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(Circulation. 2004;109:103-107.)
© 2004 American Heart Association, Inc.

Basic Science Reports

High -3 Fatty Acid Content in Alpine Cheese

The Basis for an Alpine Paradox

Christa B. Hauswirth, MD; Martin R.L. Scheeder, Dr sg agr; Jürg H. Beer, MD

From the Department of Medicine, Kantonsspital Baden, and the Federal Institute of Technology, Zürich, Switzerland.

Correspondence to J.H. Beer, MD, Department of Medicine, Kantonsspital Baden, 5404 Baden, Switzerland. E-mail hansjuerg.beer{at}ksb.ch

Received June 17, 2003; revision received August 21, 2003; accepted August 22, 2003.

	Abstract

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Background— -Linolenic acid (ALA) may protect from cardiovascular disease. Because fresh alpine grass contains high amounts of ALA, we hypothesized that the levels of -3 fatty acids would concentrate to nutritional relevance in the cheese of milk from cows with alpine grass feeding compared with cheese from silage and concentrate feeding; the newly available cheese produced from cows fed with linseed supplementation should contain even higher ALA concentrations.

Methods and Results— Forty different cheeses were analyzed by gas chromatography for their fatty acid profile: (1) 12 from well-defined alpine regions around Gstaad, Switzerland; (2) 7 commercially available English cheddar cheeses; (3) 6 cheeses from cows fed with linseed supplementation; (4) 7 industrial-type Emmentals; and (5) 8 alpine cheeses with partial silage feeding. The alpine cheese contained 4 times more linolenic acid (C18:3-3) compared with cheddar, more total -3 fatty acids, and showed a significantly lower n-6:-3 ratio. Conjugated linoleic acid (C18:2 c9/t11) was 3-fold higher, whereas the amount of palmitic acid was 20% lower. The Emmental reached 40% of the ALA content compared with alpine cheese, and surprisingly, cheese from linseed-supplemented cows contained only 49% of that of the alpine cheese (P<0.001 for each trait in the 5 cheese groups).

Conclusions— Cheese made of milk from cows grazed on alpine pastures had a more favorable fatty acid profile than all other cheese types. Alpine cheese may be a relevant source of ALA and other cardioprotective fatty acids.

Key Words: nutrition • fatty acids • coronary disease • diet • death, sudden

	Introduction

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Regular consumption of cold-water fish, and thus of the long-chain -3 fatty acids (FAs) eicosapentaenoic acid (EPA) and the docosahexapentaenoic acid (DHA), substantially lowers the incidence of sudden death, myocardial infarction, stroke, and overall mortality.^1–5 Given the exposure to mercury, which may attenuate the beneficial effects,⁶ and the exhaustion of the natural fishery resources, nonmarine sources of -3 FAs are of increasing interest. -Linolenic acid (C18:n3; ALA) may be a key candidate because it is plant derived and because a diet rich in ALA appears to be protective in the primary and secondary prevention of fatal cardiovascular events.^7–11 The minimal amount required is a subject of debate. According to the 2003 guidelines of the American Heart Association, an intake of 1.5 to 3 g/d seems to be beneficial.¹² The protective effects seem to be dose dependent; in fact, the Nurses’ Health Study suggested a relative risk reduction of sudden cardiac death as high as 45% with a dietary daily intake of 1.36 g ALA.⁹ Diets containing a relatively high ALA content are therefore of considerable epidemiological importance, and substitution of low- by high-ALA components in our nutrition is desirable.

Beneficial cardiovascular effects have long been (paradoxically) attributed to the dairy products of certain alpine regions. Preliminary data indeed suggested variably and mildly increased levels of ALA in alpine grass and in some milk and blood samples from cows grazed on these alpine pastures.¹³ Therefore, ALA might naturally concentrate up to nutritionally important levels or to cardioprotective relevance in the alpine cheese.

