Published online August 31, 2005
PEDIATRICS Vol. 116 No. 3 September 2005, pp. e432-e435 (doi:10.1542/peds.2005-0313)
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ELECTRONIC ARTICLE

Fat and Energy Contents of Expressed Human Breast Milk in Prolonged Lactation

Dror Mandel, MD, MHA*,{ddagger}, Ronit Lubetzky, MD*,{ddagger},§, Shaul Dollberg, MD, FACN*,{ddagger}, Shimon Barak, MD* and Francis B. Mimouni, MD, FAAP, FACN*,{ddagger}

* Department of Neonatology, Lis Maternity Hospital, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel
{ddagger} Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
§ Department of Pediatrics, Dana Children's Hospital, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Objective. To estimate fat and energy contents of human milk during prolonged lactation.

Methods. Thirty-four mothers, of term, healthy, growing children, who had been lactating for >1 year (12–39 months) were recruited. Control subjects were 27 mothers, of term infants, who had been lactating for 2 to 6 months. Fat contents of the milk samples were estimated as creamatocrit (CMT) levels. Energy contents of the milk were measured with a bomb calorimeter.

Results. The groups did not differ in terms of maternal height and diet, infant birth weight, gestational age, or breastfeeding frequency. They differed significantly in terms of maternal age, maternal weight, and BMI. The mean CMT levels were 7.36 ± 2.65% in the short-duration group and 10.65 ± 5.07% in the long-lactation group. The mean energy contents were 3103.7 ± 863.2 kJ/L in the short-duration group and 3683.2 ± 1032.2 kJ/L in the long-duration group. The mean CMT levels and mean energy contents were correlated significantly with the duration of lactation (R2 = 0.22 and R2 = 0.23, respectively). In multivariate regression analysis, CMT levels (or energy contents) were not influenced by maternal age, diet, BMI, or number of daily feedings but remained significantly influenced by the duration of lactation.

Conclusions. Human milk expressed by mothers who have been lactating for >1 year has significantly increased fat and energy contents, compared with milk expressed by women who have been lactating for shorter periods. During prolonged lactation, the fat energy contribution of breast milk to the infant diet might be significant.

Key Words: breast milk • breastfeeding • lactation • energy intake

Abbreviations: HM, human milk • CMT, creamatocrit

The optimal duration of breastfeeding is unknown. The American Academy of Pediatrics recommends exclusive breastfeeding for 6 months and a total duration of ≥1 year to obtain the "full benefits of breastfeeding."1 Among frequently recognized long-term benefits of breastfeeding are reductions in cardiovascular risks in adulthood.1, 2 These reductions were challenged by a retrospective epidemiologic study of men born in 1920 to 1930 in Hertfordshire, England, which suggested that the beneficial effects of breastfeeding on cardiovascular risks existed as long as weaning was performed before 1 year of age; after that time, continued breastfeeding was associated paradoxically with increased cardiovascular risks.2 Moreover, a study by Leeson et al3 suggested that prolonged breastfeeding might lead to unwelcome outcomes and might even increase cardiovascular risks in adulthood.

In developed countries, a minority of women continue to lactate for >1 year; in one study from Italy, 17% of mothers were still breastfeeding at 12 months after delivery.4 The energy contribution of human milk (HM) to the diet of partially breastfed children beyond the first year of life is unknown, because there are no data on the amounts of HM consumed by these children and the nutritional content of HM after prolonged breastfeeding is little known. In particular, the fat and energy contents of HM after prolonged breastfeeding have not been analyzed systematically. We therefore conducted this cross-sectional study of 61 women who had been lactating for periods of 2 to 6 months (short lactation duration) or >1 year (long lactation duration), to estimate the fat and energy contents of HM.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Thirty-four mothers, of term, healthy, growing children, who had been lactating for >1 year were recruited and compared with 27 mothers, of term infants, who had been lactating for 2 to 6 months. All infants were healthy, were free of congenital malformations, and had been delivered after a normal pregnancy, labor, and delivery. To control for possible diurnal variations,5, 6 for every subject we used for analyses the mean of 2 samples, one collected at 6:00 to 9:00 AM and the other collected at 9:00 PM to midnight. The mothers' diet type (omnivorous versus lacto-ovo-vegetarian) was recorded. Our study was approved by our local institutional review board, and informed consent was obtained from all of the mothers in this study.

