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research-article2015

JHLXXX10.1177/0890334415586406Journal of Human LactationOras et al

Original Research

Breastfeeding Patterns in Preterm Infants Born at 28-33 Gestational Weeks

Journal of Human Lactation 1­–9 © The Author(s) 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0890334415586406 jhl.sagepub.com

Paola Oras, RN, RM, MNSc1, Ylva Thernström Blomqvist, RN, PhD1, Kerstin Hedberg Nyqvist, RN, PhD1, Maria Gradin, RN, PhD2, Christine Rubertsson, RN, RM, PhD1, Lena Hellström-Westas, MD, PhD1, and Eva-Lotta Funkquist, RN, RM, PhD1

Abstract Background: Studies of breastfeeding patterns during preterm infants’ first year of life are scarce but are important for providing breastfeeding mothers of preterm infants with optimal support. Objective: This study aimed to describe breastfeeding patterns in preterm infants up to 1 year of corrected age. Methods: As part of a larger study on kangaroo mother care in Sweden, a 24-hour breastfeeding diary was sent home after discharge from hospital, and at 2, 6, and 12 months of the infant’s corrected age. Eighty-three mothers responded to the follow-up questionnaires, and the number of respondents to the breastfeeding diary was 48 at discharge, 43 at 2 months, 22 at 6 months, and 8 at 12 months. Infants were born at a median (range) gestational age of 32 (28-33) weeks. Breastfeeding patterns were analyzed according to durations, frequencies per 24 hours, and intervals between sessions. Results: In exclusively breastfed infants, the median (range) breastfeeding session frequency was 14 (8-26) times per 24 hours including 4 (1-9) times per night after discharge (n = 24) and 10 (6-25) times per 24 hours including 2 (0-5) times per night at 2 months (n = 23). In partially breastfed infants, the median (range) frequency was 5 (1-14) times per 24 hours including 2 (0-4) times per night at 6 months (n = 20) and 5.5 (1-12) times per 24 hours including 2 (0-3) times per night at 12 months (n = 8). Conclusion: Mothers reported large variations in breastfeeding patterns, with higher median breastfeeding session frequencies than previously described in term infants in affluent settings. Keywords breastfeeding, feeding behaviour, kangaroo mother care, lactation, newborn

Well Established Previous studies in term infants have reported low breastfeeding session frequencies in affluent societies and high frequencies in horticultural and hunter-gatherer societies.

Newly Expressed The mothers of preterm infants in our study reported higher median frequencies than described in term infants in affluent settings, probably as a reflection of all infants’ innate biological needs.

Background Breastfeeding patterns are sparsely studied both in term and preterm infants, and existing studies in different settings have presented conflicting results. The different aspects of these patterns—durations, frequencies, and intervals of suckling—have large individual variations and emerge from a

bio-cultural context.1 In the early 20th century, the standard care in Europe and North America included separation between mother and newborn infant as well as regulation of breastfeeding to occur at 4-hour intervals. This laid the groundwork for later routines and practices in neonatal care and has influenced ideas about normal breastfeeding frequencies.2 From a biological point of view, humans belong to a group of mammals with frequent suckling patterns.3 A few studies of term infants in affluent settings have described median breastfeeding frequencies of 6 to 11 times per 24 1

Department of Women’s and Children’s Health, Uppsala University, Uppsala, Sweden 2 Department of Paediatrics, Faculty of Medicine and Health, Örebro University, Örebro, Sweden Date submitted: December 11, 2014; Date accepted: April 20, 2015. Corresponding Author: Paola Oras, RN, RM, MNSc, Department of Women’s and Children’s Health, Uppsala University, SE-751 85 Uppsala, Sweden. Email: [email protected]

