The innumerable benefits of feeding human milk to preterm infants have been established.1 Making the transition from gavage feeds to direct feeding at the breast is a challenge for preterm infants due to immature or absent coordination of suck-swallow-breathe pattern, hypotonia, lack of arousal, irritability, behavioral disorganization, and poor endurance.2–4 Mothers of premature infants face several challenges in providing essential human milk for their infants, as a consequence of maternal illness, operative delivery, and prenatal therapies.5 Preterm birth causes a sudden and traumatic interruption of pregnancy in addition to infants' health complications. This causes mothers to experience physiological and emotional challenges that may adversely affect the initiation and sustainment of mother's own milk and direct feeding at the breast.6 Research in developing targeted evidence-based interventions that support breastfeeding progression in the neonatal intensive care unit (NICU) is scarce.7
Nonnutritive sucking and oral or perioral stimulation techniques are interventions used to facilitate oral motor feeding skills.8 Nonnutritive sucking may reduce the impact of adverse procedures, and delayed introduction of oral stimulation and oral feeding. It also stimulates critical aspects of oral motor development.9,10 Nonnutritive sucking on a pacifier (dummy) has significant positive effects on transition from gavage to full oral feeding, transition from start of oral feeding to full oral feeding, length of hospital stay, and intestinal transit time during gavage feeding.11,12 Efficient feeding depends on the same neuronal central pattern generators that are activated during nonnutritive sucking.13 Pacifiers are discouraged in many NICUs, as per the World Health Organization guidelines for “Baby-Friendly Hospital Initiative”14 and concerns of interference with exclusive breastfeeding.15,16 Minimizing pacifier use is associated with establishment of early breastfeeding.17 Nonnutritive sucking on the “emptied” breast is an alternate intervention that can be performed at the nutrition source without interfering with nutritional intake. This little studied intervention has been found to promote consequent weight gain18 and may provide a normal sensory experience of feeding, with similar benefits of nonnutritive sucking on a pacifier. The active participation of the mother in the intervention may have an added benefit.
The objectives of this pilot study were (a) to explore the feasibility of initiating nonnutritive sucking at the emptied mother's breast in preterm infants between 31 and 33 weeks of post–menstrual age (PMA), (b) to assess the effects on anthropometric measures, time to transition to direct breastfeeding, and breastfeeding performance, and (c) duration of exclusive breastfeeding at 3 and 6 months of PMA. Anthropometric measures (weight, length, and head circumference) were measured; length of hospital stay was recorded.
What This Study Adds
- Early initiation of nonnutritive sucking at the mother's breast before initiation of nutritive oral feeding is a safe intervention that is easily implemented in the NICU.
- It is effective in facilitating maturation of nonnutritive sucking skills and breastfeeding performance.
This study was a prospective randomized single-blinded control trial. Approval was obtained by the institutional review board, IRB Min No. 9173 dated January 27, 2015. Written informed consent was obtained from the mother by the primary investigator.
The study was undertaken in a tertiary care hospital from January 2015 to April 2015.
Criteria for inclusion were (1) infants of gestational age of 32 weeks or less and who weighed 1250 g or less at birth and (2) mothers who had a working knowledge of English or Tamil for ease of communication and training. The exclusion criteria were (1) infants with major genetic abnormalities or congenital abnormalities of the oral and pharyngeal region and (2) mothers diagnosed with postpartum psychosis or depression. Infants were recruited when physiologically stable (off respiratory support and no desaturations or apnea during nonnutritive sucking on the finger), tolerating gavage feeds, and attained a postnatal weight of at least 1000 g. At recruitment, the participants were randomized by the primary investigator into experimental and control groups using block randomization using serially numbered opaque sealed envelopes.
Infants in the control group received nonnutritive sucking on the finger during gavage feeds, which is the standard of care in our NICU, and may be comparable with nonnutritive sucking on a pacifier. In the experimental group, in addition to standard care, the infant was facilitated to suckle on the mother's emptied breast (emptied by manual expression) for 5 to 10 minutes 3 times a day till nutritive breastfeeding was begun. The intervention was initiated once the mother was comfortable holding the infant with the nurse's assistance. All infants were monitored via neonatal pulse oximetry during the intervention. Apneic episodes or feed intolerance was recorded as per the existing nursing protocol. The frequency and timing of the intervention were recorded by the mother in a chart provided. When the mother had twins or triplets, the “A” twin or triplet was recruited for the study.
Feeding progression was initiated and advanced at the discretion of the attending neonatologist. Infants routinely transition from nasogastric gavage feeds to a “paladai” (a beaked spoon) between 32 and 33 weeks of PMA. Direct breastfeeding was initiated between 34 and 35 weeks of PMA and then progressed while closely monitoring weight gain. The discharge criteria from the NICU were attaining a weight of at least 1800 g and showing weight gain on complete oral feeds. The use of bottles and formula feeding is discouraged. All mothers who took part in the study were discharged on exclusive breastfeeding as per the NICU policy. Information on exclusive breastfeeding was obtained from interview during the follow-up clinic visits at 6 weeks, 3 months, and 6 months.