Laboratory Methods
Milk was collected at home by mothers through manual expression in mid-breastfeeding, stored at 3°C to 5°C, and analyzed (after homogenization) for fat content within 24 hours. The fat content of the milk samples was measured with the creamatocrit (CMT) method, as described previously.7–11 Briefly, 75-µL aliquots were placed into 2 glass capillary tubes, which were sealed at one end and centrifuged in a hematocrit centrifuge for 5 minutes at 9000 rpm. The CMT level was recorded to the nearest 0.5 mm and expressed as a percentage of the length of the milk column in the tube. Each reading was performed in duplicate in a blinded manner, by an investigator who was not aware of the origin and time of sampling. The final result was the average of the 2 readings. A random subset of samples (n = 30) was also analyzed directly for energy content with the static bomb calorimetry method, as described by Garza et al,12 with a Parr 1261 bomb calorimeter (Parr Instruments, Moline, IL); results were expressed as kilojoules per liter of milk.

Statistical Analyses
Results were expressed as mean ± SD or number and percentage. Student's t tests were used to determine the differences between the 2 groups (2–6 months and >1 year) for continuous variables, with {chi}2 tests for categorical variables. Linear regression analysis was used to determine the correlation between CMT levels and energy contents. Backward, stepwise, multivariate regression analyses were used to determine the effects of lactation duration, maternal weight or BMI, and maternal age (independent variables) on CMT levels and energy contents (dependent variables).


   RESULTS
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 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Demographic and maternal characteristics of the participants in this study are presented in Table 1. Briefly, mothers were healthy and had not suffered from hypertensive disorders of pregnancy or diabetes mellitus. Most were omnivorous (Mediterranean-type diet), except for 2 mothers who were lacto-ovo-vegetarians (1 in each group).


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  		TABLE 1. Subject Characteristics and CMT and Energy Data

 
There were 61 mothers, who had been breastfeeding for either 2 to 6 months (short-duration group, n = 27) or 12 to 39 months (long-duration group, n = 34). The 2 groups (short-duration versus long-duration lactation) did not differ in terms of maternal height and diet, infant birth weight, gestational age, or breastfeeding frequency. They differed significantly, however, in terms of maternal age, maternal weight, and BMI (Table 1). In addition, there were significant differences between the 2 groups in terms of CMT and energy content values (Table 1). The energy contents were correlated significantly with the CMT levels (energy [kilojoules per liter] = 2288 + 117 · CMT [percent]; R2 = 0.37, P < .0001). Mean CMT levels and mean energy contents were correlated significantly with the duration of lactation (R2 = 0.22, P < .0001, and R2 = 0.23, P < .0001, respectively) (Fig 1). In multivariate regression analysis, CMT levels (or energy contents) were not influenced by maternal age, diet type, BMI, or number of daily feedings but remained significantly influenced by the duration of lactation.


Figure 1
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  		Fig 1. Correlation between mean CMT values (percent) and duration of lactation (months).

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We demonstrated that, in HM expressed by mothers who had lactated for >1 year, the fat and energy contents were increased significantly, compared with HM expressed by women who had lactated for a shorter period (2–6 months). In fact, CMT levels for the long-duration group were at times extraordinarily high (up to 28%), compared with the short-duration group or values in previous publications, which reported ranges of 5% to 17.5%.13

These results could be explained theoretically by a direct effect of the lactation duration on CMT levels and energy contents. Alternatively, inherent differences between the 2 groups in the study might also have played a role. Indeed, our study was limited by the fact that it was not a longitudinal one, and many subtle or less-subtle differences between the 2 groups other than the lactation duration might have influenced the CMT levels and energy contents. In our study, maternal diet was not studied systematically from a dietary recall standpoint. However, most women in the study ate a Mediterranean-type diet, and only 1 woman in each group was lacto-ovo-vegetarian, which did not allow us to speculate in any manner on dietary influences. The 2 groups were also similar in terms of maternal height, infant birth weight, gestational age, and breastfeeding frequency. They were, however, significantly different in terms of maternal age (older mothers in the long-duration group), maternal weight, and BMI (both higher in the short-duration group). The presence of older mothers in the long-duration group might indicate significant socioeconomic differences between the 2 groups, which theoretically might have influenced the results. However, in the multivariate regression analysis, maternal age did not influence CMT levels. The same was true for maternal weight and maternal BMI, which also were found not to influence CMT levels. Higher maternal weight and BMI in the short-duration group were probably the result of the more recent pregnancies in this group (women are known to lose most of the weight accumulated during pregnancy during the first year of life of the infant14).

