JFS M: Food Microbiology and Safety

Effects of Inulin and Oligofructose on the Rheological Characteristics and Probiotic Culture Survival in Low-Fat Probiotic Ice Cream
ABSTRACT: The effects of supplementation of oligofructose or inulin on the rheological characteristics and survival of Lactobacillus acidophilus La-5 and Bifidobacterium animalis Bb-12 in low-fat ice cream stored at –18 ◦ C for 90 d were studied. Addition of oligofructose or inulin to ice cream mix significantly increased apparent viscosity and overrun and developed the melting properties in ice cream during storage (P < 0.05). However, the highest increase in firmness, the lowest change in melting properties, and the longest 1st dripping time were obtained in probiotic ice cream containing inulin (P < 0.05). Some textural properties have also improved especially by the end of storage. Freezing process caused a significant decrease in the viability of Lactobacillus acidophilus La-5 and Bifidobacterium animalis Bb-12 (P < 0.05). Oligofructose significantly improved the viability of L. acidophilus La-5 and B. animalis Bb-12 in ice cream mix (P < 0.05). Although the viable numbers for both bacteria decreased throughout the storage, the minimum level of 106 CFU/g was maintained for B. animalis Bb-12 in only ice cream with oligofructose during storage. Keywords: Bifidobacterium animalis Bb-12, inulin, Lactobacillus acidophilus La-5, low-fat ice cream, oligofructose

M: Food Microbiology & Safety

airy products with incorporated probiotic bacteria are gaining popularity and the probiotics comprise approximately 65% of the world functional food market (Agrawal 2005). The species of bacteria most commonly used in dairy products for probiotic effect are Lactobacillus and Bifidobacterium (Saxelin and others 2005). Standards requiring a minimum of 106 to 107 CFU/g of Lactobacillus acidophilus and/or bifidobacteria in fermented dairy products have been introduced by several food organizations worldwide (Shah 2000). Therefore, it is important to ensure a high survival rate of these bacteria during the product shelf life to maintain consumer confidence in probiotic products (Saxelin and others 1999). Ice cream seems suitable for delivering probiotics in human diet because of its pleasant taste and attractive texture. However, in order to ensure that the product provides an adequate content of microorganisms, cells must survive in freezing and frozen storage. Freezing and thawing cause various degrees of damage to cells, including microorganism death, inhibition of its development, reduction, or interruption of metabolic activity (Davies and Obafemi 1985). Recent studies have focused on the survival of probiotic bacteria in ice cream produced by different techniques such as culturing ice cream mix (Hekmat and McMahon 1992; Davidson and others 2000; Akın 2005; Favaro-Trindade and others 2006), nonfermented ice cream mix (Alamprese and others 2002; Haynes and Playne 2002), or adding fermented milk to regular ice cream mix (Christiansen and others 1996; Hagen and Narvhus 1999). Nondi-

gestible food ingredients or prebiotics that selectively stimulate growth and/or activity of probiotic bacteria have been used to increase the viability of probiotic bacteria in dairy products. On the other hand, by decreasing the fat content in frozen dairy product formulations, quality characteristics on body and texture are affected (Ohmes and others 1998). In this respect, inulin and oligofructose, the best-known prebiotics and also fat replacers, possess several functional and nutritional properties that may be used to formulate innovative healthy foods for today’s consumer. Inulin is a term applied to a heterogeneous blend of fructose polymers found widely distributed in nature as plant storage carbohydrates. It has a degree of polymerization (DP) of 2 to 60. Oligofructose is a subgroup of inulin, consisting of polymers within a DP ≤ 10. Both inulin and oligofructose are widely used in functional foods throughout the world (Sangeetha and others 2005). Their structure is similar to corn sweeteners, principal carbohydrates used in ice cream technology. Classed as fat replacers, inulin and oligofructose influence the bulk and mouthfeel of the