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hours in exclusively breastfed infants up to 6 months.4-9 In contrast, term infants in hunter-gatherer and horticultural societies have demonstrated breastfeeding frequencies of several sessions per hour.10-12 Preterm mother–infant dyads face a more complicated breastfeeding initiation process because of barriers such as mother–infant separation and infant morbidity.13 In addition, a common opinion holds that an immature sucking pattern is a barrier to establishment of breastfeeding in these infants.14 However, preterm infants have the capacity to breastfeed at a lower postmenstrual age than commonly stated.15,16 In hospital, the preterm infant–mother dyad is exposed to feeding routines other than on-demand breastfeeding, before the infant is able to breastfeed exclusively.17 In most neonatal intensive care units (NICUs), feeding schedules with fixed volumes and hours are the norm, and common intervals are every 4, 3, or 2 hours, implying a feeding frequency of 6 to 12 times per 24 hours.18,19 In some settings, continuous enteral feeding through nasogastric tube is used initially to increase the tolerated feeding volumes and improve weight gain. The infant is then gradually weaned off this method between 32 and 34 weeks postmenstrual age.20 To provide warmth for the preterm infant, parents and infants are commonly separated by the use of an incubator. Kangaroo mother care (KMC) is a model of care for reducing the separation between preterm infants and their parents and for preventing infant hypothermia. It is defined as early, continuous, and prolonged skin-to-skin contact between the infant and parent or other relative. The method also recommends exclusive breastfeeding/breast milk feeding as the ideal nutrition, and early discharge from hospital with adequate follow-up. Kangaroo mother care has shown positive effects on breastfeeding in both low birth weight infants (< 2500 g) and preterm infants.21 Positive effects of KMC have mostly been observed in low-resource settings but some advantages are also reported from affluent settings.22 Descriptions of breastfeeding patterns among preterm infants after discharge from hospital are lacking. In this study, preterm infants were treated at 2 Swedish NICUs with different practices of KMC, and the objective was to describe breastfeeding patterns in these infants after discharge from hospital up to 1 year of corrected age.

Methods This descriptive study was part of a longitudinal study that aimed to investigate different aspects of KMC in neonatal intensive care. Previous reports from this study have been published on parents’ practice of this model of care23 and mothers’ and fathers’ experience of the method,24,25 including support of feeding and breastfeeding.26 The sample consisted of parents with preterm infants who were born and cared for at the NICUs at 2 tertiary level regional centers in Sweden (NICU A and NICU B) between October 1, 2008 and September 30, 2010. Inclusion criteria were infant born

as a singleton at 280/7 to 336/7 gestational weeksdays, absence of any life-threatening illness, infant cared for at the same NICU from birth to discharge, and parents with a full command of the Swedish language. Of the 244 infants born at 280/7 to 336/7 gestational weeksdays, 123 met the inclusion criteria; 19 of these 123 infants were excluded because the parents declined participation or were unable to complete questionnaires, the gestational age was incorrect, or the parents were approached too late, and in one case because the infant died. This left a total of 104 infants who were eligible and whose parents agreed to participate in the study. Background information on the infants was collected through their medical records and the Swedish Neonatal Quality Register. Background information on both parents was collected at the hospital through a predischarge questionnaire. Follow-up questionnaires, including a 24-hour breastfeeding diary, were sent to the parents’ home address after discharge and at the infant’s corrected age of 2, 6, and 12 months. A reminder to respond, by phone, text message, or e-mail, was given to parents if they had not returned the questionnaire within 2 weeks, and if they still did not return it after the reminder, a new questionnaire was sent home. Twenty-one mothers were lost to follow-up and never participated in the follow-up questionnaires. This left 83 mothers who responded to the follow-up questionnaires in the main study. Mothers were asked to record all breastfeeding sessions during a 24-hour period in a manually completed breastfeeding diary, detailed down to the minute. Some mothers did not breastfeed and others ceased to breastfeed as the study proceeded. A total of 54 mothers filled in the breastfeeding diary at least once: 48 after discharge, 43 at 2 months (of which 3 had not responded previously), 22 at 6 months (of which 2 had not responded previously), and 8 at 12 months (of which 1 had not responded previously). The response rate after discharge was 75%, at 2 months 73%, at 6 months 67%, and at 12 months 71% (Figure 1). In Sweden, parents are entitled to a total of 480 days of paid parental leave. If the child is admitted to hospital, both parents are entitled to additional paid temporary parental leave during the child’s whole hospital stay. In NICU A, at least 1 parent could stay with the infant 24 hours, 7 days a week during the whole hospital stay, with access to a parent bed in an intensivecare, open bay nursery or in a parent room. In NICU B, visiting hours were limited to days and evenings, and parents had access to a parent room only for staying overnight for a few days before the infant was discharged from the hospital. Before inclusion in the study, parents were informed that participation was voluntary, that they were allowed to withdraw at any time without giving any explanation, and that declining to participate would not have any negative effect on their infant’s treatment or care. Oral and written informed consent was obtained before inclusion. The data were coded to ensure confidentiality, and the code lists with the infants’ names were kept in a locked office where only authorized persons could access them. The study was approved by the

