J. Dairy Sci. 88:1311-1319
© American Dairy Science Association, 2005.
Seasonal Variation in Conjugated Linoleic Acid and Vaccenic Acid in Milk Fat of Sheep and its Transfer to Cheese and Ricotta
A. Nudda1,
M. A. McGuire2,
G. Battacone1 and
G. Pulina1
1 Dipartimento di Scienze Zootecniche, Università degli Studi di Sassari, Via Enrico De Nicola 9, 07100 Sassari, Italy
2 Department of Animal and Veterinary Science, University of Idaho, Moscow 83844-2330
Corresponding author: Giuseppe Pulina; e-mail: gpulina{at}uniss.it.
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ABSTRACT
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The seasonal variation in conjugated linoleic acid (CLA) and vaccenic acid (VA) concentrations in sheep dairy products and the extent of their transfer from milk fat to cheese and ricotta fat were investigated. Samples were collected from 2 sheep milk processing plants in North Sardinia (Italy) every 2 wk from March through June. Concentrations of fatty acids (FA) in fresh cheese and ricotta fat were primarily dependent on the fatty acid content of the unprocessed raw milk. The content of c9,t11-CLA averaged 1.73, 1.69, and 1.75 mg/100 mg of FA methyl esters (FAME), respectively, for milk, cheese, and ricotta, and differed significantly between cheese and ricotta. The content of VA averaged 3.40, 3.33, and 3.43 mg/100 mg of FAME, respectively for milk, cheese, and ricotta. The FA composition of dairy products was markedly affected by period of sampling: the mean c9,t11-CLA and VA concentration decreased from March (2.20 and 4.52 mg/100 mg of FAME) to June (1.14 and 1.76 mg/100 mg of FAME) in all dairy products. No differences in c9,t11-CLA and VA concentration of dairy products were observed between the 2 dairy companies obtaining milk from the same geographical origin. The seasonal changes in CLA and VA in milk fat were probably related to changes in pasture quality.
Key Words: conjugated linoleic acid • sheep • milk • cheese
Abbreviation key: CLA = conjugated linoleic acid, FA = fatty acids, FAME = fatty acid methyl esters, VA = vaccenic acid.
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INTRODUCTION
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Studies in laboratory animals demonstrate that conjugated linoleic acid (CLA) has potential anticarcinogenic, immunomodulating, and antiatherosclerotic effects (McGuire and McGuire, 2000; Belury, 2002). Estimates of daily intake of CLA in humans range in different countries from 0.015 to 1 g (McGuire et al., 1999; Ritzenthaler et al., 2001). These amounts are lower than those indicated to provide anticarcinogenic effect in laboratory animals (Ip et al., 1994). Ruminant dairy products are the major dietary sources of CLA, and the isomer c9,t11 is approximately 80 to 90% of the CLA in milk fat (Parodi, 1999). This isomer is produced as an intermediate during the rumen biohydrogenation of linoleic acid that leads to t11-C18:1 (vaccenic acid; VA), and finally to stearic acid (C18:0). During rumen biohydrogenation of linolenic acid, VA, but no CLA is formed (Bauman et al., 2000). The major portion of CLA (from 64 to 98%) in milk fat is produced in the mammary gland by 
9-desaturase from VA (Griinari et al., 2000; Corl et al., 2001; Piperova et al., 2002; Kay et al., 2004). A conversion of ingested VA into CLA in tissues has been recently observed in laboratory animals (Santora et al., 2000) and humans (Adlof et al., 2000). This further pathway of bioconversion produces CLA with the same anticarcinogenic activity of direct dietary CLA (Banni et al., 2001).
Variation in CLA content in milk of cattle and sheep has been associated with several factors such as stage of lactation, parity (Kelly et al., 1998), and breed (Secchiari et al., 2001; White et al., 2001). However, diet is the most important factor influencing milk CLA concentration (Bauman and Griinari, 2000; Chilliard et al., 2000a; Collomb et al., 2002). In particular, the CLA concentration is higher in milk from animals fed pasture than those fed dry diets (Dhiman et al., 1999; Cabiddu et al., 2001) and decreases with increasing growth stage of forage or maturity (Chouinard et al., 1998). Such a relevant effect of the diet could be partly responsible for the higher milk CLA content in sheep in comparison with cow (Banni et al., 1996). In fact, the typical semiextensive farming systems of dairy sheep in Mediterranean countries are based mainly on pasture, in which quantitative and qualitative availability is greatly influenced by environmental factors.
