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Journal of the American College of Nutrition, Vol. 25, No. 2, 151-154 (2006)
Published by the American College of Nutrition

Circadian Variations in Fat Content of Expressed Breast Milk from Mothers of Preterm Infants

Ronit Lubetzky, MD, Yoav Littner, MD, Francis B. Mimouni, MD, FACN, Shaul Dollberg, MD, FACN and Dror Mandel, MD, MHA

Department Neonatology, Lis Maternity Hospital (R.L., Y.L., F.B.M., S.D., D.M.)
Department of Pediatrics, Dana Children’s Hospital (R.L.)
Tel Aviv Sourasky Medical Center, the Sackler Faculty of Medicine, Tel Aviv University (R.L., Y.L., F.B.M., S.D., D.M.), Tel Aviv, ISRAEL

Address correspondence to: Shaul Dollberg, MD, Department of Neonatology, Lis Maternity Hospital, Tel Aviv-Sourasky Medical Center, 6 Weizman Street, Tel Aviv, 64239, ISRAEL. E-mail: dolberg{at}post.tau.ac.il


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 REFERENCES
 
Background:Little is known about circadian variations of the fat content in expressed human milk by mothers of preterm infants.

Objective: To test the hypothesis that the fat content of expressed preterm human milk is higher in samples expressed in the evening (i.e. after 3 daily meals) than in the morning (after a night-long fast).

Methods: We collected samples of expressed human milk obtained from 39 mothers of hospitalized growing preterm infants aged 7–14 days, with a gestational age at birth ranging from 26 to 33 weeks, who routinely expressed all their milk every 3 hours, during the day time, just before bed time, and as soon as they woke up, using a commercial breast pump (Medela AG, Baar, Switzerland). One sample was obtained from the first morning expression (between 0600 and 0900) and the second from the evening expression (between 2100 and 2400). The entire quantity of expressed milk was collected, mixed and measured in a capillary tube after centrifugation at 9000 rpm for 5 minutes. Creamatocrits (CMT) were performed in duplicates. Each sample was read independently by 2 investigators who were not aware of the origin and time of sampling and the results were averaged. Results are expressed as mean ± SD, and analyses were by paired t-test and regression analysis.

Results: CMT was significantly higher in evening than in morning samples (7.9 ± 2.9% vs. 6.6 ± 2.8%, P = 0.005). Neither CMT nor the morning-evening difference in CMT correlated with gestational age or birthweight. The morning CMT correlated significantly with the evening CMT (P < 0.001).

Conclusions: There are significant circadian variations in the CMT of expressed preterm human milk. We speculate that if higher caloric content of expressed human milk is needed in a specific preterm infant, evening sample, if available, should be used preferentially.

Key words: breast milk, preterm infants, fat content, circadian variations

Abbreviations: CMT = creamatocrit


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 REFERENCES
 
Little is known about circadian variations of fat content of expressed preterm human milk. Few studies have been conducted and have led to opposite results [1,2]. One study found that circadian variations of fat content exist, but without any given pattern of cyclicity [1], while another study found lower concentrations of fat in morning samples than during the rest of the day [2].

We thus designed the following prospective study in order to examine morning and evening samples of human milk expressed by mothers of preterm infants. Specifically, we tested the hypothesis that the fat content of expressed human milk is higher in samples expressed in the evening (i.e. after 3 daily meals) than in the morning (after a night-long fast).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 REFERENCES
 
Laboratory Methods
We collected samples of expressed human milk obtained from 39 mothers of hospitalized growing preterm infants aged 7–14 days, with a gestational age at birth ranging from 26 to 33 weeks, who routinely expressed all their milk every 3 hours during the day time, just before bed time, and as soon as they woke up, using a commercial breast pump (Medela AG, Baar, Switzerland). One sample was obtained from the first morning expression (between 0600 and 0900) and the second one from an evening expression (between 2100 and 2400). Each mother in the study contributed only one morning and one evening sample (obtained on the same day). The entire sample was collected and mixed. The fat content was measured using the creamatocrit (CMT) method, as previously described [3–8]. Briefly, 75 µL aliquots were filled into glass capillary tubes, which were sealed at one end and spun in a hematocrit centrifuge for 5 minutes at 9000 rpm. The creamatocrit was read 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 two investigators who were not aware of the origin and time of sampling. The results of the independent readings by the 2 investigators were averaged. This method is extremely precise and reproducible with a coefficient of variation of less than 1%. It highly correlates with total lipid biochemical measurements [9], making it an "accurate inexpensive and useful technique for estimating lipid concentration" of expressed breast milk [9].

Statistical Analyses
Results are expressed as mean ± SD, and circadian differences were tested by paired t-test. Regression analysis was used to study the correlation between CMT and gestational age or birthweight, and to study the potential correlation between morning and evening CMT.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
REFERENCES
 
Demographic and maternal characteristics of the participants in this study are presented in Table 1. Mothers were healthy, had not suffered from hypertensive disorder of pregnancy or of diabetes, and most were omnivorous, to the exception of 2 mothers who were lacto-ovo-vegetarians.


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  		Table 1. Maternal and Neonatal Characteristics of the Study Infants

 
On average, CMT was significantly higher in evening than in morning samples (7.9 ± 2.9% vs. 6.6 ± 2.8%, P = 0.005). In fact, in 32 out of 39 samples (82%), evening CMT exceeded morning values, while in 2 samples values were identical and in 5 samples CMT morning values exceeded evening values. Neither CMT nor the morning-evening difference in CMT correlated with gestational age or birthweight. The morning CMT correlated significantly with the evening CMT (R2 = 0.302, P < 0.001) (Fig. 1).