We hypothesized that cheese from these regions might contain increased concentrations of ALA (compared with cheese from silage or concentrate feeding). The secondary aim was to measure the content of other FAs that are of special nutritional interest, such as conjugated linoleic acid (CLA), arachidonic acid (AA), and/or the ratio of n-6:-3 FAs, and not least, the amount of saturated fat, particularly of palmitic acid. Because several companies currently try to increase the ALA content of dairy products by adding linseed supplements to the feed of cattle, we also wanted to directly compare the ALA content of the "natural" alpine cheese with a commercially available "high–-3" product. The Swiss (and the French) are among the first consumers of cheeses in the world. Despite their intake of fat, they have a paradoxically low mortality from cardiovascular disease. A beneficial FA pattern of the alpine cheese might explain in part a "Swiss (alpine) paradox" in analogy to the French paradox.

	Methods

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The following cheese samples were analyzed: (1) 12 samples of Swiss alpine cheese from Gstaad, produced from milk of exclusively grass-fed cows at 3700 to 6200 feet above sea level, were provided directly by the local farmers. Every piece of cheese could be tracked back to a well-defined area of production; (2) 7 samples of commercially available English cheddar cheese; (3) 6 samples of commercially available Swiss cheese from cows with declared (and advertised) linseed-supplemented feeding; (4) 8 samples of Swiss alpine cheese from the (same) Gstaad region with partial silage feeding; and (5) 7 samples of industrially produced Emmental-type cheese.

All cheese samples were analyzed in duplicate. The FAs were converted into FA methyl esters (FAMEs) and separated on a CP-sil 88 (100 mx0.25 mm, 0.2 µm; Varian Inc) column. Triundecanin was used as internal standard, and BCR-164, the European Union milk fat standard, served as reference.

Statistical Analysis
Probability values were determined by the nonparametric Kruskal-Wallis test for the comparison of the 5 cheese groups. If significant (P<0.05), post hoc tests based on Wilcoxon rank sum tests were applied with correction for the multiple testing. (The patterns of the significant groups are given for each variable in Table 2.)

View this table: [in this window] [in a new window]   TABLE 2. Patterns of Significance Between Groups

	Results

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The data obtained are summarized in Tables 1 and 2 and illustrated in Figure 1; they strongly support our hypothesis and indicate a highly significant, severalfold higher level of ALA as well as of the total -3 FA in the alpine cheese compared with the cheddar cheese. Interestingly, the alpine cheese also contained significantly more EPA and showed a favorable n-6:-3 FA ratio and in particular, a low AA:EPA ratio (Tables 1 and 2). The content of CLA (the C18:2 cis-9, trans-11 isomer) is significantly higher, whereas the percentage of saturated FA is massively reduced; eg, palmitic acid is lower by 20% compared with the cheddar cheese. It is surprising and somewhat disappointing that the linseed supplementation resulted in a cheese that contained only 49% of the ALA concentration of the alpine samples, ie, in the range of industrially produced Emmental (which contains 40%). Interestingly, the alpine cheese produced with partial silage feeding still reaches 62% of the ALA content of the alpine cheese with exclusive pasture feeding. Each of the 8 traits given in Table 1 is significantly different between the 5 cheese groups (P<0.001 for all but for AA:EPA which is P=0.015).

View this table: [in this window] [in a new window]   TABLE 1. Fatty Acid Profile

View larger version (37K): [in this window] [in a new window]   Figure 1. Superior FA profile of alpine cheese as box plots. Box gives median value and 25th to 75th percentiles; T bar illustrates largest/smallest observed value that is not an outlier. Circles indicate single values that are >1.5 box lengths from 75th percentiles (outliers). There are no values >3 box lengths from 75th percentiles (extremes). A, Linolenic acid: there is a continuous decline of ALA concentration (mg/100 g cheese) from alpine cheese with pasture grass feeding only (Alpine) to alpine cheese with partial silage feeding (Alpine-S) to cheese of milk from cows fed with linseed supplementation (LS) to industrial Emmental and to cheddar. Similar patterns are observed in B for EPA (mg/100 g cheese), C for total -3 polyunsaturated FA content, and E for CLA (% FAME), whereas D indicates a steady increase of n-6/-3 ratio, and F documents continuous increase of content of palmitic acid (% FAME).

