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Addition of Pasture Plant Essential Oil in Milk: Influence on Chemical and Sensory Properties of Milk and Cheese

G. Tornambé^*,, A. Cornu^*,, I. Verdier-Metz, P. Pradel^#, N. Kondjoyan, G. Figueredo^||, S. Hulin^¶ and B. Martin^*,1

^* INRA, UR1213 Unité de Recherches sur les Herbivores, Theix, F-63122 Saint-Genès-Champanelle, France
Dipartimento S.En.Fi.Mi.Zo, Facoltà di Agraria, Universita degli Studi di Palermo, Palermo, Italy
INRA, UR370 Unité de Recherches sur la Qualité des Produits Animaux, Theix, F-63122 Saint-Genès-Champanelle, France
INRA, UR545 Unité de Recherches Fromagères, F-15000 Aurillac, France
^# INRA, UE373 Unité Expérimentale de Marcenat, F-15190 Marcenat, France
^|| Laboratoire de Chimie des Huiles Essentielles, Université Blaise Pascal, Les Ceseaux, F-63177 Aubière, France
^¶ Comité Interprofessionnel des Fromages du Cantal, F-15000 Aurillac, France

¹ Corresponding author: bmartin{at}clermont.inra.fr

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
The aim of this experiment was to study the effect of the addition, to milk, of an essential oil (EO) obtained from the hydrodistillation of plants collected from a mountain natural pasture on the milk and cheese sensory properties. The EO was mainly composed of terpenoid compounds (67 of the 95 compounds identified) as well as ketones, aldehydes, alcohols, esters, alkanes, and benzenic compounds. In milk, the addition of this EO at the concentration of 0.1 µL/L did not influence its sensory properties, whereas at 1.0 µL/L, sensory properties were modified. In cheeses, the effect of adding EO into milk was studied in an experimental dairy plant allowing the production of small Cantal-type cheeses (10 kg) in 3 vats processed in parallel. The control (C) vat contained 110 L of raw milk; in the other 2 vats, 0.1 µL/L (EO1) or 3.0 µL/L (EO30) of EO were added to 110 L of the same milk. Six replicates were performed. After 5 mo of ripening, chemical and sensory analyses were carried out on the cheeses, including determination of the volatile compounds by dynamic headspace combined with gas chromatography-mass spectrometry. The EO did not influence the sensory properties of the cheeses at the lower concentration (EO1). However, the EO30 cheeses had a more intense odor and aroma, both characterized as "mint/chlorophyll" and "thyme/oregano." These unusual odors and aromas originated directly from the EO added. In total, 152 compounds desorbing from cheese were found, of which 41 had been added with the EO; in contrast, 54 compounds of the EO were not recovered in the cheese. Few volatile compounds desorbing from cheeses, other than the added compounds, were affected by EO addition. Among them, 2-butanol, propanol, and 3-heptanone suggested a slight effect of the EO on lipid catabolism. The antimicrobial activity of terpenes is not or is only marginally involved in the explanation of the influence of the botanical composition of the meadows on the pressed cheeses sensory properties.

Key Words: terpene • sensory property • essential oil • volatile compound

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Several trials have been conducted in Europe in recent years to describe and analyze the effect of the botanical diversity of forages fed to animals on the sensory characteristics of various types of cheeses (Martin et al., 2005a). A specific interest was lent to this topic because the botanical composition of the meadows is partly linked to environmental conditions and is therefore an important component of "terroir," a notion at the basis of the Protected Denomination of Origin (PDO) labeling. Trials performed in summer when cows graze different highland meadows on French Beaufort or Abondance cheeses (Buchin et al., 1999; Martin et al., 2005b) or Swiss Gruyere cheese (Bosset et al., 1999) indeed showed differences in cheese sensory properties according to the botanical composition of meadows. Bugaud et al. (2001b) were able to describe some associations between the botanical composition of the meadows and the sensory features of Abondance cheeses.

