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Influence of Starter Culture on Flavor and Headspace Volatile Profiles of Fermented Whey and Whey Produced from Fermented Milk

¹ Department of Food and Nutritional Sciences, University College Cork, Cork, Ireland
² Sensory Science Research Centre, Department of Food Science, University of Otago, Dunedin, New Zealand

Corresponding author. Alan L. Kelly; e-mail: a.kelly{at}ucc.ie.

	ABSTRACT

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

 
Rennet whey and skim milk were compared as media for fermentation by commercial cheese, yogurt, and probiotic starter cultures. Effect of culture, medium, and their interaction on flavor was assessed and compared by sensory descriptive analysis and headspace volatile analysis by proton transfer reaction-mass spectrometry. In general, the aroma of fermented whey was similar to that of whey separated from fermented milk, indicating a favorable possibility of substituting milk with whey in the manufacture of fermented milk-like beverages. Starter culture significantly affected most sensory characteristics of the products. Key volatile compounds for the characteristic flavor of yogurt, such as acetaldehyde and diacetyl, were not significantly affected by medium when fermented with the yogurt culture, and reached similar levels in both systems. Volatile analysis results were consistent with the results of the sensory evaluation, indicating the high reliability of proton transfer reaction-mass spectrometry in detecting important volatile compounds for aroma. Integration of this sensory and chemical information allows a better understanding of how flavor and related compounds are affected by ingredients or processing, which may be useful for the development of value-added whey products.

Key Words: fermented whey • yogurt aroma • descriptive sensory analysis • headspace volatile analysis

Abbreviation key: -ch = cheese starter culture, FRW = fermented rennet whey, -p = probiotic starter culture, PCA = principal components analysis, PLS = partial least squares, PTR-MS = proton transfer reaction-mass spectrometry, WFM = whey from fermented milk, -y = yogurt starter culture.

	INTRODUCTION

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

 
Considerable effort has been devoted over several decades to finding the least costly method of disposal of liquid whey and to identify new outlets for whey utilization, preventing the loss of potentially valuable nutrients and reducing environmental pollution (González-Martínez et al., 2002). Manufacture of beverages through lactic or alcoholic fermentations that can provide desirable sensory properties has been considered an option to add value to whey (Salminen et al., 1991; Skudra et al., 1998). Lactic fermentations of whey typically use conventional starter organisms or probiotic strains, whereas alcoholic fermentations commonly use Kluyveromyces yeast strains (Mawson, 2003).

Growth of the fermented milk sector represents an opportunity to advance the development of fermented milk-like products from liquid whey into products with interesting nutritional and sensory properties without requiring complicated or costly technology (Sienkiewicz and Riedel, 1990). However, despite the apparent simplicity in manufacturing whey beverages, product development requires extensive research to achieve a specific flavor profile (Jelen, 1992, 2003).

Fermented dairy products already have a positive health image (Jelen et al., 2003; Valli and Traill, 2005), which can be further enhanced by the addition of probiotic bacteria with therapeutic properties (Lourens-Hattingh and Viljoen, 2001). Growing worldwide popularity of this type of product can be also attributed to effective use of consumer-driven flavors and milder cultures (Jensen and Kroger, 2000).

Compared with fermented whey, much more is known about the origin of key flavor characteristics in yogurt. Volatile analysis of yogurt has shown that acetaldehyde is a key compound for typical yogurt aroma. In addition, research has shown that 2,3-butanedione (diacetyl), ethanol, 2-butanone, and acetone are also important (Ulberth and Kneifel, 1992; Marshall, 1993; Skriver et al., 2003). In a recent study, Ott et al. (2000) emphasized the importance of acidity and the balance (ratios) of more than 60 flavor compounds in the perception of yogurt flavor.