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Oras et al Figure 1.  Flowchart of the Responses from the Participating Mothers, at Different Times of the Infant’s Corrected Age. Participants in the KMC study. Inclusion criteria: Born October 1, 2008September 30, 2010; GA 28-33 w; no serious illness; Swedish speaking. (N=104 included; N=83 participated in the follow-up) Not breastfeeding (N=14) Not responding (N=21) Breastfeeding diary after discharge (N=48)

Breastfeeding diary 2 months CA (N=43)

Not breastfeeding (N=18) Not responding (N=22)

Not breastfeeding (N=34) Not responding (N=27) Breastfeeding diary 6 months CA (N=22)

Breastfeeding diary 12 months CA (N=8)

Not breastfeeding (N=51) Not responding (N=24)

Table 1.  Characteristics of the Infants Whose Mothers Responded to the Breastfeeding Diary. Characteristic Gestational age, median (range), wkd Birth weight, median (range), g Girls, No. (%) Cesarean section, No. (%) Length of hospital stay, median (range), d PMA at discharge, median (range), wkd Weight at discharge, median (range), g

No.

Respondents

54

324/7 (283/7-336/7)

54 54 54 54

1970 (740-2920) 20 (37) 31 (57) 23.5 (13-71)

54

36 (343/7-402/7)

54

2320 (1525-3080)

Abbreviation: PMA, postmenstrual age.

Results

Abbreviation: CA, corrected age.

Regional Ethical Review Board at Uppsala University, Sweden (ref: 2006/313/1).

Definitions The World Health Organization defines exclusive breastfeeding as the infant being given only breast milk with the supplement of vitamins and/or medications (including fortification of breast milk) if needed, and partial breastfeeding as the infant being given breast milk and formula and/or complementary foods.27 We chose to limit the definition of exclusive breastfeeding to infants taking all breast milk exclusively at the breast, as our focus was on the infants’ suckling pattern, not the type of milk they received. Vitzthum’s28 definition of a breastfeeding session was used in this study. To be counted, a breastfeeding session must last for at least 1 minute and be separated from the next session by an interval of at least 1 minute. A breastfeeding episode was defined as lasting for less than a minute. Two or more breastfeeding episodes separated by less than 1 minute were also defined as 1 breastfeeding session. Daytime was defined as the period between 06:00 am and 9:59 pm (ie, 16 hours), and night was defined as the period between 10:00 pm and 5:59 am (ie, 8 hours).

The infants were born at a gestational age ranging between 28 and 33 weeks, and the majority were boys. The duration of their hospital stay ranged from approximately 2 to 10 weeks (Table 1). The only difference found between infants of respondents and infants of nonrespondents was a longer duration of hospital stay in the latter group (P = .02). The 54 participating mothers had a median (range) age of 32 (22-40) years. A majority had a university degree (70%) and were born in Sweden (81%). Of the 40% who were multipara, all had previous breastfeeding experience.

Breastfeeding Session Frequencies after Discharge After discharge, the median (range) frequency of breastfeeding sessions of the 24 exclusively breastfed infants was 14 (8-26) times per 24 hours including 4 (1-9) times per night. The median frequency of the 16 infants who received breast milk only, by tube, cup, or bottle in addition to breastfeeding, reported a median frequency of 12.5 (6-28) including 4 (2-10) times per night. The median frequency of the 8 infants who were partially breastfed was 8.5 (1-15) times per 24 hours including 2.5 (0-5) times per night (Figure 2).

Breastfeeding Session Frequencies at 2 Months

Statistical Analyses Data from the breastfeeding diaries were quantified manually, counting the number of sessions, the length in minutes of each session, and the length in minutes of the intervals between sessions for each respondent. Next, the data were analyzed using version 20 of the Statistical Package for the Social Sciences (SPSS). Data are given as median (range). Spearman’s rho was used in the correlation analyses, and a P value < .05 was considered statistically significant.