products. Also they are resistant to hydrolysis in both the stomach and small intestine, and are classified as dietary fiber ingredients (Spiegel and others 1994; Niness 1999). The main uses of inulin and oligofructose are as texturizing agents, particularly in low-fat foods such as ice cream (Devereux and others 2003). Some studies have been reported on the functionality of inulin as a fat replacer in reduced fat ice cream (SchallerPovolny and Smith 2001), in yog-ice cream (El-Nagar and others 2002), and in fat-free starch-based dairy dessert (Tarrega and Costell 2006). However, no research has been reported on both functional and prebiotic effects of inulin and oligofructose as a food MS 20070590 Submitted 7/27/2007, Accepted 2/7/2008. Authors are with Ege ingredient in low-fat probiotic ice cream. Thus, our objective was to Univ., Faculty of Agriculture, Dept. of Dairy Technology, 35100, Bornova, compare the effects of inulin or oligofructose supplementation esIzmir, Turkey. Direct inquiries to author Akalın (E-mail: sakalin21@ pecially on the survival of probiotic starter culture and also the rheyahoo.com). ological characteristics of low-fat probiotic ice cream. In addition,




JOURNAL OF FOOD SCIENCE—Vol. 73, Nr. 4, 2008

C 2008 Institute of Food Technologists doi: 10.1111/j.1750-3841.2008.00728.x

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and then placed in a hardening room at –18 ◦ C. Stoughton.tiansen and others 1996). and 4% (w/w) inulin for probiotic ice cream the samples.Probiotic culture survival in ice cream . stabilizer–emulsifier was calculated by dividing the conical spindle weight (91. Turkey). 12% (w/w) milk solids nonfat. and freeze-dried DVS starter cultures of Lactobacillus fore the measurements were taken. placing the ice cream onto 1-mm stainless steel screen over a cup. degree of polymerization < 20) (Cosucra AS. termined by a Surberlin PNR 6 Penetrometer (Sommer Runge KG.). Bel. Copenhagen. 4. . 100 mg/L. 2008—JOURNAL OF FOOD SCIENCE M185 M: Food Microbiology & Safety . Overrun% = (weight of ice cream mix) – (weight of ice cream) we aimed to compare the rheological characteristics of regular low× 100 × (weight of ice cream)−1 (Marshall and others 2003). after cooling to 40 ◦ C. and Duncan’s multiple range test was as follows: Vol. Results were multiplied by RV viscometer factor (2000/N . (αδ )ik . Mixes were frozen in random order using free gas mixture of anaerobic jars (Merck). Germany) incubated aerobically at 37 ◦ C for 72 h.conducted 4 cm from the side of each cup and were repeated twice. neomycin sulphate. with 9 mL of sterile 0. 200 mg/L) was preferred at pH 5. 0. Nazilli. . δk . Firmness of ice cream was deEge Univ.βj(i) + δk + (αδ )ik + εi jk where µ. Filter sterilized NNLP was added to the autoclaved MRS base The fermented mixes were then cooled in an ice bath to 5 ◦ C. Agricultural Faculty. Calif.the subunit treatment. The model equation was Yi jk = µ + αi + mined with N /10 natrium hydroxide in the presence of phenolph. and fermented for approx. Faculty of Agriculture.of treatments in a completely randomized block design to deterples for 3.Enumeration of probiotic bacteria trose Equivalent corn syrup for regular ice cream (R) and probiotic The count of viable probiotic bacteria was determined after agice cream (P).65% (w/w) stabilizer/emulsifier. sent overall mean effect. Menemen Research Farm (Izmir.. 4% (w/w) 42 Dex. molecular weight: properties. and experimental error. Overrun was measured with a comparison of the weight of ice respectively. cow’s milk was supplied from N = 20 rpm) and given as Pa. In the production of ice cream. The counts of L. β j (i ) . Denmark). and then during the storage days of oligofructose (PO).0 program. Denmark). (Christhe regular sample (R). depth of penetration (mm). Firmness was measured as the depth (in mm) of penetration of conOther ingredients for low-fat ice cream mix included sucrose and ical spindle into the ice cream and then a firmness index (g/mm) corn syrup (G-40) (Cargill. and εi jk reprethalein and expressed as percent lactic acid. milk trode (Beckman Zeromatic SS-3. Plates containing 25 to a batch ice cream freezer (4 L capacity. g (× 0. Fuller. acidophilus La-5 and B. molecular weight: 3300. 