Skip to main content
SpringerLink
Log in

The Microstructure and Physicochemical Properties of Probiotic Buffalo Yoghurt During Fermentation and Storage: a Comparison with Bovine Yoghurt

  • Original Paper
  • Published:
Food and Bioprocess Technology Aims and scope Submit manuscript

Abstract

The physicochemical and rheological properties of yoghurt made from unstandardised unhomogenised buffalo milk were investigated during fermentation and 28 days of storage and compared to the properties of yoghurt made from homogenised fortified bovine milk. A number of differences observed in the gel network can be linked to differences in milk composition. The microstructure of buffalo yoghurt, as assessed by confocal laser scanning microscopy (CLSM) and cryo scanning electron microscopy (cryo-SEM), was interrupted by large fat globules and featured more serum pores. These fat globules have a lower surface area and bind less protein than the homogenised fat globules in bovine milk. These microstructural differences likely lead to the higher syneresis observed for buffalo yoghurt with an increase from 17.4 % (w/w) to 19.7 % (w/w) in the weight of whey generated at days 1 and 28 of the storage. The higher concentration of total calcium in buffalo milk resulted in the release of more ionic calcium during fermentation. Gelation was also slower but the strength of the two gels was similar due to similar protein and total solids concentrations. Buffalo yoghurt was more viscous, less able to recover from deformation and less Newtonian than bovine yoghurt with a thixotropy of 3,035 Pa.s−1 measured for buffalo yoghurt at the end of the storage, at least four times higher than the thixotropy of bovine yoghurt. While the titratable acidity, lactose consumption and changes in organic acid concentrations were similar, differences were recorded in the viability of probiotic bacteria with a lower viability of Lactobacillus acidophilus of 5.17 log (CFU/g) recorded for buffalo yoghurt at day 28 of the storage. Our results show that factors other than the total solids content and protein concentration of milk affect the structural properties of yoghurt. They also illustrate the physicochemical reasons why buffalo and bovine yoghurt are reported to have different sensory properties and provide insight into how compositional changes can be used to alter the microstructure and properties of dairy products.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abd El-Salam, M. H. (1978). Comparative study of the composition of casein micelles from buffalo and cow milk. Egypt Journal of Dairy Science, 6, 1–8.

    CAS  Google Scholar 

  • Abu-Jdayil, B., & Mohameed, H. (2002). Experimental and modelling studies of the flow properties of concentrated yogurt as affected by the storage time. Journal of Food Engineering, 52(4), 359–365.

    Article  Google Scholar 

  • Addeo, F., Alloisio, V., & Chianese, L. (2007). Tradition and innovation in the water buffalo dairy products. Italian Journal of Animal Science, 6, 51–57.

    Google Scholar 

  • Adhikari, K., Grun, I. U., Mustapha, A., & Fernando, L. N. (2002). Changes in the profile of organic acids in plain set and stirred yogurts during manufacture and refrigerated storage. Journal of Food Quality, 25(5), 435–451.

    Article  CAS  Google Scholar 

  • Ahmad, S., Gaucher, I., Rousseau, F., Beaucher, E., Piot, M., Grongnet, J. F., et al. (2008). Effects of acidification on physicochemical characteristics of buffalo milk: A comparison with cow's milk. Food Chemistry, 106(1), 11–17.

    Article  CAS  Google Scholar 

  • AOAC. (2006). Official methods of analysis. Washington: Association of Official Analytical Chemists.

    Google Scholar 

  • Atwood, C. S., & Hartmann, P. E. (1992). Collection of fore and hind milk from the sow and the changes in milk-composition during suckling. The Journal of Dairy Research, 59, 287–298.

    Article  CAS  Google Scholar 

  • Australia New Zealand Food Standards (2006) Fermented milk products F2011C00622, Standard 2.5.3.

  • Bezerra, M. F., Souza, D. F. S., & Correia, R. T. P. (2012). Acidification kinetics, physiochemical properties, and sensory attributes of yoghurts prepared from mixtures of goat and buffalo milks. International Journal of Dairy Technology, 65(3), 437–443.

    Article  CAS  Google Scholar 

  • Bozanic, R. (2002). Fermentation and storage of probiotic yoghurt from goat's milk. Mljekarstvo, 52, 93.

    CAS  Google Scholar 

  • Bozanic, R., Lovkovic, S., & Jelicic, I. (2011). Optimising fermentation of soymilk with probiotic bacteria. Czech Journal of Food Sciences, 29(1), 51–56.