Research on the use of whey in fermented milk, and yogurt in particular, has largely focused on substitution of milk solids by whey solids to improve texture or reduce defects such as syneresis during storage (e.g., Modler and Kalab, 1983; González-Martínez et al., 2002). Few published reports have used sensory evaluation to develop fermented milk-like beverages from un-fractionated whey on its own or mixed with milk or yogurt (e.g., Macedo et al., 1999; Penna et al., 2003) or from whey permeate (El-Salam et al., 1991; Beucler et al., 2005). Although whey protein concentrates have been used in formulation of this type of beverage, fermentation of liquid whey represents a more economical alternative, because the costs of evaporation or ultrafiltration are eliminated (Ryder, 1980). However, information on the flavor of such products produced from liquid whey directly is scarce. Moreover, little is known with regard to the sensory influence of probiotic bacteria on the resulting fermented products (Baron et al., 2000; Østlie et al., 2003).

There is an indication that fermentation of whey using Lactobacillus delbrueckii ssp. bulgaricus and Streptococcus thermophilus produces a more intense yogurt flavor (especially when threonine, a possible precursor of acetaldehyde, is added to the whey) compared with that obtained when skim milk is fermented (van der Schaft, 1995). This suggests the possibility of producing beverages from whey with similar sensory profiles to those of fermented milk drinks or with some flavor attributes of drinking yogurt, following manufacturing procedures conventionally used for milk.

The objectives of this study were (a) to objectively compare the sensory and volatile compound profiles of milk and whey fermented by commercial yogurt, probiotic, and cheese starter cultures, and (b) to investigate the chemical compounds that may be responsible for flavor of the products. Commercial cultures (direct vat set-type) were studied to ensure relevance of the results to industrial scenarios.

	MATERIALS AND METHODS

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

 
Media
Pasteurized skim milk (CMP Dairies, Cork, Ireland) was divided into 2 portions. One portion was directly used as a medium of fermentation (to obtain whey from fermented milk; WFM), and the other portion was used to produce rennet whey, which was subsequently used as a second medium of fermentation (i.e., fermented rennet whey; FRW). Pasteurization complied with typical Irish commercial practices for that purpose (72 to 74 °C for 15 s).

To produce rennet whey, calf rennet (Std. 190; Chr. Hansen Ireland Ltd., Cork, Ireland) 0.04% (vol/vol) was added to skim milk preheated at 35°C, and left for 45 min until a coagulum was formed. The coagulum was cut with a knife and transferred to a preheated water bath until a temperature of 55°C was reached. The whey obtained was filtered through a cheese sieve, transferred to centrifuge bottles, centrifuged at 8000 x g for 30 min at 6°C, and filtered through Whatman No. 113 filter paper.

Cultures and Fermentation
Three different starter cultures from Chr. Hansen (Cork, Ireland) each at a level of 0.10% (vol/vol) were inoculated separately in each media. The cultures used were 1) a thermophilic lactic yogurt culture (YC-470) containing Streptococcus thermophilus and Lactobacillus delbrueckii ssp. bulgaricus, 2) a thermophilic lactic probiotic culture (ABT-6) containing Lactobacillus acidophilus LA-5, Bifidobacterium Bb12, and Streptococcus thermophilus, and 3) a mesophilic homofermentative cheese starter culture (phage-resistant) (R-604) containing Lactococcus lactis ssp. lactis and Lactococcus lactis ssp. cremoris. Incubation was performed at the recommended temperatures of 42, 40, and 38°C, respectively, for 2.5 to 4.5 h, depending on starter culture. For both media, fermentation was arrested at pH ~4.6 by pasteurization at 63°C for 30 min in a water bath.

For the milk medium, the gels formed after fermentation were cut manually by cutters (made of stainless steel wires stretched across a frame), transferred to centrifuge bottles, and centrifuged under the same conditions as for the rennet whey to separate the aqueous phase (whey), which was then filtered through Whatman No. 113 filter paper. All 6 samples (2 media x 3 cultures) were frozen at –20°C in polyethylene containers for a maximum of 14 d, before sensory and chemical analyses.