Therefore, despite the cross-sectional aspect of our study, we think that differences in the length of lactation per se explained the striking differences in CMT levels and energy contents that we found in this study. The reasons for the differences in energy and fat contents are not found readily in the available literature. Indeed, there are very few data on the nutritional value of breast milk during prolonged (>1-year) lactation. A Medline search using the key words "lactation" or "breast milk" or "human milk" or "breastfeeding" and "duration" and "composition" revealed only 8 articles, of which 7 originated from developing countries15–21 and only 2 dealt with issues of milk composition.20, 21 The largest study on the topic, by Dewey et al,22 found that "fat ... concentrations" (in late lactation) "were similar to those in earlier stages of lactation." However, careful examination of the data reported by Dewey et al22 revealed that the aforementioned statement in their article's abstract was not supported by their actual data, which showed a significant increase in fat content in late lactation, compared with early lactation (6.22 ± 2.87 g/100 mL vs 4.03 ± 2.17 g/100 mL). This increase of ~50% in fat content from early to late lactation is very similar to the ~50% increase in CMT levels that we found in our study. In a longitudinal study by Nommsen et al,23 there were no changes in lipid or energy contents over time, but that study was limited to the first year of life and did not assess prolonged lactation beyond the first year. Moreover, the contribution of fat content to energy content was very significant in our study. Others found that CMT levels were correlated very well with energy contents of milk.7, 8 Our study confirmed this and was the only study of its type that examined the relationship between CMT and energy contents measured with direct bomb calorimetry, rather than calculated from nutritional equations.11

Therefore, it seems theoretically that, during prolonged lactation, the contribution of breast milk to the infant diet might be significant, from an energy intake standpoint. Indeed, a reduction in the volume of milk consumed by a child who is also eating solid foods might well be counterbalanced by the increase in energy concentration. A limitation of this statement is that, similar to the study by Dewey et al,22 we were not able to measure accurately the volumes consumed at the breast by each infant, for obvious technical reasons. Mothers in our study were not instructed to double-weigh the infant before and after every feeding, because of the cumbersome aspects. Nevertheless, it seemed that some women in the long-duration lactation group were able to reach extraordinarily high CMT values, such as a woman whose expressed breast milk had a CMT level of 28%.

The long-term effects of such high fat intake have not been studied. We did not analyze the fat qualitatively in this study, but it is known that, compared with infant formula, breast milk is much richer in cholesterol and saturated fat.24 The effects of high intake of saturated fat and cholesterol on infant cholesterol metabolism are consequential. We showed that, in the first few months of life, higher cholesterol intake among breastfed infants led to downregulation of endogenous cholesterol production.25 Whether continued high saturated fat and cholesterol intake through breastfeeding beyond the first year of life is beneficial is unknown. As quoted earlier, prolonged breastfeeding has been "accused" of possibly inducing long-term endothelial damage and of decreasing arterial distensibility,2, 3, 26–28 but many objections have been raised against this accusation.29–31 The type of fats present in the milk of mothers lactating for >1 year needs to be measured before suggestions of the role in adult heart disease can be mentioned. Also, because of the changes in diets from childhood to adult years, it may not be possible to determine the influence of prolonged breastfeeding on cardiovascular disease.

We must point out that, at the present time, the official policy of the American Academy of Pediatrics is not to put any limit on the duration of lactation.1 Moreover, a recent review of biological versus cultural aspects of weaning suggested that, from an anthropologic standpoint based on primates studies, "breastfeeding a child for 2.5 to 7 years is normal for our species."32


   FOOTNOTES
 
Accepted Mar 16, 2005.

Reprint requests to (D.M.) Department of Neonatology, Lis Maternity Hospital, Tel Aviv Sourasky Medical Center, 6 Weizman St, Tel Aviv, 64239, Israel. E-mail: dmandel{at}post.tau.ac.il


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 RESULTS
 DISCUSSION
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2005 by the American Academy of Pediatrics

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