    Google Scholar 

  • Braun, P. G., & Preuss, S. E. (2008). Nutritional composition and chemico-physicai parameters of water buffalo milk and milk products in Germany. Milchwissenschaft Milk Science International, 63(1), 70–72.

    CAS  Google Scholar 

  • Chawla, A. K., & Balachandran, R. (1994). Studies on yoghurt buffalo milk: Effect of different solid nonfat content on chemical, rheological and sensory characteristics. Indian Journal of Dairy Science, 47(9), 762–765.

    Google Scholar 

  • Cunha-Neto, O. C., Olivera, A. A. F., Hotta, R. M., & Sorbal, P. J. A. (2005). Physico-chemical and sensory evaluation of plain yoghurt manufactured from buffalo milk with different fat content. Science and Technology of Agriculture, 25(3), 448–453.

    Google Scholar 

  • Dairy Australia (2010) Consumption summary for year 2009–2010. Production and sale. Available at: www.dairyaustralia.com.au. Accessed 30 November 2011.

  • Damin, M. R., Minowa, E., Alcantara, M. R., & Oliveira, M. N. (2008). Effect of cold storage on culture viability and some rheological properties of fermented milk prepared with yogurt and probiotic bacteria. Journal of Texture Studies, 39(1), 40–55.

    Article  Google Scholar 

  • Dave, R. I., & Shah, N. P. (1997). Effect of level of starter culture on viability of yoghurt and probiotic bacteria in yoghurts. Food Australia, 49(4), 164–168.

    Google Scholar 

  • Domagala, J. (2009). Instrumental texture, syneresis and microstructure of yoghurts prepared from goat, cow and sheep Milk. International Journal of Food Properties, 12(3), 605–615.

    Article  Google Scholar 

  • Donkor, O. N., Tsangalis, D., & Shah, N. P. (2007). Viability of probiotic bacteria and concentrations of organic acids in commercial yoghurts during refrigerated storage. Food Australia, 59(4), 121–126.

    CAS  Google Scholar 

  • El-Dieb, S. M., Abd Rabo, F. H. R., Badran, S. M., Abd El-Fattah, A. M., & Elshaghabee, F. M. F. (2012). The growth behaviour and enhancement of probiotic viability in bioyoghurt. International Dairy Journal, 22(1), 44–47.

    Article  Google Scholar 

  • Erkaya, T., & Sengul, M. (2011). Comparison of volatile compounds in yoghurts made from cows', buffaloes', ewes' and goats' milks. International Journal of Dairy Technology, 64(2), 240–246.

    Article  CAS  Google Scholar 

  • Fernandezgarcia, E., & McGregor, J. U. (1994). Determination of organic-acids during the fermentation and cold-storage of yogurt. Journal of Dairy Science, 77(10), 2934–2939.

    Article  CAS  Google Scholar 

  • Ghadge, P. N. (2008). Effect of fortification on the physico-chemical and sensory properties of Buffalo milk yoghurt. Electronic Journal of Environmental Agricultural and Food Chemistry, Electronic journal of environmental, agricultural and food chemistry, 7(5), 2890.

    Google Scholar 

  • Gilliland, S. E., & Lara, R. C. (1988). Influence of storage at freezing and subsequent refrigeration temperatures on beta-galactosidase activity of Lactobacillus-acidophilus. Applied and Environmental Microbiology, 54(4), 898–902.

    CAS  Google Scholar 

  • Gosling, A., Alftren, J., Stevens, G. W., Barber, A. R., Kentish, S. E., & Gras, S. L. (2009). Facile pretreatment of Bacilius circulans beta-galactosidase increases the yield of galactosyl oligosaccharides in milk and lactose reaction systems. Journal of Agricultural and Food Chemistry, 57(24), 11570–11574.

    Article  CAS  Google Scholar 

  • Gun, O., & Isikli, N. (2006). The effects of fat and non fat dry matter concentration and storage time on the physical properties and acidity of yoghurts made with probiotic cultures. Food Science and Technology International, 12(6), 467–476.

    Article  CAS  Google Scholar 

  • Gundogdu, E., Cakmakci, S., & Dagdemir, E. (2009). The effect of garlic (Allium sativum L.) on some quality properties and shelf-life of set and stirred yoghurt. Turkish Journal of Veterinary and Animal Sciences, 33(1), 27–35.

    CAS  Google Scholar 

  • Haque, A., Richardson, R. K., & Morris, E. R. (2001). Effect of fermenation temperature on the rheology of set and stirred yogurt. Food Hydrocolloids, 15, 593–602.