To explain these links, the authors suggested some possible effects of fatty acids and plasmin that varied greatly from one situation to another (Bugaud et al., 2001a). Dumont and Adda (1978) also proposed that terpenes may play a role. These plant-specific molecules have recognizable aromatic properties when concentrated and are the major components of essential oils (EO). They abound in certain species, dicotyledons in particular, and terpene concentration in forage is mainly governed by its botanical composition: graminaceae-based forages are terpene-poor, whereas mountain-diversified pasture forages with a large number of dicotyledons including aromatic species are terpene-rich (Mariaca et al., 1997; Bugaud et al., 2001b; Cornu et al., 2001). These molecules very rapidly pass into the milk (Viallon et al., 2000) with some minor alterations and are found in cheese in much greater quantities when the animals are fed dicotyledon-rich natural grass forage compared with when they are fed concentrate-based rations (Moio et al., 1996) or monospecific forage (Bosset et al., 1999; Viallon et al., 1999; Carpino et al., 2004). However, it appears that changes in terpene concentration in cheese are not sufficient to exert any marked direct effect on cheese flavor (Moio et al., 1996; Verdier-Metz et al., 2000; Bugaud et al., 2001b). Nevertheless, because of their antimicrobial properties (Hammer et al., 1999; Burt, 2004), terpenes may have an indirect impact on cheese sensory properties by modifying the dynamics or the activity of the microbial ecosystem during cheese making and ripening. This hypothesis results from indirect observations in several trials on hard cooked cheeses (Buchin et al., 1999; Bugaud et al., 2001b; Martin et al., 2005b), in which the cheeses richest in terpenes had greater overall scores for milder flavors such as nutty or sweet, and lower scores for attributes such as animal, spicy, cabbage, toasted, fermented vegetable, acid, and pungent. These sensory differences could be related to differences observed in the volatiles desorbing from the cheeses: terpene content was negatively correlated to the presence of other volatile components obtained from the protein breakdown by microbial enzymes. Nevertheless, this indirect effect of terpenes on cheese sensory properties via a modification of the microbial development or activity has never been tested directly in specifically designed trials. Such was the aim of this experiment, in which we added various quantities of an EO obtained from the hydrodistillation of plants collected from a mountain natural pasture into milk before cheese making of Cantal-type cheeses.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
Grassland Botanical Composition and EO Extraction
Five times in 3 consecutive weeks in July 2003, fresh herbage was cut from one naturally diversified mountain grassland located in the Cantal area (France) at 1,100 m elevation. Forty-six plant species were identified in the plot, 14 poaceaes and 32 dicotyledons. Their relative contribution to the total number of plants was 44 and 56%, respectively. The main species identified and their relative contributions were Festuca rubra, 14.5%; Agrostis capillaris, 9.5%; Carex caryophyllea, 6.2%; Hieracium pilosella, 7.8%; Thymus pulegioides, 5.5%; Gentiana lutea, 5.0%; Stachys officinalis, 4.8%; Festuca nigrescens, 4.8%; Achillea millefolium, 4.2%; Helianthemum nummularium, 3.2%; Galium verum, 3.2%; Meum athamanticum, 2.7%; and Anthoxanthum odoratum, 2.5%. After each cutting, a rough removal of the poaceae plants was performed and the dicotyledon plants were kept in nylon vacuum bags and preserved at –18°C for 2 mo. The plant material was extracted by steam distillation in a Clevenger apparatus for 3 h. Eight successive runs with 2 kg of frozen plant material made it possible to obtain 15 mL of pooled EO.

The EO was analyzed using a gas chromatograph (model 6890 Hewlett-Packard, Agilent, SRA Instruments, Le Raincy, France) coupled to a mass spectrometer (model 5873, Hewlett-Packard) equipped with an HP5 column (30 m x 0.25 mm, film thickness, 0.25 µm) programmed from 50°C (5 min) to 300°C at 5°C/min, followed by a 5-min hold. The carrier gas was helium (1.1 mL/min); injection was set in the split mode (1/ 10). Injector and detector temperatures were 250 and 280°C, respectively. Ionization was by electron impact at 70 eV; electron multiplier was 2,200 V; and the ion source temperature was 230°C. Mass spectral data were acquired in the scan mode in the m/z range of 33 to 450.