At 2 months of corrected age, the median frequency of the 23 exclusively breastfed infants was 10 (6-25) times per 24 hours including 2 (0-5) times per night, and 21 of 23 were breastfed at night (1-5 times). The median frequency of the 5 infants who received breast milk only, by tube, cup, or bottle in addition to breastfeeding, was 9 (7-14) times per 24 hours including 2 (2-5) times per night. The median frequency of the 15 partially breastfed infants was 6 (1-12) times per 24 hours including 1 (0-3) time per night (Figure 3).

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Figure 2.  Breastfeeding Frequencies after Discharge; Infants Receiving Breast Milk Exclusively by Breastfeeding (Left Panel), Infants Receiving Breast Milk Exclusively by Tube, Cup, or Bottle in Addition to Breastfeeding (Middle Panel), and Infants Being Partially Breastfed (Right Panel).

Frequencies measured in number of breastfeeding sessions.

Figure 3.  Breastfeeding Frequencies at 2 Months of Corrected Age; Infants Receiving Breast Milk Exclusively by Breastfeeding (Left Panel), Infants Receiving Breast Milk Exclusively by Tube, Cup, or Bottle in Addition to Breastfeeding (Middle Panel), and Infants Being Partially Breastfed (Right Panel).

Frequencies measured in number of breastfeeding sessions.

Breastfeeding Session Frequencies at 6 and 12 Months At 6 months of corrected age, 2 infants were breastfed exclusively 9 and 14 times per 24 hours, including 2 and 3 times per night, respectively. The other 20 infants were partially breastfed and their median frequency was 5 (1-14) times per 24 hours including 2 (0-4) times per night. At 12 months of corrected age, all breastfed infants (n = 8) were partially breastfed with a median frequency of 5.5 (1-12) times per 24 hours including 2 (0-3) times per night.

Duration of Sessions and Intervals of Exclusively Breastfed Infants Breastfeeding sessions varied considerably in length. In exclusively breastfed infants, the median (range) duration of a breastfeeding session was 13 (5-53) minutes after discharge and 11 (1-28) minutes at 2 months. The 2 infants who were exclusively

breastfed at 6 months had a median duration of 11 and 12 minutes, respectively. The total duration of breastfeeding sessions per 24 hours was 3 hours 20 minutes (1 h 30 min to 7 h 40 min) after discharge, and 2 hours 15 minutes (10 min to 6 h 55 min) at 2 months. The 2 infants who were exclusively breastfed at 6 months had a total duration of 1 hour 50 minutes and 3 hours 10 minutes, respectively. The longest interval between breastfeeding sessions among exclusively breastfed infants was 5 hours 10 minutes after discharge, 9 hours at 2 months, and 3 hours 45 minutes at 6 months. In exclusively breastfed infants after discharge, there was a negative correlation between the number of breastfeeding sessions per 24 hours and the median length of the sessions; the lower the frequency, the longer the sessions (r = -0.462, P = .023). The same correlation was found at 2 months (r = -0.616, P = .002).

Breastfeeding Patterns Two different breastfeeding patterns stood out and were classified as regulated versus irregular. Among mothers

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Oras et al Figure 4.  Examples of Regulated Breastfeeding Patterns in 2 Exclusively Breastfed Infants at the Corrected Ages of 354/7 Weeksdays (Left) and 384/7 Weeksdays (Right).

with a regulated pattern, the majority or all of the sessions commenced at full or half clock hours exactly, and the breastfeeding sessions had a similar duration (Figure 4). In contrast, the irregular pattern reported by a majority of the mothers varied greatly in starting time, duration of sessions, and intervals between sessions (Figure 5). Mothers of 6 out of 48 infants reported a regulated pattern after discharge, 8 of 43 infants at 2 months, and 5 of 22 infants at 6 months. Figure 4 illustrates 2 examples of regulated feeding. The diary to the left was completed by a mother whose infant had been admitted to NICU A, where the routine during the hospital stay was 2-hourly feedings until the onset of exclusive breastfeeding. The diary to the right was completed by a mother whose infant had been admitted to NICU B, where the routine during the hospital stay was a scheduled feeding every 3 hours until the onset of exclusive breastfeeding. Mothers of exclusively breastfed infants who suckled frequently reported irregular patterns with wide variations in number of sessions/hour, duration of sessions, duration of intervals, and distribution between day and night (Figure 5). In Figure 6, the breastfeeding diary to the left illustrates a pattern reported by a mother who spent more than 7 hours breastfeeding per 24 hours, whereas the mother who completed the diary to the right indicated a total of only 10 minutes.