    Article  CAS  Google Scholar 

  • Jensen, R. G. (1995). Handbook of milk composition. San Diego: Academic Press.

    Google Scholar 

  • Keogh, K. M., & O’Kennedy, B. T. (1998). Rheology of stirred yoghurt as affected by added milk fat, protein and hydrocolloids. Journal of Food Science, 63, 108–112.

    Article  CAS  Google Scholar 

  • Khanna, A., & Singh, J. (1979). A comparison of yoghurt starter in cow's and buffalo milk. The Journal of Dairy Research, 46(04), 681.

    Article  CAS  Google Scholar 

  • Kumar, P., & Mishra, H. N. (2003). Effect of mango pulp and soymilk fortification on the texture profile of set yoghurt made from buffalo milk. Journal of Texture Studies, 34(3), 249–269.

    Article  Google Scholar 

  • Larson, B. L., & Hegarty, H. M. (1979). Orotic acid in milks of various species and commercial dairy-products. Journal of Dairy Science, 62(10), 1641–1644.

    Article  CAS  Google Scholar 

  • Lee, W. J., & Lucey, J. A. (2003). Rheological properties, whey separation, and microstructure in set-style yogurt: Effects of heating temperature and incubation temperature. Journal of Texture Studies, 34(5–6), 515–536.

    Article  Google Scholar 

  • Lee, W. J., & Lucey, J. A. (2004a). Effect of starter inoculation rates and incubation temperatures on physical properties of yogurt. Journal of Animal Science, 82, 93–93.

    Google Scholar 

  • Lee, W. J., & Lucey, J. A. (2004b). Structure and physical properties of yogurt gels: Effect of inoculation rate and incubation temperature. Journal of Dairy Science, 87(10), 3153–3164.

    Article  CAS  Google Scholar 

  • Lee, W. J., & Lucey, J. A. (2010). Formation and physical properties of yoghurt. Asian-Australasian Journal of Animal Sciences, 23(9), 1127–1136.

    Article  CAS  Google Scholar 

  • Lewis, M. J. (2011). The measurement and significance of ionic calcium in milk - A review. International Journal of Dairy Technology, 64(1), 1–13.

    Article  CAS  Google Scholar 

  • Lin, M. J., Lewis, M. J., & Grandison, A. S. (2006). Measurement of ionic calcium in milk. International Journal of Dairy Technology, 59(3), 192–199.

    Article  CAS  Google Scholar 

  • Lucey, J., Tamehana, M., Singh, H., & Munro, P. (1998). A comparison of the formation, rheological properties and microstructure of acid skim milk gels made with a bacterial culture or glucono-delta-lactone. Food Research International, 31(2), 147–155.

    Article  CAS  Google Scholar 

  • Marafon, A. P., Sumi, A., Alcantara, M. R., Tamime, A. Y., & de Oliveira, M. N. (2011). Optimization of the rheological properties of probiotic yoghurts supplemented with milk proteins. LWT- Food Science and Technology, 44(2), 511–519.

    Article  CAS  Google Scholar 

  • Mekmene, O., Le Graet, Y., & Gaucheron, F. (2010). Theoretical model for calculating ionic equilibria in milk as a function of pH: comparison to experiment. Journal of Agricultural and Food Chemistry, 58(7), 4440–4447.

    Article  CAS  Google Scholar 

  • Menard, O., Ahmad, S., Rousseau, F., Briard-Bion, V., Gaucheron, F., & Lopez, C. (2010). Buffalo vs. cow milk fat globules: Size distribution, zeta-potential, compositions in total fatty acids and in polar lipids from the milk fat globule membrane. Food Chemistry, 120(2), 544–551.

    Article  CAS  Google Scholar 

  • Nahar, A., Amin, M. A., Alam, S. M. K., Wadud, A., & Islam, M. N. (2007). A comparative study on the quality of Dahi (yoghurt) prepapared from cow, goat and buffalo milk. International Journal of Dairy Science, 2(3), 260–267.

    Article  CAS  Google Scholar 

  • Okonkwo, P., & Kinsella, J. E. (1969). Orotic acid in yoghurt. Journal of Dairy Science, 52(11), 1861–1862.

    Article  CAS  Google Scholar 

  • Oliveira, M. N., Sodini, I., Remeuf, F., & Corrieu, G. (2001). Effect of milk supplementation and culture composition on acidification, textural properties and microbiological stability of fermented milks containing probiotic bacteria. International Dairy Journal, 11(11–12), 935–942.