Some surveys reported a higher concentration of CLA in the fat of cheese than in the fat of milk (Ha et al., 1989; Banni and Martin, 1998; Prandini et al., 2001). However, the relationship between CLA concentration of unprocessed milk and the derived dairy products has not been investigated. This point could have great relevance to the dairy sheep industry where almost all milk is processed into cheese. In Italy, some 790,000 tonnes of sheep milk are processed to produce 95,200 tonnes of cheese (FAOSTAT, 2003). Pecorino Romano cheese, largely exported to the United States (about 20,000 tonnes per year), is the most popular product (Bencini and Pulina, 1997).
The main aim of the present study was to evaluate the extent of transfer of CLA and VA from ovine milk to cheese and ricotta. The seasonal variation of CLA and VA in sheep milk and dairy products was also investigated.
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MATERIALS AND METHODS
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Bulk tank milk, fresh Pecorino Romano cheese (24 h), and ricotta obtained from the same milk were sampled from 2 milk processing plants located in North Sardinia (Italy) every 2 wk from March to June (48 total samples). Pecorino Romano was manufactured according to the process of Protected Denomination of Origin (PDO) Regulatory Board (1995). Briefly, raw or pasteurized (68°C for 15 s) whole sheep milk was inoculated with a natural microbial culture (thermophilic lactic acid bacteria) and then coagulated at 38 to 40°C using lamb rennet paste; after cutting the coagulum into rice-sized grains, the curd was cooked at 45 to 48°C. After removal from the vats, the curd was placed into cylindrical perforated molds and pressed to facilitate whey drainage. The ricotta was obtained from the whole whey after the curd extraction. The whey was heated to 80°C, which induced coagulation of whey proteins that float to the surface; then the coagulum was skimmed from the surface and loaded into perforated molds to drain for 4 to 6 h below 8°C.
Fat content was analyzed according to Gerber method for milk and the Gerber-Van Gulik method (ISO, 1975) for cheese and ricotta. Total protein (N x 6.38) was determined by the Kjeldahl method. Milk, cheese, and ricotta fat extraction was performed according to the Röse-Gottlieb method (AOAC, 1990) modified as described by Secchiari et al. (2003). Briefly, ammonia 25% (0.4 mL), ethyl alcohol 95% (1 mL), and hexane (5 mL) were added to 1 g of sample. Samples were centrifuged at 3000 rpm and the upper layer was collected. The extraction was repeated a second time using ethyl alcohol 95% (1 mL) and hexane (5 mL); samples were centrifuged at 3000 rpm and the upper layer was collected. A third extraction was repeated using 5 mL of hexane; samples were centrifuged at 3000 rpm and the upper layer was collected. The fatty acid methyl esters (FAME) were prepared with a base-catalyzed transesterification according to the FIL-IDF standard procedure (1999). Briefly, approximately 25 mg of lipid extract was mixed with 0.1 mL of 2 N methanolic KOH and 1 mL of hexane containing the internal standard (0.5 mg/mL), vortexed for 2 min, and then centrifuged at 3000 rpm for 1 min. After addition of 0.08 g of sodium hydrogensulfate monohydrate, the samples were centrifuged at 3000 rpm for 3 min and the supernatant was used for gas chromatography. The FAME were separated on a capillary column (CP-select CB for Fame; 100 m x 0.32 mm i.d., 0.25-µm film thickness, Varian Inc., Palo Alto, CA), and quantified using nonadecanoic acid (C19:0) methyl ester (Sigma Chemical Co., St. Louis, MO) as an internal standard. The injector and flame ionization detector temperatures were 255°C. The programmed temperature was 75°C for 1 min, increased to 165°C at a rate of 8°C/min, maintained at 165°C for 35 min, increased to 210°C at a rate of 5.5°C/ min, and then to 240°C at a rate of 15°C/min. The split ratio was 1:40 and helium was the carrier gas with a pressure of 37 psi. Individual FAME were identified by comparison with the relative retention time of FAME peaks from samples, with the standards mixture 37 Component FAME Mix (Supelco, Bellefonte, PA). The standards PUFA-2, nonconjugated 18:2 isomer mixture, individual cis-5,8,11,14,17 C20:5, cis-4,7,10,13,16,19 C22:6 (Supelco), cis-6,9,12 C18:3, and cis-9,12,15 C18:3 (Matreya Inc., Pleasant Gap, PA) were used to identify polyunsaturated fatty acids. High purity individual CLA c9,t11 and t10,c12 (Matreya Inc.) were used to identify the CLA isomers of interest. Additional standard CLA c9c11, t9t11, 11–13 (77% c,t; 2% c,c; 6% t,t) (Matreya Inc.), CLA mix standard (Sigma Chemical Co.), and published isomeric profile (Kramer et al., 2004) were used to help identify the CLA isomers in ovine milk. Individual t9 C18:1, t11 C18:1, t12C18:1, t13 C18:1 (Supelco) and published isomeric profile (Griinari et al., 1998) were used to identify trans C18:1 isomers of interest. The content of each FAME was expressed as weight percentage of total FAME present.
