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© 2006 American Society for Nutrition J. Nutr. 136:2558-2561, October 2006

Nutrient Requirements and Optimal Nutrition

Trans Fatty Acids in Human Milk in Canada Declined with the Introduction of Trans Fat Food Labeling1

Russell Friesen and Sheila M. Innis*

The Nutrition Research Program, Child and Family Research Institute, University of British Columbia, Vancouver, British Columbia, Canada V5Z 4H4

* To whom correspondence should be addressed. E-mail: sinnis{at}interchange.ubc.ca.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Trans fatty acids in human milk have raised concerns because of possible adverse effects on infant growth and development. Analyses of human milk in the late 1990s in Canada showed high amounts of trans fatty acids from partially hydrogenated oils. Canada introduced labeling of trans fatty acids on retail foods in 2003. We analyzed trans and cis unsaturated and saturated fatty acids in human milk collected from 87 women in 2004–2006 and compared the levels to those in milk collected from 103 women in 1998 and analyzed using similar methods. The total trans fatty acids (mean ± SEM, g/100 g fatty acids) in human milk in Canada decreased significantly, from 7.1 ± 0.32 in 1998 to 6.2 ± 0.48, 5.3 ± 0.49, and 4.6 ± 0.32 over 3 consecutive 5-mo periods from November 2004 to January 2006. The milk total trans fatty acids were significantly and inversely related to 16:0, 18:2(n-6), 18:3(n-3), 20:4(n-6), 22:4(n-6), and 22:5(n-6) and positively related to 18:0 and conjugated linolenic acids (P < 0.05, n = 190). The estimated exposures of exclusively breast-fed infants to trans fatty acids decreased from a mean and 95th percentile intake of 2.0 and 4.4 g · infant–1 · d–1 in 1998 to 1.33 and 2.41 g · infant–1 · d–1, respectively, in late 2005. The estimated intake of the mothers was 4.0 (range 0.51–12.3) and 2.2 (0.56–7.65) g · person–1 · d–1 in 1998 and late 2005, respectively. Our studies show trans fatty acids have decreased in human milk in Canada, which suggests a concomitant decrease in trans fatty acid intake among lactating women and breast-fed infants.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Recent interest in the health effects of trans fatty acids has centered largely around potential adverse effects of trans fatty acids on lipid risk factors for cardiovascular disease, including markers of enhanced inflammatory response (1–5). During growth and development, adverse effects of trans fatty acids on the metabolism of the essential (all-cis) (n-6) and (n-3) fatty acids are additional concerns (6–8). Trans fatty acids are present in the diet from two sources: the industrial partial hydrogenation of fats and oils containing cis unsaturated fatty acids, and in the milk and meat of ruminant animals as a result of biohydrogenation of fatty acids in the rumen (9). Estimates of the average daily intake of trans fatty acids by adults in the United States, Canada, Europe, and Australia from the 1980s to 2000, based on food usage, food-frequency questionnaires, or duplicate portion analysis, ranged from 3 to 17 g/person (10–15). Whereas trans fatty acids can represent as much as 60% of the fatty acids in shortenings, trans fatty acids usually represent <5% of dairy and ruminant meat fats (9). Up until 2000, 80–90% of trans fatty acids in the diet in Canada and the United States was from partially hydrogenated fats; in the late 1990s about 50% of dietary trans fatty acids were consumed in bakery, snack, and fast food products, and about 10% were from table margarines (11,14).

Considerable evidence is available to show that the fatty acid composition of human milk is influenced by the trans, (n-6), and (n-3) fatty acid composition of the maternal diet (16–20). In addition, clinical studies that specifically alter trans fatty acid intake by lactating women have demonstrated that higher trans fat intake results in increased secretion of trans fatty acids in human milk (16,17). The fatty acids in human milk are of concern because human milk provides the fatty acids needed for growth and development of the breast-fed infant (20,21). High intake of trans fatty acids may have adverse effects during growth and development through inhibition of the desaturation of linoleic acid [18:2(n-6)] and {alpha} linolenic acid [18:3(n-3)] to arachidonic acid [ARA2, 20:4(n-6)] and docosahexaenoic acid [DHA, 22:6(n-3)], respectively, metabolism to unusual fatty acid isomers that are incorporated into membranes, effects on gene expression, or through loss of (n-6) and (n-3) fatty acids from the food supply (6,8,22–27). Previous studies by us and others in Canada and the United States have shown mean total trans fatty acid levels in human milk of about 7% total fatty acids, but levels as high as 18% in the milk of some women (18,19,28). In addition, levels of trans fatty acids in human milk are generally higher in North America than in Europe (11,18,19,28–31), probably reflecting the lower intake of trans fatty acids in Europe than in North America (15).