    Article  CAS  Google Scholar 

  • Ong, L., Dagastine, R. R., Kentish, S. E., & Gras, S. L. (2010). The effect of milk processing on the microstructure of the milk fat globule and rennet induced gel observed using confocal laser scanning microscopy. Journal of Food Science, 75, 135–145.

    Article  Google Scholar 

  • Ong, L., Dagastine, R. R., Kentish, S. E., & Gras, S. L. (2011). Microstructure of milk gel and cheese curd observed using cryo scanning electron microscopy and confocal microscopy. LWT- Food Science and Technology, 44(5), 1291–1302.

    Article  CAS  Google Scholar 

  • Ong, L., Dagastine, R. R., Kentish, S. E., & Gras, S. L. (2012). The effect of pH at renneting on the microstructure, composition and texture of Cheddar cheese. Food Research International, 48, 119–130.

    Article  CAS  Google Scholar 

  • Ozer, B. H., & Kirmaci, H. A. (2010). Functional milks and dairy beverages. International Journal of Dairy Technology, 63(1), 1–15.

    Article  CAS  Google Scholar 

  • Pandya, N., Kanawjia, S., & Dave, R. (2004). Effects of fat content on physico-chemical and sensory properties of buffalo milk dahi (yoghurt). Journal of Animal Science, 82, 236–236.

    Google Scholar 

  • Pesce, M. A., & Strande, C. S. (1973). New micromethod for determination of protein in cerebrospinal-fluid and urine. Clinical Chemistry, 19, 1265–1267.

    CAS  Google Scholar 

  • Prakash, B. S., & Sharma, R. S. (1986). Orotic acid in milk and milk products. Journal of Food Science and Technology Mysore, 23(2), 85–87.

    CAS  Google Scholar 

  • Priya, A. J., Vijayalakshmi, S. P., & Raichui, A. M. (2011). Enhanced survival of probiotic Lactobacillus acidophilus by encapsulation with nanostructured polyelectrolyte layers through layer-by-layer approach. Journal of Agricultural and Food Chemistry, 59(21), 11838–11845.

    Article  CAS  Google Scholar 

  • Purwandari, U., & Vasiljevic, T. (2009). Rheological properties of fermented milk produced by a single exopolysaccharide producing Streptococcus thermophilus strain in the presence of added calcium and sucrose. International Journal of Dairy Technology, 62(3), 411–421.

    Article  CAS  Google Scholar 

  • Purwandari, U., Shah, N. P., & Vasiljevic, T. (2007). Effects of exopolysaccharide-producing strains of Streptococcus thermophilus on technological and rheological properties of set-type yoghurt. International Dairy Journal, 17(11), 1344–1352.

    Article  CAS  Google Scholar 

  • Raju, P., & Pal, D. (2009). The physico-chemical, sensory, and textural properties of misti dahi prepared from reduced fat buffalo milk. Food and Bioprocess Technology, 2(1), 101–108.

    Article  CAS  Google Scholar 

  • Rao, M. A. (2007). Rheology of fluid and semisolid foods: principles and applications. Rheology of fluid and semisolid foods: principles and applications (2nd ed.). New York: Springer.

    Google Scholar 

  • Robinson, R. K., & Haddadin, M. S. Y. (2010). Improving the safety and quality of milk, volume 2: improving quality in milk products. In M. W. Griffiths (Ed.), Improving the safety and quality of milk, volume 2: Improving quality in milk products. Cambridge: Woodhead Ltd.

    Google Scholar 

  • Saccaro, D. M., Tamime, A. Y., Pilleggi, A., & Oliveira, M. N. (2009). The viability of three probiotic organisms grown with yoghurt starter cultures during storage for 21 days at 4 degrees C. International Journal of Dairy Technology, 62(3), 397–404.

    Article  Google Scholar 

  • Salvador, A., & Fiszman, S. M. (2004). Textural and sensory characteristics of whole and skimmed flavored set-type yogurt during long storage. Journal of Dairy Science, 87(12), 4033–4041.

    Article  CAS  Google Scholar 

  • Shiby, V. K., & Mishra, H. N. (2008). Modelling of acidification kinetics and textural properties in dahi (Indian yogurt) made from buffalo milk using response surface methodology. International Journal of Dairy Technology, 61(3), 284–289.

    Article  CAS  Google Scholar 

  • Sikka, P., Saxena, N. K., Gupta, R., Sethi, R. K., & Lall, D. (2001). Studies on milk allantoin and uric acid in relation to feeding regimens and production performance in buffaloes. Asian-Australasian Journal of Animal Sciences, 14(11), 1634–1637.