Fatty acid data were analyzed by ANOVA using sampling period and product type as fixed factors and processing plant as random factor. The ratios [c9,t11 CLA]/ [c9,t11 CLA+VA] and [C14:1]/[C14:1+C14:0] were calculated for milk samples as an indirect measurement of 9-desaturase activity.
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RESULTS AND DISCUSSION
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Means (± SE) of fat and true protein concentration were 6.16% (± 0.26) and 5.42% (± 0.03) in milk, 28.81% (± 0.65) and 21.17% (± 0.54) in cheese, and 14.29% (± 0.90) and 12.12% (± 0.60) in ricotta, respectively. The values of moisture were 47% (± 0.01) in the fresh cheese and 70% (± 0.01) in ricotta. A chromatogram of the CLA region for a sample of bulk milk is shown in Figure 1
. Differences from chromatograms reported by Kramer et al. (2004) for dairy cows could be ascribed to feeding regimen and analytical conditions. Fatty acid composition in fat of milk, cheese, and ricotta is reported in Table 1. Overall, the fatty acid (FA) profile of dairy products reflects the FA composition of raw milk used for cheese making (Table 1). The mean c9,t11 CLA values were higher than those reported for cattle (Lin et al., 1995) and goat (Prandini et al., 2001) cheese, and for short-aging sheep cheese (mean 0.74 g/100 g of fat) (Zlatanos et al., 2002). Some authors found that CLA content of cheese fat varied with processing temperature (Shantha et al., 1992) and was higher in cheese with a long aging time (Ha et al., 1989; Zlatanos et al., 2002). In addition, seasonal and nutritional influences related to the time of sampling might explain differences observed in the different trials. The content of t10,c12 CLA in milk was low (0.04 mg/100 mg of FAME) in accordance with other observations in sheep (Antongiovanni et al., 2004) and cows (Baumgard et al., 2000). No significant differences between milk and cheese, and milk and ricotta were found for any fatty acid. On the other hand, compared with cheese, ricotta showed a higher content (P < 0.05) of some long-chain fatty acids, including c9,t11 CLA. This result agreed with those of Banni et al. (1996) who observed higher content of CLA in ricotta than in cheese. The content of C16:1, c9 C18:1, c9,c12 C18:2, and C18:3n-3 was higher in ricotta than in cheese. Ricotta is obtained from heating (to 80 to 85°C) the whey obtained after the curd extraction in cheese process, and its major protein fraction is ß-lacto-globulin. The linkage between long-chain fatty acid with ß-lactoglobulin (Pérez and Calvo, 1995) should exert a protection of fatty acid against isomerization and oxidation reactions during ricotta processing (Banni and Martin, 1998). In addition, Shantha et al. (1992) reported an increase in CLA formation during processing with temperatures above 80°C. The contents of C20:5 and C22:6 in milk were extremely low and did not vary in cheese and ricotta.
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Figure 1. A partial gas chromatogram of the conjugated linoleic acid (CLA) region in bulk milk fat of dairy sheep.
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The sampling period influenced all fatty acids reported (Table 1
). Temporal evolution of c9,t11 CLA and VA concentrations in fat of milk and dairy products decreased (P < 0.05) throughout the sampling period (Figure 2). The c9,t11 CLA content declined from 2.20 to 1.14 and VA declined from 4.52 to 1.76 (mg/100 mg of FAME) from March to June. Highest contents of CLA and VA in milk and dairy products were observed when animals grazed fresh pastures, in agreement with previous reports for dairy cattle fed on pastures (Kelly et al., 1998; Dhiman et al., 1999; Ward et al., 2003; Kay et al., 2004). The content of t10,c12 CLA followed the same pattern of c9,t11 CLA and VA and decreased from 0.044 to 0.020 (mg/100 mg of FAME) from March to June (data not presented).
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Figure 2. Seasonal evolution of c9, t11-CLA and t11-C18:1 [mg/100 mg of fatty acid methyl esters (FAME)] in sheep milk, cheese, and ricotta sampled every 2 wk from March to June in 2 milk processing plants in North Sardinia. Different letters indicate significant differences (P < 0.05) between the sampling periods.
