Abstract
Objectives:
We wanted to investigate whether hyperbilirubinemia (significant or physiological) has an effect on breastfeeding, milk intake, infant's wakefulness, and if any, which level of bilirubin affects breastfeeding.
Materials and Methods:
Healthy, term, and breastfed babies with significant hyperbilirubinemia who required phototherapy were included in the study (group 1, n = 71). In the neonatal outpatient clinic, a control group was formed from babies with physiological jaundice (group 2, n = 90). All infants were monitored during breastfeeding and breastfeeding was evaluated with breastfeeding assessment tools (IBFAT and LATCH) and milk intake was assessed by test scale. The same examinations were repeated after phototherapy when normal bilirubin levels were reached.
Results:
Milk intake, Infant Breastfeeding Assessment Tool (IBFAT) (IBFAT total score [IBFATT], IBFAT first item score [IBFAT1], IBFAT sixth item score [IBFAT6]), and LATCH scores were significantly lower in group 1 than the control group (p = 0.001). In group 1, the amount of milk intake, IBFAT and LATCH scores after phototherapy increased significantly compared to prephototherapy values (p = 0.001). Looking at the correlation matrix in the whole study group (groups 1 and 2) there were moderate but very significant negative correlations between bilirubin and milk intake (r = 0.32, p = 0.001), IBFATT (r = 0.47, p = 0.001), IBFAT1 (r = 0.57, p = 0.001), IBFAT6 (r = 0.65, p = 0.001), and LATCH scores (r = 0.49, p = 0.001). In the receiving operating characteristics analysis, the cutoff bilirubin value was found to be 12 mg/dL.
Conclusion:
Hyperbilirubinemia may have a negative effect on breastfeeding and milk intake. It appears that bilirubin levels above 12, including in babies with physiological jaundice, adversely affect breastfeeding.
Introduction
At least two-thirds of newborns develop clinical jaundice in the first week of life. 1 The most common cause of jaundice in the neonatal period is indirect hyperbilirubinemia. 2 Although bilirubin is protective for the newborn with its antioxidant properties, 3 it has also neurotoxic effects when reached high levels. Therefore, the level of bilirubin in the newborn is important and should be closely monitored, especially in the early days. In our hospital, guidelines of the American Academy of Pediatrics (AAP) (2004) are being used in the management of hyperbilirubinemia 4 and values below the limits of phototherapy are accepted as physiological jaundice.
On the other hand, we receive complaints from mothers of babies who have hyperbilirubinemia and require phototherapy and mothers of babies who have physiological jaundice that their babies are very sleepy and are unwilling to suck. Health professionals also often express the same clinical impression. These findings may be an early sign of acute bilirubin encephalopathy in infants with severe hyperbilirubinemia.5–7 Nevertheless, such an effect is not expected in babies with physiological jaundice. Currently, there are very few studies investigating the effect of hyperbilirubinemia on feeding8–10 and in these studies bottle was used for infant feeding.
We did not find any studies investigating the effect of hyperbilirubinemia on breastfeeding. Therefore, in this study, we wanted to investigate whether hyperbilirubinemia (significant or physiological) has an effect on breastfeeding, milk intake, and infant's wakefulness and at which level of bilirubin breastfeeding is affected. To our knowledge, this is the first study on this subject and we believe that it will make an important contribution to the literature.
Materials and Methods
This prospective study was conducted in the third level neonatal intensive care unit and in the neonatal outpatient clinic between January 2018 and April 2019. The local ethics committee approved the research, and informed consent was obtained from the legal caregiver of each child before enrollment. Study groups were determined based on bilirubin level only. Healthy, term, and breastfed babies who were admitted to the intensive care unit to receive phototherapy treatment due to significant hyperbilirubinemia (group 1) and babies who had physiological jaundice in the neonatal outpatient clinic (group 2) were included in the study along with their mothers. The indication for phototherapy was determined according to the AAP guidelines. 4
Initially, all mother's breasts were expressed by an electric pump to evaluate whether they had enough milk volume for each breastfeeding session that will be suitable for baby's postnatal age. The amount of milk volume that infants should take for each feeding session within the 3-hour interval was calculated according to postnatal age and weight (60 mL/kg for the first postnatal day, increased by 10 mL/kg for each day, and reaching 150 mL/kg/day on postnatal day 10 and thereafter).