In 2003, Canada became the first country to introduce food labeling of the trans fatty acid content per serving on food labels of packaged foods; this food labeling became mandatory in the retail sector in December 2005 (32). Food industries and manufacturers in Canada responded to the concern over high amounts of trans fatty acids on human health, and partially hydrogenated fats have been replaced in many foods such as breads, cookies, crackers, and in frying, with fats and oils containing cis unsaturated and saturated fatty acids (33). The objective of this study was to determine whether the introduction of labeling of retail foods' trans fat content and removal or reduction of trans fatty acids from vegetable oils in many foods has been accompanied by a decline in the trans fat concentration of human milk (32,33). To achieve this, we analyzed mature human milk from 87 women giving birth to term infants following the introduction of trans fat labeling and compared the results to our previous studies conducted with milk collected from 103 women in 1998 and analyzed using identical methodology (19).


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Subjects. This study involved women (n = 87) who gave birth to full-term (37–41 wk) gestation, single-birth infants between October 2004 and December 2005 and who provided their own milk as the sole source of nutrition to their infants. The women in these studies are part of a larger cohort involving measures of infant development with the same inclusion and exclusion criteria as in our previous studies (19,34). All the women for whom breast milk samples were available were included in this study. These milk samples were compared to samples collected from 103 women in 1998 and analyzed similarly (19). The procedures and methods used in this study were reviewed and approved by the Committee for Ethical Review of Research Involving Human Subjects at the University of British Columbia and the British Columbia's Children's and Women's Hospital Research Coordinating Committee. Informed written consent was obtained from all the women who participated.

    Methods. Samples of breast milk (60–100 mL) were collected at 1-mo postpartum during the course of a feeding, at approximately the midpoint of the feeding, and stored at –70°C until analyzed (19). The milk samples were thawed in ice-cold water, directly transmethylated to avoid potential losses of medium-chain saturated fatty acids, and the fatty acid methyl esters separated and quantified by capillary GLC, as in our previous studies (19,34). For the purposes of this report, all fatty acids containing one or more trans unsaturated bonds in which all double bonds were methylene interrupted were grouped as trans fatty acids. Fatty acids in which one or more of the double bonds were conjugated were grouped and termed conjugated linoleic acids (CLA). As in our previous studies, we did not include specific analytical techniques to confirm the identity of specific trans 18:1 isomers, as reported by others (18,28); however, the {Delta} 9, 10, and 11 isomers, which are the major isomers in partially hydrogenated oils and dairy fats, were all well separated by our GLC methodology (19,34).

    Statistical analysis. The data were tested for normality then evaluated by ANOVA and Fisher's LSD test. Potential relations between the levels of total trans fatty acids and the saturated, and cis monounsaturated and (n-6) and (n-3) fatty acids was examined by using Pearson correlation analysis. A P-value ≤0.05 was considered significant. All statistical analyses were performed with the Statistical Package for the Social Sciences (version 7.5; SPSS).


   Results
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 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
The composition of the major saturated, cis (n-9) and (n-7) monounsaturated, (n-6), and (n-3) fatty acids, CLA, and total trans unsaturated fatty acids in human milk are shown in Table 1. The total trans fatty acid level in human milk in western Canada has decreased, such that the level in milk collected between September 2005 and January 2006 was 35% lower than that in milk collected in 1998 (P < 0.05). Whereas the mean concentration of total trans fatty acids was 7.1 g/100g, with a range of 2.2 to 18.7 g/100g fatty acids in the milk collected in 1998, the mean (range) for milk collected and analyzed in 3 consecutive 5-mo periods from November 2004 to January 2006 was 6.2 (3.4–13.7), 5.3 (3.0–14.5), and 4.6 (2.2–12.2) g/100g milk fatty acids. Figure 1 illustrates the mean level of trans fatty acids, and the 25th–75th percentile range and range of concentrations of trans fatty acids in the human samples. The decrease in the mean levels of trans fatty acids in human milk (Table 1) is explained by a downward shift in women with high amounts of trans fatty acids in their milk, such that the 75th percentile value in the last time period studied approached the mean in milk samples analyzed in 1998 (Figure 1). The level of cis monounsaturated or (n-6) or (n-3) polyunsaturated fatty acids did not differ among the sampling times, although the levels of 16:0 were higher and 18:0 and CLA were lower in milk collected between 2004 and 2006 than in samples collected in 1998 (Table 1).