Identification was carried out by calculating retention indices and comparing mass spectra with data banks published by Adams (1995) and McLafferty and Stauffer (1989). Peak areas were quantified as a percentage of the total ion count. Peaks contributing to the total area by more than 0.01% were identified.

Trial 1: Influence of EO Addition on the Milk Sensory Properties
The milk from the morning milking of 3 Holstein cows fed a maize (Zea mays L.) silage-based diet was collected twice, 2 d apart, for milk sensory analyses. On average, this milk contained 5.2% fat, 3.6% protein, 4.8% lactose, and 125,000 somatic cells/mL. The EO described previously was added to this milk (control, C) in 2 different concentrations: 0.1 µL/L (EO1) and 1.0 µL/L (EO10). Sensory evaluations, consisting of a triangular test, were conducted in a red light environment by a panel of 16 untrained assessors. The full-fat raw milk samples were served at room temperature (22°C). The test consisted of comparing C and EO1 milk and C and EO10 milk in 2 sessions. During each session 4 tests were performed, with the 2 comparisons being repeated to obtain 61 answers for each of the comparisons. For every test, 3 samples of milk (2 identical and 1 unique) were presented simultaneously to different assessors in 3 opaque white plastic glasses. Every assessor had to identify the unique sample from among the 3 and describe the magnitude of the differences perceived on a structured scale from 1 (very small) to 5 (very high). Results are expressed as a percentage of correct answers.

Trial 2: Influence of EO Addition on Chemical and Sensory Properties of Cheese
Animals.
Twenty-four cows (Montbéliarde n = 13 and Holstein n = 11) calving between November 15 and January 10 and producing, on average, 20.5 kg of milk/ d with 3.61% fat and 2.97% protein were used in this experiment. From March 15 until April 20, cows were fed a terpene-poor diet based on rye-grass silage fed ad libitum and 6 kg (DM)/cow per d of cocksfoot hay. This diet was completed with, on average, 5.9 kg (DM) of a commercial mixture based on cereals and soybean meal distributed individually according to each cow’s milk yield.

Cheese Making.
During the final 3 wk of the experiment, twice a week, the raw milk from the evening milking was stored at 4°C and pooled with the milk collected from the following morning’s milking. In total, 330 L of this milk was distributed into 3 vats. Each 200-L vat allowed the production of 1 small Cantal-type cheese (about 10 kg instead of 40 kg). Every cheese making day (6 in total), 3 vats were manufactured in parallel. One vat contained 110 L of full-fat raw milk (control), and the other 2 consisted of 110 L of the same milk with 0.1 (EO1) or 3.0 µL/L (EO30) of EO. Previous studies (A. Cornu, unpublished data) showed that the terpenes desorbing from milks obtained from cows fed a mountain-diversified hay were similar to those desorbing from milk with 1.0 µL/L of this EO added, which correspond to the EO1 samples of this experiment. In addition, previous work (A. Cornu, unpublished data) showed that the terpenes desorbing from milks obtained from cows fed a mountain-diversified pasture composed of 15% aromatic plants was similar to the terpenes desorbing from milk with 0.1 µL/L of this EO added. We have chosen the EO30 concentration to test an extreme situation. The total amount of terpenes desorbing from this milk was about 3 times greater than the total amount of terpenes desorbing naturally from milk obtained from cows fed a mountain-diversified pasture. Considering that the proportion of aromatic plants in the grassland may exceed 15%, particularly in Mediteranean grasslands, and that EO may be added in the cow’s diets to modify rumen microbial fermentations (Calsamiglia et al., 2007), we hypothesized that the EO30 concentration could be found in practice.