Mothers who did not have enough milk for each feeding or who had nipple problems (plain, cracked, or inverted nipple) that caused breastfeeding difficulties and infants who had any condition such as congenital abnormality, any infection, anemia, ankyloglossia, central or peripheral nervous system disorders other than jaundice that prevented sucking were excluded from the study. All mothers were informed about the correct breastfeeding techniques, regardless of whether they were educated on this topic or not. Same breastfeeding assistance and instructions were given to mothers of the babies with the significant jaundice group and with the ones in the control group. Milk intake was evaluated with test scale and breastfeeding was evaluated with latch and Infant Breastfeeding Assessment Tool (IBFAT) instruments. Therefore, the nurses who worked in the clinic and wanted to participate in the study were also trained on breastfeeding techniques, test weighing, study protocol, and LATCH and IBFAT applications at the start of the study. The nurses were blind to this study and they were not aware of each other as well. In addition, they were not informed about the purpose and scope of the study.
A nurse (N1) weighed the babies admitted to neonatal intensive care unit (group 1) before phototherapy. After weighing, the baby was breastfed for 40 minutes by their mother. During the breastfeeding process, the mother and baby were monitored by the nurse (N1) and breastfeeding was evaluated by latch scoring system and IBFAT. Another nurse (N2) weighed the babies after breastfeeding, with the same articles of clothing on the same electronic scale. The same procedures were repeated after phototherapy. The control group consisted of babies with physiological jaundice in the neonatal outpatient clinic. Mothers and infants in the control group were also monitored during breastfeeding and were given IBFAT and LATCH scores by a breastfeeding consultant. Each nurse and breastfeeding consultant placed the results in the envelope for each infant and the envelopes were put into a drawer and locked. At the end of the study, the researcher received results. Breast milk intake was determined with test-weighing. In the test weight, 1 g of weight gain postfeeding represented 1 mL of milk intake uncorrected for insensible water loss (1 g = 1 mL).
Serum bilirubin values and demographic characteristics of all infants in the study group were recorded.
Instruments
The LATCH breastfeeding assessment tool developed by Jensen et al., 11 in 1994 is used in evaluating the breastfeeding techniques of mother/infant dyads validity. Each letter in the abbreviation refers to a different evaluation field. L describes the ability of the infant to latch onto the breast, A describes audible swallowing noted at the breast, T describes the type of nipples, C describes the comfort level of the mother regarding her breasts, and H measures the amount of help the mother requires to position her baby at the breast. A numerical score (0, 1, or 2) is assigned to each measure for a possible total score of 10. Scores below 9 were considered as a failure in breastfeeding.
Infant Breastfeeding Assessment Tool
The IBFAT was developed to measure rooting, fixing, and suckling behavior of the infant during a feeding. 12 The first item of the tools assesses whether the infant is quite alert, drowsy, crying, or sleeping at the start of the feed. Items 2–5 measure the infant's readiness to feed and rooting, fixing, and suckling behaviors. Item 6 assesses the satisfaction of the mother with the breastfeeding experience. The range of scores for each component is 0–3. The mother's evaluation score is not calculated in the total IBFAT score (IBFATT). A total score can range from 0 to 15. We evaluated the first item (IBFAT1), sixth item (IBFAT6), and total IBFAT score (IBFATT) separately to indicate the baby's alertness condition, satisfaction of the mother, and breastfeeding behaviors of infants, respectively. Values less than three for IBFAT1 and IBFAT6 and less than 10 for IBFATT were evaluated as failure.
Statistical analysis
Statistical analysis was performed using SPSS version 16 software (SPSS, Inc., Chicago, IL). Kolmogorov–Smirnov test was conducted to analyze the normality of variables. In summarizing the data, mean ± SD for the normally distributed variables or median values (minimum-maximum) for the non-normally distributed variables were used. The chi-square test was used for categorical variables and expressed as observation counts (in percentages). While investigating the associations between non-normally distributed variables, the correlation coefficients and their significance were calculated using the Spearman test. A 5% type-I error level was used to infer statistical significance. Group comparisons were done with Student t-test or Mann–Whitney U-test. The capacities of serum bilirubin values in predicting failure of breastfeeding were analyzed using receiving operating characteristics (ROC) curve analysis. When significant cutoff values for IBFAT1, IBFATT, IBFAT6, and LATCH scores were observed, the sensitivity and specificity were presented. While evaluating the area under the curve, a 5% type-I error level was used to accept a statistically significant predictive value of the test variables. Statistical significance was accepted when the two-sided p-value was <0.05.
Results
One hundred eighty-five mother-baby dyads were included in the study. Fifteen mothers were excluded because of insufficient milk volume. Consequently, 80 infants with hyperbilirubinemia (group 1) who required phototherapy according to AAP guidelines and 90 babies with physiological jaundice (group 2 or control group) and their mothers were included in the study. The follow-up of 9 babies from group 1 could not be completed and as a result, group 1 consisted of 71, group 2 consisted of 90 infants and mothers. Demographic characteristics of the study population were given in Table 1.