12 were obtained from Chr. Univ.1% (w/v) peptone water (Oxoid. agar. ˙ Istanbul. MRS-NNLP (nalidixic acid. was evaluated on ice cream samples stored at –18 ◦ C. of Ege. acidophilus pasteurized at 68 ◦ C for 30 min. One gram of probiotic ice cream sample was diluted with inulin (PI). and oligofructose (Fibrulose F97..La-5 were enumerated on MRS agar (Merck. Apparent viscosities of the mixes were evaluated at 4 ◦ C after Materials and Methods 24 h aging using a Brookfield RV Viscometer fitted with spindle no:5 at 20 rpm (Brookfield Engineering Laboratories. and days of storage were ton.6 fat milk powder was supplied from Pınar Dairy Industry (Izmir. 50-mL plastic cups (as 25 g for melting behavior). For the storage exthe Gerber method (AOAC 1990). animalis Bb-12 was enumerated acproximately 108 CFU/g. Beckman Instruments Inc.Melting properties were determined by carefully cutting the plastic gium). Mass. (Hoersholm.domized complete block design.5 regarding overall acceptance by judges. The experiment was conducted in Statistical analysis triplicate. effect of milk treatment i.cording to the method of Lankaputhra and others (1996) using imately 4 h at 40 ◦ C until the desired pH of 5. lactis Bb.A. U. BeTurkey).was also determined (Christiansen and others 1996). Nr. mixed well.. αi .. cups from the ice cream samples (preweighed as 25 g). Subsecans.3%) except for stadt. 4% (w/w) oligofructose for probiotic ice cream with ing of the mix for 24 h at 4 ◦ C. Mix formu. and weighManufacture of ice cream ing the amount of ice cream drained into the cup over a 90-min All ice creams were manufactured in the pilot plant of Dairy period at 20 ± 0. Turkey). Raw milk and cream were weighed into stainless steel milk Hampshire. B. Basingstoke. The formula for overrun is the SPSS Win 9.) and mixed uniformly with a vortex mixer. L.). effect of storage time k.5 h at 100 ◦ C and fat contents were analyzed by means of mine whether significant differences existed.Berlin. Rheological analyses milk treatment by storage time interaction.5 ◦ C. Ingredients and formulation for ice cream U. and non. All dry ingredients were mixed into the cold liquid ingre. Fontenoy. U˘ gur.K. expressed as 1st dripping time and melting ization > 20). Hansen Lab. inulin (Fibruline XL.A.5 was reached. Penetrations of a conical spindle weighing 91. 13% (w/w) sucrose. The pH values of ice cream sam. The titratable acidity in ice cream was deter. 73. 3 mg/L and paramomycin sulphate. just before pouring (Laroia and Martin 1991). the set of data was conducted as a split plot in a ranples were measured with a pH-meter combined with a glass elec. Darmimalis Bb-12 cultures were added to the mixes (0. an. The ice cream was packaged into 150-mL plastic cups and forming units (CFU)/g of sample. to achieve ap. Data were analyzed using the general linear model procedure of cream mixture before and after freezing.quent serial dilutions were made and viable cell numbers enumerdients and complete incorporation was ensured. The time for the 1st drop of melted ice cream Technology Dept. Germany). lation was 4% (w/w) milk fat. Each experiment was independently replicated 3 times and all analysis and enumerations were done in duplicate. fat ice cream and probiotic ice cream. 15 mg/L. degree of polymerMelting behavior. The inoculated plates All mixes were aged at 4 ◦ C for 24 h to ensure complete hydra. KGaA 64271.S. Each replication was a block. 1000.. random effect of block j receiving milk treatment i. pasteurized cream containing 35% milk fat.S. Analysis of variCompositional analyses ance for each set of data was conducted as a factorial arrangement Total solids in the ice cream was determined by drying the sam. Turkey) for 250 colonies were enumerated and recorded as logarithm of colony 35 min. The mixes were ated using the pour plate technique.periment.s. U.1 mm) to ice cream at –18 ◦ C were measured after 5 s. penetrations of the probe were acidophilus La-5 and Bifidobacterium animalis subs.treatment was the main unit treatment. Hekmat and McMahon (1992) reported that probiotic ice cream lithium chloride.were incubated anaerobically at 37 ◦ C for 72 h using an oxygen tion of all ingredients.6 g) to the mixture of Cremodan SE 30 (Danisco AS.