Sensory Evaluation
A panel of 9 highly trained assessors participated in the sensory evaluation of the samples under controlled conditions of lighting and environment according to international standards (Standard 8589; ISO, 1988). Assessors developed a descriptive vocabulary in four 2-h sessions (Table 1). Trial descriptive tests were carried out on selected samples, and panel reliability was verified by Kendall’s coefficient of concordance and ANOVA of trial data (McDonnell et al., 2001). For sensory evaluation, 30 mL of each sample at room temperature (~20°C) was presented to assessors in 3-digit-coded stemmed black glasses. To further mask potential visual differences between samples, yellow lighting was used. Samples were evaluated in triplicate on separate days, using a balanced order design (MacFie et al., 1989). On each day, 2 sessions were conducted, with a maximum of 4 samples per session. Unsalted crackers and water were given to assessors for palate cleansing between samples, and 15-min breaks between sessions were enforced to avoid sensory fatigue. Samples were evaluated using 100-mm unstructured line scales. Data were collected using Compusense-five version 4.0 (Compusense Inc., Guelph, Canada).

Mass spectra for each sample were obtained using a PTR-MS system and software (Ionicon Analytik GmbH, Innsbruck, Austria). The analytical procedure involved placing 50 mL of each sample in a 500-mL glass flask. After reaching headspace equilibrium at ~20°C (1 h), the inlet of the PTR-MS was connected by a polyethylene tube to the flask, and the headspace sample was drawn by a vacuum pump at 20.5 mL/min. The volatile concentration measurement was performed in duplicate on 2 consecutive days.

Data Analysis
The experimental design comprised of 2 fixed factors (starter culture and medium) for the sensory and chemical data sets and an additional random factor (assessors) for the sensory data set. Data were analyzed by 2-way ANOVA using SPSS version 13.0 (SPSS Inc., Chicago, IL).

Principal component analysis (PCA) on each set of data, standardized (1/SD) and cross-validated, and partial least squares (PLS) regression (Type 2, multiresponse) were performed using Unscrambler 9.1.2 (CAMO Process AS, Oslo, Norway). For PLS regression, the independent variables were the chemical compounds expressed as m/z ratios (predictors) and the dependent variables (response variables) were the sensory attributes. By plotting PLS components, it is possible to illustrate main associations between both sets of variables, and interrelationships within both sets of data.

	RESULTS AND DISCUSSION

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

 
Hereafter, samples will be denoted as WFM or FRW according to the medium of fermentation, followed by a suffix indicating the starter culture used (-y = yogurt culture, -p = probiotic culture, and -ch = cheese culture).

Sensory Evaluation
The mean scores of the sensory attributes perceived in each sample and the statistical significance of the effects of starter culture, medium, and their interaction on odor and flavor are shown in Table 2. In general, there was a larger effect of culture than media on odor and flavor of the samples, because 6 sensory characteristics were significantly affected by culture, in contrast with 3 attributes significantly affected by medium. The direction of these effects is more clearly seen through the multivariate analysis diagram (Figure 1) that is explained below. There was a significant interactive effect of culture and medium on "oaty" odor and "acid" flavor, indicating that starter cultures behaved differently in different media, with regard to reactions leading to these characteristics. The probiotic and yogurt cultures produced a slightly more intense "oaty" odor in FRW than in WFM, whereas the cheese culture produced a considerable increase in this characteristic for FRW. On the other hand, the probiotic and cheese cultures produced a slightly less or similarly intense "acid" flavor, respectively, in WFM than in FRW, whereas the yogurt culture produced a (perceptually) significantly less acid product in FRW.

View larger version (17K): [in this window] [in a new window]   Figure 1. Principal component analysis diagram of significant sensory attributes of the samples (cumulative variance explained = 89%). FRW = Fermented rennet whey; WFM = whey from fermented milk; -y = yogurt starter culture; -p = probiotic starter culture; -ch = cheese starter culture; o- = odor characteristics; f- = flavor characteristics.

The yogurt and probiotic culture samples (i.e., WFM-y, WFM-p, FRW-y, and FRW-p) produced higher sensory scores for yogurt odor compared with the cheese culture samples (WFM-ch and FRW-ch), as expected. The samples produced with the probiotic culture (WFM-p and FRW-p) had significantly higher intensity scores for "fruity" odor than those produced with the other 2 cultures. This characteristic may be related to a particular acetaldehyde:diacetyl ratio, as discussed later. Probiotic strains, like the one used in this research, normally contain Lactobacillus acidophilus to promote acid development, and are often mixed with Streptococcus thermophilus to achieve a desired flavor. Moreover, special probiotic cultures have been developed to bring out the preferred flavors in the products in which they are used (Saarela et al., 2000).