The EO was added just before cheese making after the milk had been heated to 33°C. Then, the milk was inoculated with 0.2 g of a lyophilized mesophilic starter culture (Flora Danica Direct, Chr. Hansen, Arpajon, France) reconstituted in sterile skimmed milk (100 g/ L) with a ripening starter (2 mL of Monilev and 1.5 mL of Penbac, Laboratoire Interprofessionnel de Production, Aurillac, France) and with 0.33 g/kg of rennet (Beaugel 500, Villefranche sur Saône, France) containing 520 mg of active chymosin/L. Forty-five minutes later, the curd was cut for 5 min to produce pellets 5 to 6 mm in diameter. The curd-whey mixture was then blended for 12 min and left to stand for 7 min. After draining the whey, the curd was placed in a pressing tray where it was pressed, cut in 15-cm cubes, and turned 12 times in approximately 3 h to reach 50% DM. After pressing, the curd cubes were left to drain for 24 h at 20°C and were pounded into grains 20 mm in diameter. The mixture was salted with 20 g/kg of dry salt and left to stand for 6 h at 20°C before 1 cheese per vat was formed in a cloth mold and pressed for 24 h at 13°C. The cheeses were placed in a ripening cellar for 5 mo at 10°C and 95% minimum relative humidity.

Milk Analyses.
pH (at 20°C) and protein, fat, and lactose contents (infrared method, Milkoscan 4000, Foss System, Hillerød, Denmark), SCC (Fossomatic 5000, Foss System; IDF, 1997), and butyric spore count were assessed in a representative sample of each vat. The FFA content of milk was measured by the copper soap method (Jellema, 1991).

The Cinac system (Ysebaert Dairy Division, Frepillon, France) was used to measure the acidification properties of the milk (Corrieu et al., 1989). pH measurements were taken every 10 min for 72 h as per dynamic and static (32°C) temperature kinetics. Dynamic kinetics reproduces the thermal cycle of Cantal cheese making: 10 min at 33°C, 35 min at 32°C, 30 min at 31°C, 3 h at 30°C, 13 h and 20 min at 22°C, 8 h at 20°C, 22 h and 20 min at 17°C, and 24 h at 13°C. The 3 milks (C, EO1, and EO30) were studied with the starters used for cheese making.

Cheese Analyses.
Dry matter content was determined by heating at 103°C for 24 h. The fat content of the cheeses was measured by using the butyrometric method (IDF, 1997). Total nitrogen, water-soluble nitrogen, and phosphotungstic-acid-soluble nitrogen were measured using the methods described by Ardö (1999).

All ripened cheeses were submitted to 12 trained assessors who scored the intensity of 38 attributes (7 for texture, 7 for flavor, 11 for odor, 13 for aroma) on a 0 (very low) to 7 (very high) structured scale. Two preliminary sensory test sessions were carried out by assessors using these experimental cheeses to define specific attributes for these cheeses.

For volatile compound analyses, wrapped cheese cuts were allowed to thaw overnight at room temperature before the bags were opened. Pieces of about 5 g were taken from the middle of the cuts and rapidly ground in a mortar with 10 g of anhydrous sodium sulfate. Five grams of the resulting powder was deposited on 0.15 g of glass wool in a cylindrical 40- x120-mm glass extraction cartridge (Ets Mallières Frères, Aubière, France). The volatile compounds were extracted by a dynamic heads-pace method with an automatic Tekmar LSC2000 system (Tekmar, Cincinnati, OH) under the following conditions: purge 30 min at room temperature (21°C) by a 65 mL/min helium flow, trap on Tenax, dry purge 3 min, desorb preheat 175°C, desorb 5 min at 180°C, and cryofocusing at –150°C in the gas-chromatograph inject port. The volatile compounds were separated using a gas chromatograph (model 5890, Hewlett Packard, Les Ulis, France, Agilent) and a Supelco capillary column (60 m x 0.32 mm, Supelco, Gland, Switzerland) coated with a 1-µm-thick SPB5 stationary phase. The injection port was heated for 2 min at 225°C, the carrier gas was helium at 1 mL/min, and the oven temperature program was 40°C for 5 min, increasing at 3°C/min up to 230°C, and held for 2 min. The volatile compounds were detected using a mass selective detector (model 5971A, Hewlett Packard, Agilent) operating at 70 eV electron impact. Identifications were proposed by comparing the experimental data to the published mass spectral (Wiley 275K, 1995; NIST/EPA/NIH, 1996) and retention index (Kondjoyan and Berdagué, 1996) databases. Integrations were performed for each component using a selected ion whose peak was not deformed by a coelution.