Inulin.05) (Figure 1).01b 0.76 ± 0. inulin is less soluble than oligofructose and has the ability to form inulin microcrystals when sheared in water or milk. 4.17a 5.1 ± 0. Alamprese and others (2002) also reported that Lactobacillus johnsonii La1 addition did not modify the overrun of ice cream.01c 3. As expected. In addition.1 ± 0.01 5.51 ± 0.02a 33.05) (Table 1).04d a Fat (%) 4.14 ± 0. acidophilus La-5 and B.90 ± 0. 2008 C M: Food Microbiology & Safety Figure 1 --.01b 0.s) 1. the ability of inulin to bind water molecules and form a particle gel network can improve the firmness of the product (Franck 2002).0 ± 0. the times prolonged in all samples as storage time increased while the .6 ± 1.01 0. High apparent viscosity in the probiotic ice cream mix containing oligofructose or inulin can be explained by the interactions of the dietary fiber and liquid components of the probiotic ice cream mix.05a b Ice cream Total solids (%) 33. a.04 33.90 ± 0.1a 4.05). inulin increased the 1st dripping time more than oligofructose. significantly higher apparent viscosity was obtained by replacing 100% of the 42 DE corn syrup with inulin in a reduced fat ice cream mix (Schaller-Povolny and Smith 2001).05).05) while similar lactic acid contents and pH values were determined in all probiotic ice creams (P > 0. respectively. However.05).s (P < 0.42 ± 0.05). P = probiotic ice cream. being highly hygroscopic.05) except for the 60th day for the P sample. P = probiotic mix or ice cream. There were significant differences in viscosities among all mixes. PI = probiotic mix or ice cream with inulin.6 ± 2.52 ± 0. cream.90 ± 0. The authors reported that higher apparent viscosity resulted from the higher molecular weight of inulin and that a potential interaction between the inulin and milk proteins could also be present in the system. R = regular ice cream.91 ± 0.38 ± 0.01.7 ± 1. used to compare means when the effect was significant (P < 0. However.0 2. Regular ice cream sample had a mean pH value of 6.47 ± 0.05).05a a Apparent viscosity (Pa. including probiotic ice cream mixes. The error bars represent the standard deviation (n = 3).00 5. Nr. statistical significance was given in terms of P values. PO = probiotic ice cream with oligofructose.17a b Overrun (%) 23.06a 5.05). ice cream supplemented with inulin was significantly firmer than other products throughout the storage except the 1st day (P < 0.05a 5. which would increase the viscosity of the system (Schmidt and others 1993). and the least change was obtained at the 60th and 90th days for the PI sample and the 90th day for the other products (P < 0. Although it seems that firmness was improved in all products by extension of storage.05) being considered statistically significant (SPSS 1997). Results and Discussion ompositional analyses of ice cream samples performed in the 1st day of storage revealed that the targeted total solids and fat levels were achieved (Table 1). Similar to our findings. The highest overrun value was also obtained in probiotic ice cream mix containing inulin (P < 0.14 ± 0. The addition of L. would modify the rheology of the mix.68 ± 0.05).45 ± 0. and viscosity increased by addition of oligofructose or inulin to mix (P < 0. indicating its responsibility for the increased air incorporation (Table 1).52 ± 0.05). animalis Bb-12 and fermentation of the mix did not significantly affect the overrun values (Table 1). The change in melting properties decreased in all samples as storage time increased. The highest mean apparent viscosity of 3905 MPa.51 ± 0.3b 50. These crystals interact to form a creamy texture (Niness 1999). A slower change in melting properties was observed in probiotic ice creams when compared to control sample during storage (P < 0. which was found to be statistically significant for all storage days (P < 0. The 1st dripping time was also longer in probiotic ice creams supplemented with oligofructose and inulin in comparison to the control sample (Figure 3). in addition to other components (like corn syrup or emulsifier–stabilizer mixture).b.0 ± 0.Results (mean ± SD. Melting properties were also improved by using oligofructose and inulin (P < 0.02b a pH 6.1a 4. . a direct correlation has been determined between firmness and melting behavior.05).01 and lactic acid percentage of 0. (P < 0.b. Due to its longer chain length.Probiotic culture survival in ice cream . However. In addition. n = 3) of