Higher Fat Content in Breastmilk Expressed Manually: A Randomized Trial

Abstract

Objective:

This study aimed to evaluate the effect of milk expression method (manual expression versus electric pump) on the composition of breastmilk.

Study Design:

Data on 21 mothers of 21 newborns 48–72 hours postdelivery were collected and analyzed. The women were randomly assigned to express breastmilk manually followed by pump, or in reverse order. The fat, carbohydrate, and protein contents of the milk samples were analyzed using a human milk analyzer (Miris AB, Uppsala, Sweden).

Results:

The fat and energy contents of milk obtained through manual expression were higher than those obtained by pump (p=0.024 and p=0.04, respectively, by the Wilcoxon signed rank test). There were no significant differences in protein or carbohydrate content of milk obtained by either method of expression. The difference in fat content between milk obtained by the two methods was not correlated with mother's age, delivery method, gestational age at delivery, parity, or the interval between delivery and the time the sampled milk was obtained.

Conclusions:

Manually expressed human milk had higher fat content than milk expressed by electric pump. We speculate that this difference is due to the presence of hindmilk in the manually expressed milk because the technique of massaging the breast during manual expression is more likely than the pump to eject hindmilk, which has been shown to have higher fat content than foremilk.

Introduction

Breastmilk is a unique and unmatched nutritional and nonnutritive source of bioactive factors for the health and development of infants.¹ Colostrum, which is produced in low quantities for the first 3–4 days after birth, is rich in immunologic components and developmental factors.² Breastfeeding difficulties during the first days of life of an infant are common.^3–5 Moreover, not all infants can be directly fed at the breast.⁶ Therefore, breastmilk feeding at this early stage is initiated and promoted by the expression of breastmilk either manually or by use of a pump. Whether the method of milk expression at this stage has a qualitative impact on colostrum is currently unknown. We conducted this randomized controlled study in order to compare the effect of manual expression with electric pump expression on the macronutrient composition of breastmilk.

Subjects and Methods

Mothers of full-term newborns (n=21) were enrolled for this study at the Lis Maternity Hospital of Tel Aviv Sourasky Medical Center, Tel Aviv, Israel. The study was approved by our local Institutional Review Board, and written informed consent was obtained from the mothers. We included healthy breastfeeding mothers, who were not taking any medication, between 48 and 72 hours after delivery. Of the 50 mothers who agreed to participate in this study, 29 were excluded due to insufficient milk volume (n=24), accidental thawing of frozen samples (n=4), or withdrawn consent (n=1), leaving 21 pairs of samples for analysis (13 mothers at 48 hours and eight mothers at 72 hours following delivery). The subjects were randomly assigned to express breastmilk manually followed by pump (n=9) or to express milk by pump followed by manual expression (n=12). Therefore two samples of milk were analyzed from each participating mother. A certified lactation consultant (M.A.) was available to assist the mothers in using both techniques.

For pump expression, we used hospital-grade electric pumps (Symphony^® breast pump; Medela, Baar, Switzerland), and breastmilk was pumped into a sterile receptacle. During manual milk expression, the women were instructed to gently massage the breast, and milk was drained by holding the breast between the fingers while pushing toward the chest wall followed by rolling the fingers toward the areola. At least 2 mL of breastmilk was collected per method of expression from the same breast during the same meal. The whole procedure did not exceed a few minutes of milk expression for each of the methods.

Samples were stored at −20°C for 48 hours and then preserved at −80°C until analysis. The determination of the macronutrient (fat, carbohydrates, and proteins) composition of human milk was performed with a mid-infrared human milk analyzer (Miris AB, Uppsala, Sweden). The samples were assayed in duplicate, and the average of the two results was used for analysis.

Statistical analysis was performed using Minitab (State College, PA) release 14 software. The Wilcoxon signed rank test was used to compare macronutrient composition of breastmilk expressed by the two methods, and regression analysis was used to assess the impact of independent variables, such as parity, time of obtaining milk since delivery, mother's age, delivery method and gestational age, on the dependent variables. A p value of <0.05 was considered significant.

Results

The demographic data of mothers and infants are listed in Table 1.

Table 1.

Maternal and Neonatal Characteristics of the 21 Study Mothers and Their 21 Infants

	Mean±SD	Median	Range
Birth weight (g)	3,048.714±470.263	2,965	2,130–4,068
Gestational age (weeks)	38.619±1.283	39	36–41
Maternal age (years)	32.9±3.935	32	26–41

SD, standard deviation.

We analyzed 21 pairs of milk samples. The fat content of milk obtained through manual expression (2.3±1.27 g/100 mL) was significantly higher than that obtained by pump (1.84±1.36 g/100 mL) (p=0.024). Energy content of milk expressed manually was also higher (53.47±13.66 kcal/100 mL) compared with pumping (48.9±14.8 kcal/100 mL) (p=0.04). There were no significant differences in protein or carbohydrate content of milk obtained by manual expression versus pump (Table 2).

Table 2.