The separation of the (C18:1) trans isomers on the CP-Sil 88 column revealed that the alpine cheese contained more than twice the amount of C18:1 trans-isomers (6.5±0.6 g/100g FAME) compared with the cheddar cheese (3.0±0.9 g/100g FAME), of which the by far predominant proportion was trans-vaccenic acid. Trans-vaccenic acid can be converted into CLA by -9-desaturase in the mammary gland (as well as in the human liver). This important pathway is illustrated in Figure 2.

View larger version (19K): [in this window] [in a new window]   Figure 2. Proposed pathway of formation of CLA and long-chain -3 polyunsaturated FA from ALA: during biohydrogenation of ALA in rumen, trans-vaccenic acid is formed, which can be desaturated to CLA endogenously. Part of dietary ALA may escape microbial biohydrogenation in rumen and can be incorporated into body lipids or secreted with milk fat. It can also be transformed to EPA and DHA by endogenous chain elongation, 5 and 6 desaturation and, in DHA, by ß-oxidation of C24:6 -3.

	Discussion

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The evidence for the cardioprotective effects of ALA comes from epidemiological data,^7–11 basic science studies, and animal models^14–17: the Lyon Diet Heart Study and the Indo-Mediterranean Diet Heart Study, 2 secondary prevention trials for coronary artery disease by a nutritional intervention, demonstrated a significant reduction of cardiovascular deaths, and this effect was ascribed primarily to the cardioprotective effects of increased intake of ALA.^7,9 Indeed, ALA has been shown to slow the heart rhythm,¹⁷ to reduce the beating rate of isolated rat cardiac myocytes,^14,15 and to suppress arrhythmias.^16,17 These findings are well in accordance with data of the Nurses Health Study,⁹ in which the dietary intake of ALA correlated with a reduced risk of fatal cardiac disease, in particular sudden death. The risk appears to decrease dose-dependently, and an intake of 1.36 g of ALA (fifth quintile) impressively reduced the relative risk for cardiac death to 0.55 (compared with an intake of 0.71 g in the first quintile).⁹ The average consumption of 55 g of cheese per day by a Western population¹⁸ could provide 272 mg of ALA if consumed as alpine cheese but only 62 mg if ingested as cheddar. This means that an additional 210 mg of ALA may be added to the daily intake by simply changing the type of cheese (ie, without changing the eating habits). The extrapolation of the relative risk in the Nurses Health Study indicates that 210 mg of ALA will reduce the relative risk of a fatal myocardial infarction by 15% to 20%. The estimate is strengthened by the fact that the total fat intake remains stable and that several other FAs are positively altered (see below). The median ALA intake of 11 258 Americans was 1.1 g/d, with a wide variability (10%/90% percentiles: 0.6/2.1 g¹⁹); the "cheese-switch" as described would provide an additional 20% of ALA on top of the daily consumption. Alpine cheese could therefore constitute a relevant ALA-containing nutritional component, together with the other sources of ALA, such as nonhydrogenated vegetable oils, walnuts, beans, broccoli, and green leafy vegetables. Interestingly, the linseed-supplemented feeding of the cows appears to result in a higher ALA content than in cheddar but, disappointingly, reaches only 50% of the levels of the alpine cheese.

Several other aspects of the lipid composition observed in alpine cheese deserve attention.

The ratio of n-6 to -3 FA is more favorable in the alpine samples (Table 1), and this is important because the uptake of ALA is influenced by the linoleic acid (LA) content in the food: a high ratio will reduce the uptake of ALA. ALA (-3) competes with LA (n-6) for chain elongation to EPA (for -3 FA) or to AA (for n-6 FA) by the same enzymatic machinery,²⁰ and the efficiency of the conversion seems to be in the range of 10%,^20–23 which is well in accordance with our data: the content of EPA in the alpine and in cheddar cheese is 10% of the ALA concentration and is (as analyzed by its absolute contents) significantly higher in the alpine cheese.