The samples obtained from fermentation by the cheese culture, regardless of medium, had significantly higher scores for "oaty" odor, "sweet" flavor, and "oaty" flavor than the rest of the samples. This "oaty" note may be related to Maillard reaction products based on the relationship found with thermally induced flavors (e.g., heated milk and caramelized milk) in a previous study on raw whey obtained from rennet casein manufacture (Gallardo-Escamilla et al., 2005).

All samples exhibited a "rancid" odor and flavor at similar (low) intensity levels. The term "rancid," as defined by the panel, encompassed an oxidized note probably generated because of heat treatment and exposure to air. Therefore, this sensory characteristic may be explained by the procedures followed to prepare the samples—heating of the curd to release rennet whey, "slow" pasteurization, handling of samples for centrifugation, and so on.

Overall, results showed that samples FRW-y and FRW-p compared favorably with WFM-y and WFM-p, respectively, with regard to aroma characteristics. On the other hand, the use of the cheese starter culture, regardless of the medium, did not seem to produce a dairy beverage with a desirable sensory profile, because the corresponding samples, especially FRW-ch, although having an oat-like odor note, in general, lacked flavor.

Headspace Volatile Analysis
Sixteen different ionized molecules detected by PTR-MS significantly discriminated between samples by at least one of the factors examined; these are expressed as mass to charge ratios (m/z) and attributed to specific volatile compounds based on previous work with chemical standards (Buhr et al., 2002) and yogurt (unpublished results). A tentative identification of compounds is shown in Table 3. Additional compounds were detected (e.g., m/z 105, attributed to methional), but their concentrations did not significantly differ between samples and therefore, were not included in subsequent statistical analysis. Concentration of individual compounds are expressed in parts per million. Unequivocal identification of compounds was not always possible as some isomeric compounds have been reported to be present in yogurt (Ott et al., 1997) and, although minimal, fragmentation of ions does occur (Buhr et al., 2002). Therefore, for some m/z ratios, several possible compounds were considered.

View larger version (17K): [in this window] [in a new window]   Figure 2. Principal component analysis diagram of the volatile compounds detected in the samples by proton transfer reaction-mass spectrometry (cumulative variance explained = 70%). Numbers refer to ions (m/z ratios) attributed to chemical compounds. FRW = Fermented rennet whey; WFM = whey from fermented milk; -y = yogurt starter culture; -p = probiotic starter culture; -ch = cheese starter culture. For clarity, only significant volatile compounds are shown.

Thus, concentrations of m/z 45 and 87 (attributed to acetaldehyde and diacetyl, respectively) in the experimental samples (FRW-y and WFM-y) were at a level considered normal when a yogurt culture is used, and did not differ significantly (as an effect of the medium) between each product. Headspace analysis results obtained were therefore consistent with the results of the sensory evaluation.

An important chemical compound for yogurt odor seemed to be that of m/z 101, attributed to 2,3 pentanedione, because concentrations higher than 0.07 ppm of this compound were found in the samples inoculated with the yogurt culture. Attribution of this volatile compound was based on its previous identification in yogurt (Ott et al., 1997), but other isomers such as hexanal or 2-hexanone, which elicit "fruity" and "nutty" flavors, respectively (Yannai, 2004), could also be attributed to this ion.