The sample size was calculated using G Power, using a previous study completed by Narayanan et al.18 Considering the outcome measure of duration of exclusive breastfeeding in months, using “The difference between 2 independent means” with an effect size of 0.875, an alpha error of 5% and power of 80, the required participants in each group were 22. In this study, a convenient sample of 14 mothers was recruited.
The Preterm Infant Breastfeeding Behavior Scale (PIBBS) is a well-validated and reliable scale used in describing the maturational steps in breastfeeding behavior, ranging from most immature to full-term mature behavior and assesses the infant's emerging competence.19 The components of the scale include rooting, how much of breast was in the infant's mouth, latched on and stayed fixed to the nipple, sucking, the longest sucking burst, swallowing, behavioral state, let down reflex, and time taken to complete feeding.20 The first 6 items were scored to obtain a total score, a higher score indicating more mature feeding behavior.
“Stages of Nutritive and Nonnutritive Sucking” is a 5-stage descriptive scale of the development of nutritive sucking in infants characterized by the presence or absence of the suction and expression components of sucking and the rhythmicity and frequency of its sequential appearance. The descriptions of the stages of nonnutritive sucking are as follows: In stage 1a, the sucking pattern consists of arrhythmic expression without suction; in stage 1b, attempts to generate suction are present; in stage 2a, the expression component becomes rhythmic; in stage 2b, the alteration of suction and expression begins to appear; in stage 3a, sucking still consists of rhythmic expression and no suction; in stage 3b, the rhythmicity of suction expression improves with longer sucking bursts; in stage 4, the rhythmic alteration of suction and expression is established; and in stage 5, longer duration of sucking bursts and greater suction amplitude are seen.21 Assessments were completed by observation of nonnutritive skills and through visual and tactile feedback. The movement and coordination of oral motor structures, lip seal, rhythmicity, and force of sucking on the finger were used in the classification of the stages.22 Maturation of the stages correlates with improved oral feeding performance and assists in the assessment of oral feeding readiness.23
Outcome variables such as average weight gain per day, head circumference, length, duration of stay at the hospital, and transition to complete direct breastfeeding were obtained from the hospital records. “Stages of Nutritive and Nonnutritive Sucking” was assessed once a week, beginning 1 to 2 days after recruitment. Neonatal breastfeeding behaviors were assessed using the “PIBBS” at the time of discharge. The outcome assessor, an occupational therapist, was blinded to the group allocation of the infant.
Descriptive statistics and frequency tables were used to characterize mother and infant variables and length of hospital stay and describe breastfeeding milestones (PMA at first breastfeed, time to complete oral feeds, and PMA at discharge). For ease of analysis of “Stages of Nonnutritive Sucking Scale,” stages a and b were merged together into single stage. The difference between the 2 groups for the PIBBS, Nonnutritive sucking Scale, and exclusive breastfeeding were examined using Mann-Whitney U test. Other categorical outcome measures were compared using Fisher exact test. SPSS 16.0 software was used for data analysis in this study.
The final sample analyzed consisted of 9 mother–infant dyads: 5 infants in the control group and 4 infants in the experimental group (Figure 1). There were no significant differences between the groups with regard to gestational age, birth weight, length or head circumference at birth, maternal age, or education (Table 1). In the experimental group, one infant was one of triplets and another infant was one of twins. Two mothers in the experimental group and all mothers in the control group reported adequate lactation. All the mothers continued to at least partially breastfeed their infants at 6 months. None of the mothers had abnormalities of the breasts or nipples.
The mean PMA at which intervention was begun was 33.27 (SD = 1.25). There was no significant difference between the groups in the PMA at first assessment, PMA at first nutritive breastfeeding, days from start of breastfeeding to discharge, PMA at discharge or total length of hospital stay (Table 2). There was no significant difference between the groups with respect to weight gain, length, or head circumference at the interim assessments. During the period of the study, none of the infants in the experimental group had an apneic episode, aspiration during the intervention, or feeding intolerance. There was a significant difference between the groups in stages of nonnutritive sucking, with the experimental group having a more mature pattern of sucking during the second week assessment (P = .04) and showing a trend toward significance in the third-week assessment (P = .05). See both Table 3 and Figure 2.
The longest sucking burst (the maximum number of consecutive sucks), a component of the PIBBS scale, was superior in the experimental group (P = .06). The total score was higher in the experimental group but not statistically significant (Figure 3).
There was no significant difference in rates of exclusive breastfeeding between the groups at 6 weeks, 3 months, and 6 months. Three mothers in the control group and 1 mother in the experimental group were exclusively breastfeeding their infants at 6 months.