Comparison of Fat, Protein, and Carbohydrate Levels in Breastmilk Expressed Manually or by Pump

	Manual expression	Pump expression	p value
Mean fat (g/100 mL)	2.3±1.27	1.84±1.36	0.024
Mean protein (g/100 mL)	2.06±0.98	2.03±0.89	NS
Mean carbohydrates (g/100 mL)	5.39±0.92	5.39±0.78	NS
Mean energy (kcal/100 mL)	53.47±13.66	48.9±14.8	0.04

NS, not significant.

The difference in fat content between milk obtained by the two expression methods was not correlated with the mother's age, delivery method, gestational age at time of birth, parity, or the amount of time that had passed since delivery.

Discussion

The results of the present study showed that breastmilk obtained within the first 48–72 hours after delivery by manual expression contains a higher fat content than breastmilk obtained by a pump. There were no similar differences in protein and carbohydrate concentrations. In order to compare the macronutrient composition of the breastmilk obtained by each method, the participating mother provided one sample for each method in a randomized sequence (pump expression followed by manual expression, or in reverse order) and from the same breast during the same meal. In essence, each mother served as her own control. This design ensured that the results were not influenced by confounding variables, such as maternal age, parity, and diet.

A recent randomized controlled study showed that early manual milk expression increased breastfeeding rates by 25% at 2 months compared with breast pumping.⁷ Several studies have also evaluated the effect of expression methods on milk volume. Due to conflicting results, it is still undetermined whether manual expression of breastmilk also yields greater milk volume than the volume expressed by use of an electric pump in the early postpartum period: either no significant volume differences existed between manual versus pump expression,⁶ or hand expression yielded consistently higher volume.⁸ Additionally, in mothers of preterm infants, the hands-on pumping approach that combines hand expression with electric breast pumping increased milk production during the first 8 weeks of milk expression⁹ and increased both fat and caloric content of mature milk.¹⁰ It was shown that manual expression within 48 hours after delivery was more comfortable for the mothers compared with using a hospital-grade electric pump.⁸ Once milk production was well established, however, breastmilk expression by electric pump led to greater volume of human milk.¹¹ In the 2015 updated Cochrane review, the authors concluded that low-cost measures such as early initiation of expressing, relaxation, hand expression, and lower-cost pumps may be as effective or more effective than large electric pumps for some outcomes.¹² In a recent study on African mothers, the use of an electric breast pump yielded a greater breastmilk volume on average, especially 48 hours after delivery, although hand expression still generally provided enough milk volume for the infant needs.¹³ Those authors concluded that hand expression may be an adequate alternative to direct breastfeeding in developing countries in cases of sick and premature infants.

The present study is the first to evaluate differences in macronutrient composition of breastmilk expressed using these two methods early after delivery. The reason for the difference in fat content is not clear. Previous studies have shown that hindmilk has higher fat content than foremilk, whereas there was no significant difference in protein or lactose content.¹⁴ A randomized controlled study by Jones et al.¹⁵ found no difference in fat concentration between breastmilk expressed by pumping compared with milk expressed by pumping while simultaneously massaging the breast at day 5 or later post-partum. In contrast, Foda et al.¹⁶ found that breast massage significantly increased lipid content of milk expressed during the late lactation period (3 months postdelivery) but not in the early lactating period.

The reason for the increase in fat concentration in breastmilk obtained by hand expression with concomitant breast massage such as that seen in our study is not known. We speculate that the process of breast massaging may mix hindmilk and foremilk, resulting in higher fat content. A plausible explanation for this mixing of hindmilk and foremilk may be the fact that hand expression mimics the movement of infantile suckling better than the use of an electric breast pump. Hand expression uses positive pressure and the milk ejection reflex to release milk from the ducts, whereas breast pumps generate negative pressure combined with the milk ejection reflex. In addition, Morton et al.^9,10 have suggested that breast compression during hand expression allowed a more effective removal of the viscous colostrum and increases forward flow.

Recent ultrasound studies of term infants showed that during breastfeeding, as the tongue is drawn downward, the nipple expands evenly and milk flows into the infant's oral cavity.^17,18 Moreover, intraoral vacuum applied by the established breastfeeding infant corresponds with the downward movement of the tongue and milk flow.¹⁸ An example for nonefficient milk expression is an infant with severe symptomatic tongue-tie.¹⁹ Lingual frenotomy allows for more efficient milk expression, probably by allowing a better mechanical effect rather than by influencing vacuum production.²⁰ Whether effective emptying is influenced more by negative pressure produced by sucking or by the infant's tongue movements remains unresolved.

The fact that it is more difficult to obtain colostrum by electrical pumping of the breast compared with manual expression⁸ supports the use of manual expression with massage as we used in our study for infants who are unable to breastfeed. The greater amount of fat content supplies the infants with a higher caloric intake and increases the availability of essential fatty acids and fat-soluble vitamins.

Conclusions

Manually expressed human milk has a higher fat content than milk expressed by electric pump within the first 72 hours after delivery. We speculate that this difference is due to the presence of hindmilk in the manually expressed milk because the technique of massaging the breast during manual expression may result in the ejection of hindmilk, which has higher fat content than foremilk. We further speculate that the higher fat content of the expressed breastmilk may be beneficial to the breastfed infant.

Footnotes

Acknowledgments

The researchers are indebted to Esther Eshkol, MA, the institutional medical/scientific copyeditor, for editorial assistance.

Disclosure Statement

No competing financial interests exist.

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