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  		TABLE 1 Total trans fatty acids and major saturated and cis unsaturated fatty acids in human milk collected at different times1

 

Figure 1
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  		Figure 1  Trans fatty acid concentrations in human milk samples collected from women in 1998 (n = 103), 11–2004 to 03–2005 (n = 24), 04–2005 to 08–2005 (n = 24), and 09–2005 to 01–2006 (n = 39). The figure illustrates the mean, interquartile range, and range.

 
The results of the correlation analyses between the levels of total trans fatty acids and the levels of saturated and cis unsaturated fatty acids in milk using results for all samples (n = 96) are presented in Table 2. The levels of total trans fatty acids was significantly and inversely related to 16:0, cis 18:1(n-9), 18:2(n-6), 20:4(n-6), 22:4(n-6), 22:5(n-6), and 18:3(n-3). Milk total trans fatty acids were not associated with 20:5(n-3) (P = 0.32), 22:5(n-3) (P = 0.34), or 22:6(n-3) (P = 0.12) concentrations.


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  		TABLE 2 Pearson correlation coefficients for relations between trans fatty acids and specific saturated, monounsaturated, polyunsaturated fatty acids, and CLA in human milk1

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
Human milk is the sole source of nutrition for the exclusively breast-fed infant and provides all of the fatty acids needed for the infant's growth and development, including fatty acids for synthesis of membrane lipids and adipose tissue (18,19). The presence of high amounts of trans fatty acids in human milk has raised concern because of possible adverse effects on growth and development of the recipient breast-fed infant, particularly through interference with the metabolism of the essential (n-6) and (n-3) fatty acids (6,8,17). In addition, high intake of trans fatty acids by pregnant and lactating women could have adverse effects on lipoprotein metabolism and inflammatory mediators or (n-6) and (n-3) fatty acid metabolism in the mother, which may also impact transfer of ARA and DHA to the developing fetus and breast-fed infant (1–5,34,35). Previously, we reported a mean of 7.1 g total trans fatty acids/100 g in human milk fat in western Canada (19), similar to that recently reported for human milk collected in the United States between 1996 and 2002 (28) and also found by Chen et al. (18) in analyses of human milk collected from different regions of Canada prior to 2000. Using the equation generated by Craig-Schmidt et al. (17) to describe the relation between trans 18:1 in the milk and the maternal diet, Chen et al. (18) estimated trans fatty acid intakes were 3.9% of total energy, equivalent to 10.1 g/d, for Canadian women with mean total trans fatty acid levels of 6.9 g/100 g milk fatty acids. Similarly, applying the equation Y = 1.49 + 0.42X, where Y and X represent the percent of trans 18:1 in the milk and dietary fat, respectively, and assuming 30% dietary energy from fat in the women's diet (14,18), the estimated mean (range) of intake of trans fatty acids by women in the present study was 4.0 (0.51–12.32), 3.4 (1.36–8.72), 2.7 (1.07–9.29), and 2.2 (0.56–7.65) g · person–1 · d–1 for the women in our studies in 1998 and in the 3 consecutive 5-mo periods from November 2004 to January 2006, respectively.

A similar approach can be taken to estimate the exposure of breast-fed infants to trans fatty acids derived from the maternal diet. On average, mature human milk provides 37 g fat/L, with 50% of the energy in the milk as fat (18). Using the results in the present study, the mean and 95th percentile of intake (percent total energy intake) of breast-fed infants to trans fatty acids from human milk, estimated from the analyses of human milk and assuming an average intake of 780 mL/day of milk was 2.05 and 4.40 g/d (1.02 and 2.2%), 1.79 and 3.80 g/d (0.89 and 1.90%), 1.53 and 3.77 g/d (0.76 and 1.88%), and 1.33 and 2.41 g/d (0.66 and 1.21%), for milk samples analyzed in 1998 and the 3 5-mo periods beginning in November 2004. However, we note that because these estimates are based on the average fat content of human milk and the average milk intake of the fully breast-fed infant, individual intakes may be much different.