This study assessed the feasibility and safety of nonnutritive sucking at the emptied mother's breast in preterm infants between 31 and 33 weeks of PMA and the impact of the intervention on breastfeeding performance and exclusive breastfeeding at 6 months. None of the infants in the experimental group had apneic episodes, aspirations or feeding intolerance during the period of the intervention, which was completed under minimal professional supervision. Nonnutritive sucking at the mother's breast can therefore be deemed safe for this population of preterm infants. Safety concerns in oral feeding of preterm infants include a threat to the balance of oxygenation and ventilation between swallows, decrease in minute ventilation causing shortened inspiration (that threatens balanced oxygen carbon dioxide exchanges), and episodes of deglutition apnea (a respiratory pause in the pharyngeal phase of swallow24).25 Respiratory conditions further delay oral feeding.26 Direct breastfeeding is not typically attempted until 32 weeks of PMA or later although stable preterm infants are found to maintain physiological stability during breastfeeding as early as 27 to 28 week of PMA.27 A study by Gerges et al28 found initiation of bottle-feeding at 30 weeks of PMA safe when used alongside cue-based feeding. This is consistent with findings of Nyqvist,29 who demonstrated safe breastfeeding from 29 weeks of PMA onward.
In this study, the intervention had no effect on duration of exclusive breastfeeding. The number of mothers who exclusively breastfed their infants at 6 months was higher in the control group than in the experimental group. This finding may be explained—50% of infants in the experimental group were of multiple gestations. These mothers also reported difficulties in lactation, which is common in multiple gestations.30 Breastfeeding infants in higher-gestation pregnancies pose additional challenges, with extra demands on the mother of frequent suckling.30 Reported rates of exclusive breastfeeding are lower in twins or triplets compared with singletons.31,32
The duration of direct breastfeeding is associated with providing the first oral feed at the breast and the gestational age at first direct breastfeeding.33 Longer period of exclusive breastfeeding was found in infants who received nonnutritive sucking on the breast compared with a control group.18 Nonnutritive sucking at the breast may be used as an intervention of family-integrated care (a model in which parents provide all but advanced medical care for their infants), which has shown to increase the frequency of exclusive breastfeeding at discharge compared with infants who received standard NICU care.34 The effects of nonnutritive sucking on anthropometric measures and transition to oral feeding, length of hospital stay, and shorter intestinal transit time during gavage feeding found in other studies11,12,35 were not replicated. Both groups in this study received nonnutritive sucking, whereas most studies on nonnutritive sucking had a comparison group that received no intervention.11
Infants in the experimental group had a faster transition to stage 2 and stage 3 of the Nonnutritive Sucking Scale than those in the control group, implying better readiness for oral feeding. This supports the concept that maturation of sucking skills and suck-swallow-breathe coordination may be dependent not only on physiologic maturation but also on learning experiences.18 This is especially relevant since breastfeeding requires more mature feeding skills than bottle-feeding, which may be completed even with an immature suck.25
Breastfeeding behavior scores were higher for the majority of items assessed in the experimental group. Infants exposed to nonnutritive sucking at the breast latched on and stayed fixed to the nipple and actively sucked for a longer time, had significantly longer sucking bursts, spent more time swallowing, and had higher total scores than those in the control group, indicating more mature feeding behavior. Providing positive feeding experiences in the NICU include: providing tastes of mother's milk or formula, perioral and intraoral touch or pressure, nipple- and finger-sucking experiences, adequate skin-to-skin contact, and opportunities at the breast that allow them to nuzzle, lick, and suck without overwhelming them with feeding volume demands.9,36 Multisensory intervention was shown to improve sucking organization in premature infants.37 Kangaroo mother care led to earlier attainment of breastfeeding in the NICU.38 Oral and tactile kinesthetic interventions improved swallow-respiration coordination.39 This study's attempt at providing infants with a multisensory experience along with nonnutritive sucking may have positively facilitated and improved breastfeeding behavior when compared with nonnutritive sucking on the finger alone.
Limitations of the Study
Because of medical complications and/or physiological instability, the mean age at which the intervention was begun was 33.27 weeks of PMA, though the aim was to begin intervention between 31 and 33 weeks. Two of the mothers in the experimental group had multiple gestations, which may have been a confounding factor to exclusive breastfeeding at 3 and 6 months. A larger sample population may have mitigated these limitations. The reasons for discontinuation of exclusive breastfeeding and barriers were not assessed. Breastfeeding experience needs to be examined longitudinally to identify and remediate potential barriers at various time periods.2
The assessment of “Nonnutritive Sucking” was done subjectively by the occupational therapist. In future studies, more objective measures such as the “Nonnutritive Sucking Scoring System” by Neiva et al,40 or the “Quantitative Assessment of Nonnutritive and Nutritive Sucking” by Lau and Kusnierczyk22 can be used. The qualitative aspects of mothers' perception of the intervention were not studied and may be in future studies. This study is a pilot study; the results cannot be generalized without further research.
Breastfeeding in the NICU is challenging, but motivation to exclusively breastfeed is fueled by positive feeding experiences.41 Providing nonnutritive feeding experiences to premature infants without interfering with nutritional intake may advance oral feeding skills and improve breastfeeding behavior. As a measure of family-centered care, this study highlights the benefits of maternal involvement in the attainment of independent feeding skills. It was found safe and easy to implement. Larger studies need to be done to recommend this intervention in clinical practice.
The authors thank each of the mothers and the infants who participated in this study. They also thank all the nursing staff of the neonatology unit for their support and cooperation.
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Keywords:© 2019 by The National Association of Neonatal Nurses
breastfeeding; breastfeeding performance; nonnutritive sucking; premature infant; oral feeding skills