Figure 1
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  		Fig. 1. Correlation of morning creamatocrit (%) and evening creamatocrit (%).

 

   DISCUSSION
 
We have demonstrated that in human milk expressed by mothers of preterm infants, similar to what has been observed in term infants [10], there are significant circadian variations in CMT, which is consistently lower in morning than in evening samples.

We believe that the differences observed between morning and evening values of CMT reflect differences in fat content. Indeed, Lucas et al [4], as well as Wang et al [8] have shown that the CMT method correlates highly and linearly both with total fat content and energy content of milk. Thus, we may assume that morning human milk expressed in such a fashion is lower in fat and energy than evening milk.

The reason, or reasons for these circadian variations have not been fully understood to date. It is possible that the circadian variations in human fat content may have been influenced by the degree of breast fullness [11] together with, or rather than circadian dietary habits. Indeed, total fat content of milk is lower in foremilk than in hind milk [12] and theoretically it is possible that the breast of the women in our study were fuller in the morning (after more than 3 hours without expressing) than in the evening after the whole day of pumping every 3 hours. We must point out to the fact that Insull et al, demonstrated that the volume of milk obtained by pumping and or manual expression is surprisingly higher (thus more complete or less incomplete) than when the breasts are nursed by the baby [13]. Daly et al, demonstrated that changes in the rate of milk synthesis were not directly associated with the frequency of breastfeeds but rather with the degree of emptying of the breast [14]. Nevertheless and regardless of the specific explanation, the fact remains that morning samples are lower in fat than evening samples.

We further speculate that dietary habits may be responsible for this phenomenon. Indeed, morning samples are obtained most probably after a nightlong fast, while evening samples are expressed after several daytime meals. It is well known that dietary fat is highly influential upon the quality of fat content in human milk. For instance, fatty acid distribution in human milk is strikingly different in vegetarian or macrobiotic lactating mothers and omnivorous mothers [15]. Insull et al, have shown that daily fat milk production may be affected by dietary manipulations for a period of 4 days, in that it correlated with high energy and fat intake by the mother [13]. Whether altered diet indeed influenced fat content between morning and evening samples is currently not known. In our study, morning and evening CMTs were highly correlated, which might indicate that a given dietary intake in a given mother is influential on fat content. Moreover, limited studies with supplementary feeding of poorly nourished lactating women have suggested the feasibility of improvement in volume output and in nutritional quality of breast milk [16].

We speculate that if a higher caloric content is needed in a specific preterm infant fed his mother’s expressed human milk, evening samples, if available, should be used preferentially. However, in many cases, the volume of expressed breast milk may not be sufficient to allow for preferential use of evening samples. Furthermore, from the fact that morning and evening CMT values were highly correlated, we also suggest that more studies should be designed to test the hypothesis that specific dietary manipulations might allow caloric enrichment of expressed human milk.

Received October 9, 2004. Accepted February 16, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 REFERENCES
 

  1. Gross SJ, Geller J, Tomarelli RM: Composition of breast milk from mothers of preterm infants. Pediatrics68 :490 –493,1981 .[Abstract/Free Full Text]
  2. Weber A, Loui A, Jochum F, Buhrer C, Obladen M: Breast milk from mothers of very low birthweight infants: variability in fat and protein content. Acta Paediatr90 :772 –775,2001 .[Medline]
  3. Fleet IR, Linzell JL: A rapid method of estimating fat in very small quantities of milk. J Physiol175 :14 –17,1964 .
  4. Lucas A, Gibbs JA, Lyster RL, Baum JD: Creamatocrit: simple clinical technique for estimating fat concentration and energy value of human milk. Br Med J1 :1018 –1020,1978 .[Medline]
  5. Lemons JA, Schreiner RL, Gresham EL: Simple method for determining the caloric and fat content of human milk. Pediatrics66 :626 –628,1980 .[Abstract/Free Full Text]
  6. Lonnerdal B, Smith C, Keen CL: Analysis of breast milk: current methodologies and future needs. J Pediatr Gastroenterol Nutr3 :290 –295,1984 .[Medline]
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  10. Cregan MD, Mitoulas LR, Hartmann PE: Milk prolactin, feed volume and duration between feeds in women breastfeeding their full-term infants over a 24 h period. Exp Physiol87 :207 –214,2002 .[Abstract]
  11. Daly SE, Di Rosso A, Owens RA, Hartmann PE: Degree of breast emptying explains changes in the fat content, but not fatty acid composition, of human milk. Exp Physiol78 :741 –755,1993 .[Abstract]
  12. Forsum E, Lonnerdal B: Variation in the contents of nutrients of breast milk during one feeding. Nutr Rep Int19 :815 –820,1979 .[Medline]
  13. Insull W Jr, Hirsch J, James T, Ahrens EH Jr. The fatty acids of human milk. II. Alterations produced by manipulation of caloric balance and exchange of dietary fats. J Clin Invest38 :443 –450,1959 .[Medline]
  14. Daly SE, Kent JC, Owens RA, Hartmann PE: Frequency and degree of milk removal and the short-term control of human milk synthesis. Exp Physiol81 :861 –875,1996 .[Abstract]
  15. Specker BL, Wey HE, Miller D: Differences in fatty acid composition of human milk in vegetarian and nonvegetarian women: long-term effect of diet. J Pediatr Gastroenterol Nutr6 :764 –768,1987 .[Medline]
  16. Jelliffe DB, Jelliffe EF: The volume and composition of human milk in poorly nourished communities. Am J Clin Nutr31 :492 –515,1987 .




This Article
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Right arrow Articles by Lubetzky, R.
Right arrow Articles by Mandel, D.

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