compositional and physical analyses on aged mix and ice cream.6 ± 4. Mix Mix or ice cream R P PO PI pH 6. . PI = probiotic ice cream with inulin. Addition of oligofructose or inulin increased the firmness in probiotic ice cream. pH and lactic acid contents of regular and probiotic ice cream samples were significantly different (P < 0. would bind water and form a gellike network that.11a 33. Our results indicated that all probiotic ice creams were found to be firmer than regular ice M186 JOURNAL OF FOOD SCIENCE—Vol. Additionally. PO = probiotic mix or ice cream with oligofructose.1a a Lactic acid (%) 0. significant increases were not found (P > 0. Similar results in relation to the effect of inulin on viscosity were also reported by El-Nagar and others (2002) and Akın (2005) for yog-ice cream and probiotic-fermented ice cream. The overrun value increased approximately 2 times when inulin was used in the manufacture. Ice cream mixes containing carbohydrate-based fat replacers exhibit a viscous behavior because of the capability for imbibing water. Table 1 --.05) was obtained in the probiotic mixes containing inulin (Table 1). with differences at the 95% confidence interval (P < 0.0a 27. a.0 4. the most remarkable improvement in melting behavior was obtained in the product containing inulin (P < 0.05) (Figure 2). and the 90th day for the R and PO samples.49 ± 0.35 ± 0. 73.05).52 ± 0. in contrast to the findings of Akın (2005) for probioticfermented ice creams.45 ± 0.05a 5.c Means with different letters in the same column are different (P < 0.5c R = regular mix or ice cream. the 60th and 90th days for the PI sample.c Means with different letters in the same storage day are different (P < 0. In the current study.03b 3.Firmness index of ice cream during storage.47 ± 0. Higher molecular weight of inulin may be related to higher apparent viscosity of the ice cream mix with inulin in our study.35 ± 0.9ab 31.

In our study.05). a. acidophilus La-5 and 7. The gelling properties of inulin improve the consistency of mix and retard the melting of the product. as a result of freezing.0 log units. but not by Hekmat and McMahon (1992). animalis Bb-12 in the ice cream mixes P . Christiansen and others 1996. in vitro fermentation of inulin revealed that molecules with a shorter chain length are fermented quicker than molecules with a longer chain length (Roberfroid and others 1998). and 8. Furthermore. The viable counts of probiotic bacteria were 7.b. Alamprese and others (2002).b. In the storage. possibly depending on the higher viable Vol.44 ± 0. animalis Bb-12 survived better than L. however. and PO samples and at the 90th day for the PI sample (P < 0. the ice cream products supplemented with oligofructose contained higher viable counts of both probiotic bacteria during the storage. PO.c Means with different letters in the same storage day are different (P < 0. Fructooligosaccharides (FOS). These observations are consistent with those of El-Nagar and others (2002) who demonstrated that inulin supplementation reduced the melting rate and increased firmness in yog-ice cream.24 ± 0. 8. ice recrystallization occurs. Therefore. .28 log CFU/g for B. PI = probiotic ice cream with inulin. acidophilus La-5. B. a. The counts also significantly decreased (0.98 to 6. with a slightly lower melting point.05). different production technologies and formulations.14. acidophilus La-5 in ice cream over 90 d (Table 2).60 log CFU/g for B.05). Figure 3 --. P = probiotic ice cream. Addition of inulin led to the lowest change in melting properties and longest 1st dripping time as well as the most increase in firmness (P < 0.05) due to the possible prebiotic effects of oligofructose in the ice cream mix. and pH. and their numbers in the frozen ice cream were found to be in the range of 5. 4.16. animalis Bb-12 significantly increased in the probiotic ice cream mix by addition of oligofructose (P < 0. ice crystal size increases by about 30% to 40% during hardening of ice cream.12±0.51.05). . and Haynes and Playne (2002). Air cells act as an insulator (Marshall and others 2003). When compared to the control sample. This study has verified that the highest values for the apparent viscosity. and firmness and the most remarkable improvement in the meltdown characteristics were obtained in the mix or ice cream containing probiotics and inulin (P < 0. the counts of both viable bacteria decreased by 1. Therefore. P = probiotic ice cream. and 8. 