If LA (n-6) is the predominant substrate for chain elongation, the result is an increased production of AA and the proinflammatory eicosanoids, eg, its vasoconstrictor and platelet-activating metabolite thromboxane. The ratio of ALA to LA in human plasma and blood cell membranes is 1:100,²⁴ but because the enzymes involved in FA chain elongation and desaturation have much higher affinities for ALA, even minimal dietary increases in ALA intake might result in a relevant incorporation into membranes and tissue. The clinical importance of these findings is supported by the recent data of Baylin et al,²⁵ who demonstrated that the content of adipose-tissue ALA and nonfatal myocardial infarction were inversely correlated. Furthermore, the diet-dependent incorporation into red cells and the effect on blood FA composition in humans has been shown for linolenic acid and CLA.²⁶ CLA (see Figure 1E) is >2.5-fold higher in the alpine samples than in the cheddar. Anticarcinogenic properties of CLA have been known since 1985 from in vitro studies and animal models.^27,28 CLA was found to have antiatherosclerotic and antidiabetic effects in animal models^29,30; it increases lean body mass³¹ and reduces body fat,³² which lead to its application for weight loss in humans. It indeed reduced abdominal fat in middle-aged men.³³ Negative consequences such as insulin resistance and elevated C-reactive protein levels have been attributed to the t10c12 isomer,^34,35 which (surprisingly) is found in the synthetic CLA supplementations, whereas the predominant form in cheese is the (beneficial) c9,t11 isomer (Figure 2). Two reasons account for this predominance: (1) the consumed young alpine flora with the increased dicotyledonous species found at this altitude instead of grass³⁶ and (2) the presence of the anaerobic bacterium Butyrinvibrio fibrisolvens in the rumen, which converts ALA and -LA into vaccenic and rumenic acid (CLA c9,t11,³⁷ as illustrated in Figure 2).

The content of trans-FAs is a matter of concern,³⁸ because they may increase cardiovascular risk; however, the trans-FA predominantly present in cheese is trans-vaccenic acid (C18:1 trans-11), and interestingly, a recent study has not been able to show an association of this FA in biopsies of adipose tissue and the incidence of myocardial infarction.³⁹

Both trans-vaccenic acid and CLA are directly or indirectly derived from biohydrogenation of polyunsaturated FA in the rumen. This indicates that the dietary supply of -3 FA of the cows achieved by grass feeding positively alters the FA profile of the cheese, which may not be achieved by the exclusive fortification with -3 FAs.

Saturated fats consumed in cheese are, of course, a matter of concern; again, alpine cheese had a lower proportion of saturated fats, in particular, a reduced proportion of palmitic acid by 20% compared with cheddar cheese.

These qualitative differences call for a careful analysis of the cheese types consumed.

We conclude that alpine cheese contains a lipid pattern that is rich in ALA and more favorable than that of industrially produced cheeses from the lowlands (based on concentrate and silage feeding) than previously thought. Surprisingly, it is even superior to cheese produced from milk of cows fed with -3–rich supplements, and it may explain in part a "Swiss alpine paradox." It seems to be of utmost importance how and where the cattle are kept and fed. Therefore, the study may have agricultural impacts.

Further studies will be needed to analyze the impact of the consumption of alpine cheese on inflammation and platelet function.

	Acknowledgments

 
This work was supported in part by a grant from the Swiss National Foundation for Science (32-59449.99), a grant from the Swiss Foundation for Nutrition Research, and a grant from the Federal Institute of Technology/ISFE. We thank Prof Dr Jürg Hüsler, University of Bern, Switzerland, for statistical analysis, Dr vet Hans Hauswirth, Gstaad, Switzerland, for valuable advice, and Karin and Gisela Zehnder for outstanding secretarial assistance.

	Footnotes

 
Presented in part at the Scientific Sessions of the American Society of Cardiology, Chicago, Ill, November 17–20, 2002, and at the Swiss Society of Internal Medicine Meeting, Basel, Switzerland, May 21–23, 2003, and published in abstract form (Circulation. 2002;106[suppl II]:II-741, and Swiss Med Forum. 2003:[suppl 12]:24S).

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This Article Abstract Full Text (PDF) All Versions of this Article: 109/1/103    most recent 01.CIR.0000105989.74749.DDv1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hauswirth, C. B. Articles by Beer, J. H. Search for Related Content PubMed PubMed Citation Articles by Hauswirth, C. B. Articles by Beer, J. H. Pubmed/NCBI databases Compound via MeSH Substance via MeSH Medline Plus Health Information Dietary Fats Related Collections Nutrition Risk Factors