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A possible explanation for fatty acids patterns can be found in the variation of animal diet during the survey period, particularly in the progressive variation of fatty acid profile as grass matured. In fact, the productive cycle of Sarda sheep is synchronized with the quantitative and qualitative availability of pastures (Macciotta et al., 1999). The main fatty acid in grass lipids is 
-linolenic acid (C18:3) that decreases, both in absolute and relative values, as grass matures (Chilliard et al., 2000b; Nudda et al., 2003). Such a decrease of C18:3 could have resulted in a decrease of VA produced in the rumen by biohydrogenation (Bauman et al., 2000) and, consequently, in a reduction of CLA that is mostly synthesized in the mammary gland from VA by 9-desaturase (Kay et al., 2004). It is also possible that something in green grass enhances the growth of the particular bacteria in the rumen that are responsible for producing CLA or blocks the final reduction of VA to C18:0. The temporal evolution of short- and medium-chain fatty acids (from C6:0 to C14:0) and of C18:3 content in milk reflects those of CLA and VA.
Other FA responded in the opposite direction. Concentrations of C16:0, C18:0, and c9 C18:1 increased (P < 0.05) throughout the sampling period in milk and dairy products. The content of C16:0 in milk originates both from de novo synthesis in the mammary gland and from uptake from arterial blood (Bauman and Davis, 1974). In the current work, the pattern of C16:0 might be due to an increased uptake of preformed fatty acids, because the FA that are synthesized entirely de novo by the mammary gland (C8-C14) followed the opposite trend (data not presented).
Only the pattern of linolenic acid (Figure 3) and palmitic acid (Figure 4) are reported to show the typical evolution followed by the FA mentioned previously. No differences between the cheese processing plants were observed for CLA (1.73 and 1.72 ± 0.013) and VA (3.37 and 3.41 ± 0.036 mg/100 mg of FAME) concentrations (± SE) of milk and dairy products, probably because the milk used to make these products originated from the same geographic location.
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Figure 3. Seasonal evolution of C18:3n-3 [mg/100 mg of fatty acid methyl esters (FAME)] in sheep milk, cheese, and ricotta sampled every 2 wk from March to June in 2 milk processing plants located in North Sardinia. Different letters indicate significant differences (P < 0.05) between the sampling periods.
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Figure 4. Seasonal evolution of C16:0 [mg/100 mg of fatty acid methyl esters (FAME)] in sheep milk, cheese, and ricotta sampled every 2 wk from March to June in 2 milk processing plants located in North Sardinia. Different letters indicate significant differences (P < 0.05) between the sampling periods.
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A strong relationship between c9,t11 CLA and VA was found in milk samples (Figure 5), which is consistent with a predominant origin of this CLA isomer in the mammary gland from VA via 9-desaturase (Bauman et al., 2000). The high value of determination coefficient observed in this study can be due to the use of bulk milk samples, which reduces the high individual variation among and within animals in CLA content (Kelly et al., 1998; White et al., 2001). The ratios [c9,t11 CLA]/[c9,t11 CLA+VA] and [C14:1]/[C14:1+C14:0] in milk samples, as an indirect index of 9-desaturase activity (Kelsey et al., 2003), increased as lactation progressed (Figure 6). The drop in pasture quality after spring and the reduction of polyunsaturated fatty acids content as grass matured might, in part, explain the increase of these ratios as lactation progressed. The polyunsaturated fatty acids content in various tissues has been found to reduce the expression of 9-desaturase (Sessler and Ntambi, 1998). A slight increase in desaturase index with increasing DIM has been reported in cows by Kelsey et al. (2003) using individual data of animals fed a TMR. Therefore, effects related to physiological state of animals could influence the extent of 9-desaturase activity.
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Figure 5. Relationship between c9,t11-conjugated linoleic acid (CLA) and t11-C18:1 in bulk sheep milk sampled every 2 wk from March to June in 2 milk processing plants located in North Sardinia (SE: intercept = 0.059; slope = 0.019).
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Figure 6. Temporal evolution [c9,t11 conjugated linoleic acid (CLA)]/[c9,t11-CLA + t11-C18:1] and [C14:1]/[C14:1 + C14:0] ratios in bulk sheep milk sampled every 2 wk from March to June in 2 milk processing plants located in North Sardinia.
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CONCLUSIONS
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The results of this survey showed that CLA and VA concentrations in fresh cheese and ricotta fat were primarily dependent on the fatty acid content of the unprocessed raw milk. The CLA and VA concentrations in milk fat decreased as lactation progressed and consequently in fat of dairy products, probably due to variation in pasture availability and fatty acid composition of grass lipid. These results highlighted the important role of sheep dairy products as a natural source of CLA and VA.
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ACKNOWLEDGEMENTS
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This research was funded by the National Project of Ministero delle Politiche Agricole e Forestali (MiPAF, Italy). The authors thank M. Graziano Usai for precious assistance in laboratory analyses, and Cooperativa Lait Ittiri and Cooperativa San Pasquale Nulvi for providing samples.
Received for publication August 27, 2004.
Accepted for publication November 29, 2004.
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ABSTRACT
INTRODUCTION