Streptococcus thermophilus, a bacterium present both in the probiotic and yogurt culture used, produces diacetyl, acetoin (3-hydroxy-2-butanone), and acetaldehyde; however, acetaldehyde is produced to a lesser extent compared with the amount normally produced by Lactobacillus delbrueckii ssp. bulgaricus, which was present only in the yogurt culture (Marshall and Tamime, 1997; Lourens-Hattingh and Viljoen, 2001). This may explain some of the differences observed when comparing the effect of the yogurt culture with that of the probiotic culture on flavor in both media. The "fruity" odor perceived in the samples with the probiotic culture appeared to be influenced by the ratio of concentrations of diacetyl (1.2 ppm in FRW-p and 1.3 ppm in WFM-p), acetaldehyde (3.1 ppm in FRW-p and 3.5 ppm in WFM-p), and 3-heptanone (0.02 ppm in FRW-p), because the latter compound elicits a "fruity" odor (Yannai, 2004). Acetaldehyde may be described as "fruity," and diacetyl has been reported to be important in enhancing dairy flavors (Eaton, 1994), as discussed earlier. In addition, the vinegar note perceived when the probiotic starter culture was used may be explained by the fact that bifidobacteria can produce acetic and lactic acids (Shah, 2003).

With regard to the "oaty" odor perceived in FRW-ch, the only chemical compound detected in this study and reported in the literature with that sensory description is butanal, attributed (as an isomer) to m/z 73 (Law, 1982; Burdock, 2002; Yannai, 2004). However, based on the PCA diagram, it appeared that the lack of compounds rather than the presence of a single compound responsible for this note might explain the perception of this characteristic. Zhow et al. (2000) suggested that the nut-like flavor associated with oat products could be related to products of thermal degradation of lactose; for example, furfural, furfuryl alcohol, or pentyl furan, as stated by Tamime and Robinson (2000).

Relationship Between Volatile Chemical Compounds and Sensory Attributes
Partial least squares regression was used in an attempt to model the complex interactions and relative contribution of chemical compounds important for eliciting odor characteristics, as shown in Figure 3. This plot accounted for 64% of the explained variance in the regression model of the chemical and sensory variables in the first 2 PLS factors. Although not constituting a cause-and-effect model, this revealed high validation coefficients (i.e., predictive ability >0.8) for a number of chemical compounds.

View larger version (23K): [in this window] [in a new window]   Figure 3. Partial least squares (PLS) regression diagram showing the relationships between the sensory (response variables) and chemical data (predictor variables). Lines represent ion (m/z ratios) loadings (i.e., chemical compounds related to the sensory characteristics). FRW = Fermented rennet whey; WFM = whey from fermented milk; -y = yogurt starter culture; -p = probiotic starter culture; -ch = cheese starter culture. Only significant volatile compounds are shown.

	CONCLUSIONS

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

 
The potential for use of whey as a medium for manufacturing products with a sensory profile similar to that of fermented milk beverages was demonstrated by the results of this study. For example, there was no evidence that, when using the yogurt culture, the medium of fermentation (whey or milk) significantly affected aroma; apparently, the only major difference produced was related to the intensity of acid flavor.

Levels of key volatile flavor compounds such as acetaldehyde and diacetyl (attributed to specific masses) were not significantly affected by fermentation medium and exceeded threshold recognition levels in all cases. In addition to previously reported odor volatile compounds of yogurt, results indicated that 2,3 pentanedione and 2-butanone seemed to be significant for eliciting yogurt odor, whereas 3-hydroxy-2-butanone, 2,3 butanedione, and 3-heptanone appeared to be important for "fruity" odor in the products fermented using a probiotic culture, thus contributing to a better understanding of how flavor can be affected by the presence of critical compounds.

Probiotic strains such as those tested in this study produced products with mild acid notes (mean sensory scores of ~25 in the 100-mm line scale) and "fruity" and "yogurt" flavor characteristics. However, a potential problem in manufacturing beverages containing probiotic bacteria could be the production of acetic acid, which may impart an unpleasant vinegar odor.

Diverse strains of starter cultures may be combined and investigated further to suit individual preferences, as it was clear that choice of culture was the factor that had the greatest influence on flavor compared with effects of fermentation medium or their interaction.

	ACKNOWLEDGEMENTS

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

 
F. J. Gallardo-Escamilla gratefully acknowledges a Ph.D. studentship from Consejo Nacional de Ciencia y Tecnología (CONACyT) and postgraduate leave from Universidad Autonoma Metropolitana, Mexico.

Received for publication May 31, 2005. Accepted for publication August 1, 2005.

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

 


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