Data Analysis
The data were processed by ANOVA using the GLM procedure (version 6.12, SAS Institute, Inc., Cary, NC). For milk composition and acidification properties and for cheese composition and rheological properties, the statistical model included the effect of the treatment. For sensory data, the statistical model included the effect of the treatment, the assessor, and the treatment x assessor interaction. For the milk triangular test, we used the values from the table calculated as binomial law of parameter P = 1/3 with n repetitions (AFNOR, 1983).

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
EO Composition
Ninety-five volatile compounds, representing 75.4% of the total area, were identified in the EO (Table 1), with each of the remaining peaks accounting for less than 0.01%. The most abundant family was the terpenoid family with 14 monoterpenes, 24 monoterpene derivatives, 18 sesquiterpenes, and 11 sesquiterpene derivatives, together accounting for 61.1% of the total peak area. Beside terpenes, the 7 benzenic compounds identified account for 12% of the total peak area and are also commonly found in plant EO. The benzenic compounds dill apiole and carvacrol were the most abundant in the EO after the sesquiterpene germacrene D. The remaining compounds (1 ketone, 6 aldehydes, 4 alcohols, 3 esters, and 7 alkanes) accounted for 2.3%. The EO obtained from pasture plants contained the usual terpenes already encountered in pasture plants, milk, and cheese from the same region (Cornu et al., 2001, 2005; Tornambé et al., 2006).

Trial 2: Influence of EO Addition on Chemical and Sensory Properties of Cheese
Milk Properties.
The C, EO1, and EO30 milks used for cheese making had very similar fat, protein, and lactose contents, SCC, lipolysis, and spores of butyric acid bacteria (Table 2). The 3 milks also behaved similarly during acidification for the 2 temperature kinetics (Table 2). The latter result showed that even at the EO30 concentration, the acidification activity of the starters was not modified. In dairy products, the absence of influence of EO on microbial activity has not been reported previously. In other complex microbial ecosystems such as rumen fluid, some EO (e.g., cinnamon, anise, or garlic oils) have been shown to exert an influence on fermentation activities when added at concentrations (ranging from 0.2 to 2.0 mg/L) slightly lower than EO30 (Calsamiglia et al., 2007). Nevertheless, the main active compounds of the EO studied by Calsamiglia et al. (2007) were not identified in the EO tested in this study.

Sixty compounds were significantly affected by treatment. Among them, 40 had been added with the EO and logically were much greater in EO30 than in C (average enrichment of 270 from C to EO30 for compounds present in C). Thirty-one of these 40 compounds were not significantly greater in EO1 than in C, even though the average enrichment from C to EO1 was 10 (for compounds present in C). As is usually observed, the areas of the most important peaks exhibited large variation among cheeses. This variability was observed also for the compounds added with the EO at a high concentration (EO30). As a result, the statistical analysis failed to demonstrate any significant differences between the C and EO1 cheeses for 31 compounds. Indeed, the same statistical analysis performed on C and EO1 values alone (not shown) presented significant differences for the 19 added and recovered monoterpenoids.

