6Studies among VLBW infants are further
complicated by small sample sizes from a single institution that may include programs influencing infant feeding patterns. The VLBW infants in this study were born between 1991–1993, a period when national breastfeeding rates were increasing.6
Sev-eral factors including the Baby Friendly Hospital Initiative, which began in 199128 and efforts to
pro-mote breastfeeding through the Special Supplemen-tal Nutrition Program for Women, Infants, and Chil-dren29 may also increase the rate of breastfeeding
within our study population.
In this study, low maternal education and lack of private insurance were more common among women who did not commence expressed milk
feed-TABLE 3. Factors Associated With the Transition to Direct Breastfeedings Among 215 Mothers Who Initiated Expressed Milk Feedings for Their Very Low Birth Weight Infants Recruited From 5 Hospitals in New York, New Jersey, and Massachusetts During 1991–1993
Characteristic Child Received Odds Ratio
(95% Confidence Interval)
Maternal verbal IQ 96.6⫾15.6 103.4⫾15.9* 1.3 (1.1,1.6)¶
Marital status (% married) 63.3 83.9* 3.1 (1.6,6.1)
Maternal education (%ⱖhigh school) 65.0 81.1* 2.1 (1.1,4.0)
Ethnicity of mother (%)
White 39.2 75.0* 1.0
Black 20.0 10.9 0.4 (0.2,0.7)
Hispanic 29.5 11.1 0.3 (0.1,0.6)
Other 11.3 3.8 0.5 (0.2,0.9)
Smoking (% smokers) 22.5 12.1* 0.5 (0.2,0.9)
Breastfeeding experience (%)
No other children 22.3 20.4* 1.9 (0.7,4.8) 2.0 (0.8,4.9)
Did not breastfeed other children 22.3 8.6 1.0
Breastfed other children 55.4 70.9 2.7 (1.2,6.1) 2.8 (1.3,6.2)
% With private insurance or health maintenance organization
71.7 91.4* 4.1 (1.9,9.1) 3.4 (1.4,8.5)
Hospital center (%)
A 32.2 50.4* 1.0
B 26.4 24.7 0.6 (0.3,1.2)
C 14.0 6.5 0.3 (0.1,0.8)
D 27.3 18.4 0.4 (0.2,0.9)
Multiple birth (% singleton) 72.7 73.2
Birth weight (g) 970.0⫾264 1080.3⫾241* 1.4 (1.1,1.7)
Gestational age (wk) 27.6⫾2.6 28.8⫾2.4* 1.1 (1.0,1.3)
Length of hospital stay (d) 69.1⫾36.3 50.6⫾25.3* 0.87 (.82,.94)# 0.86 (.80,.93)# Values are mean⫾standard deviation for maternal age, verbal IQ, birth weight, gestational age and length of hospital stay. *p⬍.05.
† Excluding 2 women who did not report providing expressed milk feedings before direct breastfeeding and 2 women who did not know whether their infants received expressed milk feedings.
‡ Univariate model provides odds ratio and 95% confidence interval for each characteristic.
§ Final model includes maternal education, breastfeeding experience, insurance status, and length of hospital stay. The odds ratio and 95% confidence interval for each characteristic are adjusted for the other variables in the final model.
㛳Per 10 years maternal age. ¶ Per 10 IQ points. # Per 7 days.
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ings. Maternal age and measures of economic advan-tage such as education, verbal IQ, marital status, and family income have been frequently associated with increased breastfeeding initiation among mothers of term infants.14 These findings suggest that public
health efforts to increase knowledge, feasibility, and social acceptability of breastfeeding, targeting groups with low breastfeeding rates such as women with lower educational and economic backgrounds, may also improve uptake of breastfeeding among mothers of VLBW infants.
Less than half (43%) of the mothers who provided expressed milk feedings went on to directly breast-fed their VLBW infants. Another study reported that 8 (20%) of 39 women who were expressing milk for their VLBW infants transitioned to direct breastfeed-ings and did not observe any differences between these mothers and those who continued to express milk.18The study stipulated that breastfeedings must
provide half of the infant’s total daily feeding for⬎1 month for the transition to be considered successful. In contrast, our study included all women who di-rectly breastfed their VLBW infants regardless of the proportion or duration of breastfeedings. Further, both sociodemographic and neonatal factors influ-enced the transition to direct breastfeedings in this cohort of VLBW infants. Maternal age, private insur-ance, breastfeeding experience, and shorter hospital stays were positively associated with the transition to direct breastfeedings. Duration of hospitalization likely reflects the overall health of the infant and the morbidity encountered during the neonatal course. Inclusion in a multiple birth did not appear to affect either the initiation of expressed milk feedings, the transition to direct breastfeedings, or the duration of human milk feedings. Infants from multiple births in our cohort had higher birth weights, more mature gestational ages and shorter hospital stays as well as sociodemographic advantages that contributed to their unexpectedly high breastfeeding rates which did not differ from singleton births.