Discussion The main finding was that a majority of the infants were breastfed more frequently than what is commonly described as a “normal breastfeeding frequency” in term infants in affluent settings. Furthermore, large individual variations were found in duration and frequency of breastfeeding sessions, intervals between sessions, and distribution of sessions between day and night, contradicting the idea of the existence of normal breastfeeding frequencies at set ages. The concept of normality in a behavior can be defined either as the phenomenon that is most common in a population or as the phenomenon that is proposed to be more biologically appropriate. Since breastfeeding patterns arise in a bio-cultural context, both biological and cultural perspectives can be used to shed light on the root of some differences in breastfeeding patterns. Breastfeeding patterns in affluent settings need to be put into context by giving a historical explanation. Restriction of physical contact between mother and infant combined with regulated breastfeeding at 4-hour intervals and not during the night became the norm in Europe and North America in the early 20th century. These restrictions aimed to create more disciplined and productive adults by teaching infants to suppress their needs and endure discomfort. Although these ideas are considered obsolete, they still affect care routines and parents’ expectations of infants’

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Figure 5.  Examples of 2 Exclusively Breastfed Infants at the Corrected Ages of 372/7 Weeksdays (Left) and 370/7 Weeksdays (Right), Both with Frequent Breastfeeding Sessions.

Figure 6.  Examples of Long Sucking Sessions (392/7 Weeksdays of Corrected Age) (Left) and Short Sucking Sessions (at 3.5 Months of Corrected Age) (Right).a

a

Both infants were exclusively breastfed.

normal behavior.2 In our study, some mothers reported a regulated feeding pattern, which largely reflected the routines of the hospital to which they had been admitted. However, the actual cause of regulated breastfeeding

patterns remains unclear—whether it was because some mothers had a more regulated feeding style or because some infants got used to regulated feeding and continued to follow a certain pattern.

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Oras et al One idea persisting from the time of regulated breastfeeding includes the notion that breastfed infants should stop feeding at night after a few months, and the classification of night awakenings as sleeping problems.29 In our study, almost all exclusively breastfed infants up to 6 months suckled to some extent during the night. Another Swedish study reported that 98% of infants ages 2 to 26 weeks were breastfed at night (1-5 times),4 and an Australian study reported that 64% of infants ages 4 to 26 weeks were breastfed at night (1-3 times).7 Bed sharing promotes breastfeeding30 and more breastfeeding women than nonbreastfeeding women choose to co-sleep with their infant.31,32 It is likely that a mother who is breastfeeding frequently at night chooses to co-sleep with her infant, which could be the case with mothers in our study, especially since co-sleeping has been found to be a common practice in Sweden.33 Concerns have been raised about the safety of co-sleeping since it often entails bed sharing, which has been associated with increased risk of sudden infant death syndrome.34 However, different conclusions have been drawn about these risks. Carpenter et al35 argued that the dangers of bed sharing apply to all parents and children, even in the absence of risk factors, whereas Fleming et al36 suggested that there is little risk for parents who lack risk factors. Studies from affluent settings have reported a decrease in breastfeeding frequencies and durations as the infant gets older.7 This is in line with the results from our study; breastfeeding frequencies and median sucking duration decreased over time. Conversely, in a study of hunter-gatherers, breastfeeding frequency increased over time and peaked at 18 months.10 A cultural heritage where sparse feeding intervals have become the norm may cause a discrepancy between the behavioral cues the infant gives when wanting to breastfeed and the mother’s interpretation of the infant’s behavior. When expectations do not match reality, some mothers stop breastfeeding earlier than intended.2 Mothers have commonly described their infants’ crying, fussiness, and wakefulness as signs of perceived insufficient milk supply, and this in turn is one of the common reasons for discontinuation of breastfeeding.37 Using a biological perspective, there is a correlation between milk composition and suckling frequency in different mammals. Human milk has rather low contents of fat and protein, which implies that human infants may be adapted to be breastfed up to several times an hour.3 This is consistent with the findings in studies of hunter-gatherer and horticultural societies, where mothers and infants stay in close physical contact and frequent breastfeeding (3 to 4 times per hour) is practiced.10-12 The similarities between the patterns found in many mother–infant pairs in our study and the patterns observed in hunter-gatherer societies support the interpretation of a frequent and irregular pattern as a pattern reflecting innate biological needs in human infants. However, regarding the interpretation of our results with respect to “normality,” the fact that the sample consisted exclusively of preterm