Demographic Characteristics of the Study Population
Boldface indicates p < 0.05, statistically significant.
Data are presented as medians (minimum-maximum).
Data are presented mean ± standard deviation.
C/D, cesarean delivery; NSVD, normal spontaneous vaginal delivery.
Before phototherapy milk intake, IBFAT (IBFATT, IBFAT1, IBFAT6) and LATCH scores were significantly lower in group 1 than in the control group (p = 0.001) (Table 2). When normal bilirubin levels were reached after phototherapy, an increase in milk intake, IBFAT and LATCH scores was detected, and the difference between pre- and postphototherapy values was statistically significant (Table 3).
Breastfeeding Scores of Infants with Significant and Physiological Hyperbilirubinemia
Data are presented as medians (minimum-maximum).
Data are presented mean ± standard deviation.
IBFAT, Infant Breastfeeding Assessment Tool; IBFATT, IBFAT total scores; IBFAT1, IBFAT first item scores; IBFAT6, IBFAT sixth item scores.
Breastfeeding Scores of Babies with Significant Hyperbilirubinemia
Data are presented as medians (minimum-maximum).
Data are presented mean ± standard deviation.
Looking at the correlation matrix in the whole study group (groups 1 and 2) there were moderate but very significant negative correlations between bilirubin and milk intake (r = 0.32, p = 0.001), IBFATT (r = 0.47, p = 0.001), IBFAT1 (r = 0.57, p = 0.001), IBFAT6 (r = 0.65, p = 0.001), and LATCH scores (r = 0.49, p = 0.001).
There were also negative correlations between bilirubin and milk intake (r = 0.28, p = 0.007), IBFATT (r = 0.21, p = 0.047), IBFAT1 (r = 0.31, p = 0.003), and IBFAT6 (r = 0.39, p = 0.001) scores in babies with physiological jaundice.
In the ROC analysis, the cutoff bilirubin value for predicting breastfeeding failure in breastfeeding assessment tools was found to be 12 mg/dL. Cutoff bilirubin values, the sensitivity, specificity, and area under the curve values were presented in Table 4. Figure 1 shows the ROC curves for IBFATT, IBFAT1, and LATCH.

Total serum bilirubin has a significant power to predict breastfeeding failure. The ideal cutoff bilirubin value for predicting breastfeeding failure in breastfeeding assessment tools (IBFATT, IBFAT1, and LATCH) was found to be >12 mg/dL. IBFAT, Infant Breastfeeding Assessment Tool; IBFATT, IBFAT total scores; IBFAT1, IBFAT first item scores.
Cutoff Total Bilirubin Values and Receiving Operating Characteristics Analysis Results in Predicting Breastfeeding Failure with Breastfeeding Assessment Tools
AUC, area under the curve.
Discussion
Our study showed that LATCH and IBFAT breastfeeding scores and the milk intake in babies with significant hyperbilirubinemia requiring phototherapy according to AAP guidelines were statistically lower than those with physiological jaundice. In addition, these babies lost more weight than the babies in the control group and their mothers were already less satisfied with their babies' sucking. These results may suggest that hyperbiluribinemia has a negative effect on breastfeeding. However, we know that babies who do not feed well and lose weight are more prone to develop significant jaundice because of inappropriate feeding. Maybe these babies were sleepier in the first days and that is why they could not feed properly.
There are very few studies in the literature investigating the effect of hyperbilirubinemia on breastfeeding, and they were performed with bottle feeding.8–10 Therefore, our study was the first to evaluate the effect of hyperbilirubinemia on breastfeeding.
Bromiker et al. (2016) 8 compared suction parameters (number of suctions, average maximum suction pressure, burst number, average burst time, burstler pauses, and the number of bursts in each burst) and milk intake between 17 infants with bilirubin level 15 mg/dL and above (total serum bilirubin 17.8 ± 1.6 mg/dL,) and 24 controls with bilirubin level below 10 mg/dL. They demonstrated that moderate hyperbilirubinemia (15–20 mg/dL) did not affect the suction parameters and did not reduce the volume of milk consumed. The mean bilirubin levels of the groups in our study were similar to their study. However, our work designs are quite different. First of all, we evaluated the breastfeeding of babies with breastfeeding assessment tools and observed the breastfeeding process from start to finish. They fed babies with a bottle called neonur (a modification of Krohn's Nutritive sucking [NS] Apparatus) and measured the milk volume consumed manually in the first 5 minutes. We know that breastfeeding and bottle-feeding work with different mechanisms. The milk flow from the bottle is faster and the baby's milk intake is easier. However, the baby needs to have a higher suction pressure to be able to suck from the breast. Due to this difference, our results may differ. Perhaps the comparison of bottle-feeding and breastfeeding in babies with hyperbilirubinemia may elucidate this issue. We measured the milk volume with the test scale. The accuracy of the test scale could not be demonstrated in some studies,13,14 but in most studies it was found to be a valid method of measuring the amount of milk the baby received.15–18 In the same study, the milk volume in the first 5 minutes was examined. In our study, we looked at the milk volume obtained as a result of a 40-minute breastfeeding. The fact that the number of babies in the same study is quite low is also a limiting feature.