2008—JOURNAL OF FOOD SCIENCE M187 Figure 2 --. During freezing and storage of ice cream. animalis Bb-12 in ice cream samples during storage are presented in Table 2. The error bars represent the standard deviation (n = 3). more or less reduction in the survival of probiotic bacteria was also reported (Hekmat and McMahon 1992. PI = probiotic ice cream with inulin. Typically.05). especially oligofructose. Davidson and others (2000) and Alamprese and others (2002) reported that starter culture bacteria in low-fat ice cream did not change significantly during storage. Ice creams containing a high amount of air (high overrun) tend to melt slowly. overrun.9 log CFU/g) throughout the storage (P < 0. according to the general mean value of storage. M: Food Microbiology & Safety . animalis Bb-12 and 5. The changes in the viable counts of L.58 ± 0. acidophilus La-5 and B. longest time was reported at the 60th and the 90th days for the R. is most likely due to the freeze injury of cells leading eventually the death of cells. respectively. animalis Bb-12 were higher than the recommended minimum limit of 106 CFU/g only in ice cream containing oligofructose during storage. are more sensitive to temperature fluctuations than larger crystals (Marshall and others 2003). 73.05). Akın (2005) also reported that addition of inulin retarded the melting time of probiotic-fermented ice cream. A similar finding was reported by Hagen and Narvhus (1999). acidophilus La-5 and B. and PI.5 to 2. The error bars represent the standard deviation (n = 3).First dripping times of ice cream during storage. the 1st dripping time of all samples can be improved by these interactions as storage time increased.62.c. Nr.96 to 6. The small crystals melt at the same time that large crystals grow.Melting properties of ice cream during storage.21 log CFU/g for L. freezing and mixing involved in converting the mix into ice cream had a greater effect on culture viability than storage in ice cream (P < 0.49 ± 0.Probiotic culture survival in ice cream . R = regular ice cream. PO = probiotic ice cream with oligofructose. P .74 ± 0.04 log CFU/g for L. are preferred by bifidobacteria as a source of carbon and energy. However. During freezing of the mix. the incorporation of oxygen into the mix may have resulted in an additional decrease in viable cell counts as well as the mechanical stresses of the mixing and freezing process. The decline in bacterial counts. Hagen and Narvhus 1999) for different microorganisms. Inulin or oligofructose can control ice recrystallization like a stabilizer agent. The changes in ice crystals due to the thermodynamic ripening process are enhanced by temperature fluctuations. the viable counts of B. In addition. due probably to the high molecular weight and hygroscopic properties of inulin.05). Growth rates of bifidobacteria cultivated on either oligofructose or inulin were evaluated and better growth was obtained on oligofructose than inulin (Wang and Gibson 1993. R = regular ice cream.3 to 0. higher survival of these probiotics in ice cream mix containing oligofructose can be sourced from shorter chain length or lower polymerization degree of oligofructose than inulin.d Means with different letters in the same storage day are different (P < 0. PO = probiotic ice cream with oligofructose. On the other hand. the viable counts for both L. 8. Gibson and Wang 1994). In addition. Small crystals.

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Compr Rev Food Sci F 3:117–24. animalis Bb-12 P PO PI P = probiotic ice cream. London. Fonden R. animalis Bb 12 (mean ± SD.22c 5. Prapulla SG.9 log CFU/g) during the storage.) ice cream. Brennan CS. Shah NP.05). Sangeetha PT. but at the initial freezing and churning stage of converting mix into ice cream a greater decrease (1. McMahon DJ. Milchwissenschaft 51:502–4. Safety and benefits of fructooligosaccharides as food ingredients. Food Aust 48:113–8.10aA 5. Roberfroid MB. Lundy A. Boling JW. Saxelin M. 2000.28cAB 5. 1999.3 to 0. Viscosity and freezing point of a reduced fat ice cream mix as related to inulin content. The lowest viable counts of B.47 ± 0.12 ± 0. Saxelin M. Mattila-Sandholm T. Hagen M. D. counts in mixes with oligofructose and more conducive structure of oligofructose to cell viability during storage (P < 0. Gibson GR.13 ± 0. Hunter WC. 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