Fatty acids secreted in human milk are derived from synthesis in the mammary gland and by uptake from maternal plasma. Due to the mammary gland enzyme, thioesterase II, fatty acid synthesis in the mammary gland is terminated at the level of myristic acid (14:0) rather than palmitic acid (16:0), as in other tissues (18). Our results show that the total trans fatty acids in the milk (n = 187) was significantly and inversely associated with the levels of 16:0, and cis 18:1(n-9), 18:2(n-6), and 18:3(n-3) are consistent with the replacement of partially hydrogenated fats and oils in retail foods with unhydrogenated soybean and canola oils or more saturated fats, such as palm and palm kernel oil. Similarly, the positive association between 18:0 and trans fatty acids in milk shown in our study is not unexpected because 18:0 is higher in hydrogenated oils than in their unhydrogenated counterparts. The lower CLAs in human milk in late 2005 than in 1998 shown in the present study, however, may suggest that the intake of dietary fats derived from ruminant animals, which are also a source of trans fatty acids CLA and 18:0, may have decreased among women in our population. On the other hand, available estimates suggest that endogenous conversion of trans 11–18:1 (vaccenic acid) to cis 9, trans 11–18:2 (CLA) contributes ~25% of the CLA in humans (36), suggesting the lower CLA in human milk collected in 2005 than in 1998 may be explained at least in part by a lower intake of trans 11–18:1. In addition, ruminant meats and dairy fats contain 2–5% trans fatty acids (9) and contribute about 10% of the total dietary trans fatty acids/d (14). This suggests that a decrease in the intake of trans fatty acids from animal foods is not likely to explain the estimated 45% decrease in trans fat intake among breast-feeding women from 1998 to 2005 suggested by our studies. Consistent with our results, Mosley et al. (28) recently reported a positive relation between total trans fatty acids and 18:0, as well as CLA in human milk collected from women in the United States. Whether or not women with higher intake of ruminant fats are also those with higher intake of foods more likely to contain partially and fully hydrogenated vegetable oils cannot be determined from our data. The results of the present study also show a significant inverse association between trans fatty acids in human milk and the levels of ARA and its longer chain metabolites, 22:4(n-6) and 22:5(n-6). Several studies have raised concern that trans fatty acids may inhibit the desaturation of dietary linoleic acid and {alpha} linolenic acid, and evidence of an inverse association between ARA and trans fatty acids in maternal and newborn plasma has been reported (8,34). We found no evidence of an inverse relation between trans fatty acids and DHA in human milk. Whether these results are explained by differences in dietary intake or differences in the possible interactions between trans fatty acids and the (n-6) and (n-3) series of fatty acids is unclear.

In summary, our results show a decrease in trans fatty acids in human milk and provide evidence that the intake of trans fatty acids has decreased among women, particularly those women with higher intake of trans fatty acids, following the introduction of labeling of trans fat on foods sold at retail and the decrease in partially hydrogenated fats and oils in foods such as breads, snack foods, and fried foods in Canada (32,33). New food-labeling laws were also recently adopted in the United States (37). Our studies suggest that changes in the exposure to trans fatty acids derived from the industrial partial hydrogenation of vegetable oil has decreased in Canada. Future studies will need to address the possible benefits to human growth, development, and health.


   ACKNOWLEDGMENTS
 
We gratefully acknowledge the assistance of Carmen Neufeld in the enrollment of subjects in this study.


   FOOTNOTES
 
1 Supported by a grant from Canadian Institute of Health Research (CIHR). RF supported by the Molly Towell Perinatal Research Foundation. Back

2 Abbreviations used: ARA, arachidonic acid; CLA, conjugated linoleic acid; DHA, docosahexaenoic acid. Back

Manuscript received 12 April 2006. Initial review completed 10 June 2006. Revision accepted 6 July 2006.


   LITERATURE CITED
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 

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