infants may have contributed to the breastfeeding patterns reported by these mothers. We cannot rule out the possibility that at least some of the observed patterns are more typical of infants born prematurely. This indicates a need for similar studies of healthy infants born at term, with mothers practicing a true on-demand breastfeeding. There may be many different reasons that an infant wants to breastfeed. Using attachment theory, breastfeeding patterns can be interpreted within an evolutionary framework. Evolutionary changes take a long time to manifest. Although the living conditions for the majority of humans have drastically changed over the past 10 000 years, and especially in the past few centuries, we are still biologically adapted to a life as nomadic hunters and gatherers. The greatest danger to an infant in such conditions is to be left alone, and therefore, infants have a strong inherent fear of separation from the primary caregiver (usually the mother). Human infants are relatively immature at birth and need constant supervision and a lot of body contact. The attachment theory emphasizes the importance of appropriate and timely parental responses to the child’s needs. Body contact and free access to the breast are seen as parts of a biological safety net that contributes to a secure attachment.38 Thus, frequent breastfeeding is not merely an issue of nutrition and milk content but also a pattern reflecting the infant’s attachment behavior and strategy to seek comfort and security. A standard definition of what constitutes a breastfeeding session is lacking and different definitions have been used in different studies. Quandt5 defined a session as a breastfeeding episode separated from other episodes by at least 30 minutes. Cable and Rothenberger39 defined it as a 10-minute block of time where 1 or more nipple sucks occurred; thus, 30 minutes of nursing was counted as 3 suckling episodes. Hörnell et al4 used the definition of suckling for 2 minutes or longer, with an interval of at least 30 minutes from the previous breastfeed; consequently, suckling for less than 2 minutes was not recorded, even though some studies have reported an average breastfeeding session duration of around 2 to 3 minutes.11,12 In our study, 1 infant who was exclusively breastfed at 2 months never sucked for more than 1 minute at a time, 10 times in 24 hours. This strengthened our choice of definition. Another issue of debate is which method is optimal for studying breastfeeding patterns. Many older studies used observational research methods. In our setting, self-reporting was considered more feasible. A weakness in our study is the reliability of self-reporting, particularly at night, though a pilot study in the same participant group showed a high reliability when comparing parents’ and nurses’ records on time spent skin-to-skin.40 However, whichever method is chosen, the problem with reliability of night recording remains, unless the mother–infant pair is studied by video recording. Another problem in longitudinal studies on breastfeeding is that many mothers cease breastfeeding over time. A limitation in this study was the low breastfeeding prevalence at 12

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months when only 8 mothers filled in the diary. It is difficult to draw any conclusions from those 8 participants.

Conclusion This study is one of the first to describe breastfeeding patterns in infants born preterm. Most infants were breastfed more frequently than previously described in term infants in affluent settings, and almost all of the exclusively breastfed infants were breastfed during the night. Mothers also reported large variations in breastfeeding patterns. This information should be included in breastfeeding counseling to mothers with preterm infants, both to prevent mothers’ anxiety about their infants’ feeding pattern and to prevent a premature discontinuation of breastfeeding. Acknowledgments The authors would like to thank the participating infants and their mothers who devoted time to fill in the breastfeeding diary and other questionnaires. They also want to thank Eva Sjöholm for help with the data collection.

Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, or publication of this article.

Funding The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by grants from the Regional Research Council in the Uppsala-Örebro region, Uppsala County Council, and Uppsala University Funds.

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Breastfeeding Patterns in Preterm Infants Born at 28-33 Gestational Weeks.

Studies of breastfeeding patterns during preterm infants' first year of life are scarce but are important for providing breastfeeding mothers of prete...
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