The other 20 compounds significantly affected by the treatment had not been added with the EO or at least were not included in the 95 most important compounds of the EO. These included 11 terpenoids, 3 alcohols, 1 ketone, 1 ester, 1 hydrocarbon, and 3 unidentified compounds. Most of these compounds were present at significantly greater concentrations in EO30 than in C and EO1 and followed the pattern of the added compounds. These compounds may have resulted directly or indirectly from the addition of the EO. Nevertheless, propanol, 2-butanol, and 3-heptanone are particularly interesting because they did not follow the pattern of the added compounds. The concentration of propanol was greater and that of 3-heptanone lower in the EO1 than in the C or EO30 cheeses and the concentration of 2-butanol was greater in C than in EO1 and EO30. These products are produced from lipid catabolism resulting from the action of the native or microbial enzymes (Marilley and Casey, 2004). Callon et al. (2005) observed 2-butanol to be significantly affected by changes in the indigenous microflora such as the facultative heterofermentative lactobacilli population of the raw milk. Therefore, it can be hypothesized that the addition of EO slightly modified the metabolism of some lactobacilli. Nevertheless, this possible effect was subtle and did not influence the proteolysis or the flavor of the cheese. This slight influence of EO on the activity of cheese microflora has not previously been described in the literature. Because the EO used in this study contained a variety of compounds, it is not possible to identify the active compounds. Nevertheless, some of the most important compounds of the EO (e.g., thymol, carvacrol or terpinen-4-ol) have recognized antimicrobial properties (Calsamiglia et al., 2007) even if their activity, when added alone, in complex microbial ecosystems (i.e., in rumen) was shown only at concentrations greater than 50 mg/L, which is much greater than the maximum concentration tested in this study.

Our results suggest that the influence of the botanical composition of the forages fed to the animals on the sensory properties of Cantal type cheeses is not (or is only slightly) linked to the terpenes arising from consumption of aromatic plants. This result is not in accordance with those obtained by other authors (Buchin et al., 1999; Bugaud et al., 2001b) who observed negative correlations between cheese terpenes and alcohols, esters, and sulfur compounds resulting from the breakdown of sulfur amino acids by microbial enzymes. First, this discrepancy may be linked to the cheese model chosen in the present study, an uncooked pressed cheese, whereas the results suggesting an inhibitory action of terpenes on cheese microorganisms were obtained on semicooked or cooked cheeses. Second, the effect of EO addition is probably different from that of the plants grazed on the grassland. Indeed, the terpenes ingested by cows are known to have an influence on the rumen microflora: they affect, in particular, protein degradation and volatile fatty acid production (Calsamiglia et al., 2007), which may result in milk compositional changes due to the nutrient flow out of the rumen. In addition, other dicotyledonous plant compounds such as phenols are known to be partially transferred into the milk (Sakakibara et al., 2004). Those nonvolatile compounds were not addressed in this experiment. It would be interesting to investigate their possible involvement in the links between cheese sensory properties and pasture botanical composition.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
When EO was added at a concentration chosen so that the terpenes desorbing from milk correspond to the terpenes desorbing naturally from milk from cows fed a diversified hay (EO1), the EO seemed to be only marginally involved in the production of propanol, 2-butanol, and 3-heptanone from lipid catabolism by microorganisms. This effect had no consequence for cheese sensory properties. Even when EO was added at a much greater concentration chosen so that the terpenes desorbing from milk were greater than the maximum terpenes desorbing naturally from milk produced from cows fed a diversified pasture, the EO had a marginal influence on the production of volatile compounds by the microorganism activity. At those concentrations (1.0 and 3.0 µL/L), the great influence of EO on milk and cheese sensory properties is a direct effect of EO. It would be interesting to investigate the influence of intermediate concentrations of EO. Nevertheless, with the current results, we can conclude that a possible indirect influence of terpenes (via the antimicrobial activity of terpenes) is not, or is only marginally, involved in the explanation of the influence of the botanical composition of the meadows on the sensory properties of pressed cheeses.

	ACKNOWLEDGEMENTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 
We wish to thank all those who helped in this trial, particularly Isabelle Constant (INRA) and Olivier Troquier (INRA) for their technical assistance, René Lavigne (INRA) for the cheesemaking, and Hervé Dubroeucq (INRA) for milk triangular test organization.

Received for publication March 1, 2007. Accepted for publication September 7, 2007.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS ACKNOWLEDGEMENTS REFERENCES

 


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