In another study, Bourgoin-Heck et al. 9 investigated the effect of hyperbilirubinemia on nutritive swallowing and swallowing-breathing coordination in preterm lambs, and showed moderate hyperbilirubinemia (150–250 μmol/L) reduced NS efficiency and NS-breathing coordinate. This effect disappeared after HB normalized. Similarly, also in our study, after the phototherapy, the baby's wakefulness scores (IBFAT1), maternal satisfaction scores (IBFAT6), breastfeeding evaluation scores (IBFATT and LATCH), and milk intake increased significantly.
What was the reason for this improving? The normalization of bilirubin values may have improved the baby's wakefulness and would allow them to suck better. On the other hand, it can be thought of as follows: mothers were taught technics for breastfeeding and emphasis on feeding was made. Therefore, the improvement in the scores could have been due to improved feeding techniques, which could be the actual reason for the strengthened feeds, rather than the reduction in bilirubin levels. We could only understand this by evaluating the breastfeeding once again in the babies within the control group. However, we evaluated the control group only once. This can be considered as a limitation of the study.
In a previous study, Alexander and Roberts examined the first week's milk consumption and sucking behavior in 24 babies with physiological jaundice. They found that hyperbilirubinemia was significantly correlated with the infants who appeared to be disinterested in being fed when assessed by clinical observations of apparent hunger and alertness at the onset of the test feed. But they did not see a divergence of the measured parameters from normal 19 and concluded that clinically acceptable levels of bilirubin did not adversely affect the feeding performance. In their study serum bilirubin levels showed no correlation with milk consumption on each day of the study or with the pooled data of feeding parameters. In contrast to their study, our study shows there is a negative correlation between bilirubin levels and milk volume and IBFAT scores in physiologically jaundiced infants. When the whole study group was examined, there was a moderate but very strong negative correlation between bilirubin values and breastfeeding scores and milk volume.
In our study, we found that bilirubin levels above 12 had a negative effect on wakefulness of infants and breastfeeding success. Perhaps at these levels, there is a slight influence on the brain that cannot be detected in today's conditions. We pay attention to these results because it also shows that the levels of bilirubin, which is ought to be accepted at physiological limits, are to be questioned whether they are truly safe at those rates. At least it tells us that babies who do not exceed photo limits but who have bilirubin more than 12 mg/dL should also be monitored closely for nutrition. Perhaps these levels of bilirubin should be identified as a risk to breastfeeding. However, before reaching a final judgment, it should be supported by more detailed and comprehensive studies using more objective tools.
Limitations
Our study has some limitations. (1) We measured breastfeeding and milk intake only once in the control group, and we did not monitor those babies. The babies cannot be expected to exhibit the same behavior in all feeding sessions. If we reevaluated these babies, we could see whether there was an improvement in their sucking ability over time as in postphototherapy values of infants with significant jaundice. (2) No suction parameters such as number of suction, average maximum suction pressure, number of bursts, average burst duration, inter-burst pauses, and number of suction per burst could not be analyzed. (3) Bottle feeding was not evaluated, only breastfeeding was evaluated. If both were evaluated, it would be possible to determine whether there was a difference in the effects of bilirubin on breastfeeding and bottle-feeding. If bottle-feeding is not affected in hyperbilirubinemia, this can be preferred for feeding in these babies.
Conclusions
Hyperbilirubinemia sufficiently elevated to require phototherapy may have a negative effect on breastfeeding and milk intake. Reaching normal bilirubin levels after phototherapy may eliminate this negative effect. There was a negative correlation between bilirubin levels and milk volume, LATCH and IBFAT scores. Bilirubin levels above 12, including in babies with physiological jaundice, appear to adversely affect breastfeeding. Larger and more planned studies needed to be conducted for a final judgment on this issue.
Footnotes
Acknowledgments
I thank breastfeeding consultant Ayşe Ünsal and the nurses Serpil Altunel and Nurcan Çiftçi Tekin for their valuable contributions to our study.
Authors' Contributions
N.A. conceptualized and designed the study, acquired and interpreted the data, drafted the article, and approved the final article as submitted.
Disclosure Statement
No competing financial interests exist.
Funding Information
No funding was received for this article.