In examining the results of the current study, a number of methodologic issues should be consid-ered. Information regarding the initiation and dura-tion of breast milk feedings was reported by mothers 6 to 8 years after the birth of their VLBW infants. Maternal recall of major infant feeding events has been examined after intervals up to 15 years.30 –32
Recall of breastfeeding initiation was in agreement with written records for 85% of mothers interviewed after 14 to 15 years31 but the recall of breastfeeding
duration was less precise with 37% to 79% of moth-ers reporting accurately within 1 month.31,32
Misclas-sification of breastfeeding duration may have con-tributed to this study’s inconclusive results regarding predictors for the duration of expressed milk and direct breastfeedings. Nearly all respon-dents were the biological mothers of the VLBW in-fants and none of them reported that they were did not know whether they directly breastfeed their in-fant. However, 3 biological mothers were uncertain whether their infant received expressed milk feed-ings. Information about the proportion of expressed milk or direct breastfeedings relative to other
feed-ings was not available but a recent study that re-corded daily nutritional intake during hospitaliza-tion did not observe any effect of age at first or full enteral feed or age of first bottle or breastfeed on the proportion of infants whose mothers continued lac-tation beyond 40 weeks.19Further, although the
spe-cific breastfeeding policies and practices at each hos-pital center were not known, the cohort was drawn from 5 different hospitals located in 2 major cities and a suburban site. Altogether, the subjects repre-sented a more diverse population than previously reported on. VLBW infants selected for follow-up were at particular risk for neurodevelopmental dis-abilities and they may have experienced increased morbidity during their neonatal course compared with other VLBW infants. Given that our data indi-cated that infant characteristics did not influence initiation of expressed milk feeding, these factors are most influential with the transition to direct breast-feeding. As survival of extremely premature infants continues to improve, infants at high risk will con-stitute an increasing proportion of VLBW infants.
Mothers need to receive information describing the benefits of human milk for their VLBW infants along with the practical means to help them express breast milk until their child is able to directly breast-feed. It is difficult to sustain sufficient milk volumes for extended periods without direct breast stimula-tion33,34and an electric breast pump that allows for
frequent and simultaneous emptying of both breasts may help maintain long-term milk expression.35To
increase the likelihood of transition to direct breast-feedings, health professionals need to provide sup-port for long-term pumping as well as specific advice regarding the timing and progression to direct breastfeedings. Manipulating the volume of milk in the breast through partial or complete milk expres-sion may permit a VLBW infant to prepare for direct breastfeedings even before sucking and swallowing movements are fully coordinated.36
The decision to breastfeed is part of a broad cul-tural context. The sociodemographic factors identi-fied in this study, eg, maternal education, maternal verbal IQ, and insurance status, represent indirect predictors of breastfeeding behavior. Knowledge of specific factors associated with initiation of ex-pressed milk feedings and the transition to direct breastfeedings may facilitate identification of women who are more favorably inclined to breastfeed as well as women who may benefit from additional encouragement and support.
sup-port and information while their infants remain in the NICU. A women’s breastfeeding experience with her VLBW infants may affect subsequent infant feed-ing decisions. A public health perspective can pro-mote a supportive breastfeeding environment both in the NICU and in the community.
ACKNOWLEDGMENT
This work was supported in part by National Institutes of Health grant NS 36285-01.
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1342 INITIATING BREASTFEEDING AMONG MOTHERS OF VERY LOW BIRTH WEIGHT INFANTS . Provided by Indonesia:AAP Sponsored on July 18, 2010
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DOI: 10.1542/peds.111.6.1337
2003;111;1337-1342
Pediatrics
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Melanie M. Smith, Maureen Durkin, Veronica J. Hinton, David Bellinger and Louise
Initiation of Breastfeeding Among Mothers of Very Low Birth Weight Infants
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