    CAS  Google Scholar 

  • Tamime, A. Y., & Robinson, R. K. (2007). Yoghurt: Science and technology, Third Edition. In A. Y. Tamime & R. K. Robinson (Eds.), Tamime and Robinsons Yoghurt: Science and Technology (3rd ed.). Cambridge: Woodhead Publ Ltd.

    Chapter  Google Scholar 

  • Tan, W. S., Budinich, M. F., Ward, R., Broadbent, J. R., & Steele, J. L. (2012). Optimal growth of Lactobacillus casei in a Cheddar cheese ripening model system requires exogenous fatty acids. Journal of Dairy Science, 95(4), 1680–1689.

    Article  CAS  Google Scholar 

  • Thi, M. P. N., Lee, Y. K., & Zhou, W. B. (2012). Effect of high intensity ultrasound on carbohydrate metabolism of bifidobacteria in milk fermentation. Food Chemistry, 130(4), 866–874.

    Article  Google Scholar 

  • Tormo, M., & Izco, J. M. (2004). Alternative reversed-phase high-performance liquid chromatography method to analyse organic acids in dairy products. Journal of Chromatography. A, 1033(2), 305–310.

    Article  CAS  Google Scholar 

  • Varricchio, M. L., Di Francia, A., Masucci, F., Romano, R., & Proto, V. (2007). Fatty acid composition of Mediterranean buffalo milk fat. Italian Journal of Animal Science, 6, 509–511.

    Google Scholar 

  • Venkatappaiah, D., & Basu, K. P. (1952). Non-protein nitrogenous constituents of milk. I. Variation due to species, breed, individuality, season and stage of lactation. Indian Journal of Dairy Science, 5(2), 95–116.

    CAS  Google Scholar 

  • Wishon, L. M., Song, D. F., & Ibrahim, S. A. (2010). Effect of metals on growth and functionality of Lactobacillus and Bifidobacteria. Milchwissenschaft-Milk Science International, 65(4), 369–372.

    CAS  Google Scholar 

  • Yadav, H., Jain, S., & Sinha, P. R. (2007). Evaluation of changes during storage of probiotic dahi at 7 degrees C. International Journal of Dairy Technology, 60(3), 205–210.

    Article  CAS  Google Scholar 

  • Yazici, F., & Akbulut, C. (2007). Impact of whey pH at drainage on the physicochemical, sensory, and functional properties of Mozzarella cheese made from buffalo milk. Journal of Agricultural and Food Chemistry, 55(24), 9993–10000.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge the Australian Government for providing the Australian Postgraduate Award (International) (APA-International) scholarship, Rural Industries Research and Development Cooperation (RIRDC) for financial support and Shaw River for kindly supplying the buffalo milk. The authors also thank the Particulate Fluids Processing Centre (PFPC) and the Bio21 Institute for access the equipment and Mr Roger Curtain for his help in operating the scanning electron microscope in cryo mode.

Author information

Authors and Affiliations

  1. Department of Chemical and Biomolecular Engineering, The University of Melbourne, Parkville, Victoria, 3010, Australia

    Hanh Thi Hong Nguyen, Lydia Ong, Sandra Elizabeth Kentish & Sally Louise Gras

  2. The Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Parkville, Victoria, 3010, Australia

    Hanh Thi Hong Nguyen, Lydia Ong & Sally Louise Gras

  3. Institute for Technology Research and Innovation, Deakin University, Geelong, Victoria, 3220, Australia

    Christophe Lefèvre

Authors
  1. Hanh Thi Hong Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lydia Ong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christophe Lefèvre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sandra Elizabeth Kentish
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sally Louise Gras
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sally Louise Gras.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PPTX 524 kb)

ESM 2

(PPTX 492 kb)

ESM 3

(PPTX 67.0 kb)

ESM 4

(PPTX 528 kb)

ESM 5

(PPTX 58.8 kb)

ESM 6

(PPTX 398 kb)

ESM 7

(PPTX 91 kb)

Supplementary Table 1

Volume, surface area, mean diameter and number of fat globules (FGs) in buffalo milk and fortified bovine milk determined using CLSM or light scattering. (DOC 35 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nguyen, H.T.H., Ong, L., Lefèvre, C. et al. The Microstructure and Physicochemical Properties of Probiotic Buffalo Yoghurt During Fermentation and Storage: a Comparison with Bovine Yoghurt. Food Bioprocess Technol 7, 937–953 (2014). https://doi.org/10.1007/s11947-013-1082-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11947-013-1082-z

Keywords

Search

Navigation