Skip to main content
Log in

The Effect of Fermentation Temperature on the Microstructure, Physicochemical and Rheological Properties of Probiotic Buffalo Yoghurt

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

Abstract

The properties of buffalo and bovine milk differ and the procedures developed to make bovine yoghurt may require optimisation for the production of buffalo yoghurt. This study aimed to apply cryo-scanning electron microscopy and confocal laser scanning microscopy to determine the optimal temperature for processing buffalo yoghurt. Milk was fermented at three different temperatures (37, 40 and 43 °C), stored for 28 days and the yoghurt microstructure, physicochemical and rheological properties assessed. Yoghurt fermented at 37 °C had a compact microstructure and the probiotic Lactobacillus acidophilus La-5 was more viable on storage. In contrast, yoghurt produced from a faster fermentation at 43 °C was firmer with a more porous microstructure that exhibited a higher degree of syneresis. The rheological properties during storage including the thixotropy, consistency coefficient and flow behaviour index were not significantly affected by temperature nor were the concentration of lactose, ionic calcium or titratable acidity. This study shows how changes to processing can be used to alter the microstructure of buffalo products and suggests that a decrease in fermentation temperature could be used to improve the quality of buffalo yoghurt.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbasi, H., Mousavi, M. E., Ehsani, M. R., Emamdjomea, Z., Vaziri, M., Rahimi, J., et al. (2009). Influence of starter culture type and incubation temperatures on rheology and microstructure of low fat set yoghurt. International Journal of Dairy Technology, 62(4), 549–555.

    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 

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

    Article  CAS  Google Scholar 

  • Anema, S. G. (2008). Effect of temperature and rate of acidification on the rheological properties of acid skim milk gels. Journal of Food Processing and Preservation., 32(6), 1016–1033.

    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. Journal of Dairy Research, 59(3), 287–298.

    Article  CAS  Google Scholar 

  • Australia and New Zealand Food Standards (2006). Fermented milk Products-F2011C00622- Standard 2.5.3.

  • Baati, L., Roux, G., Dahhou, B., & Uribelarrea, J. L. (2004). Unstructured modelling growth of Lactobacillus acidophilus as a function of the temperature. Mathematics and computers in simulation., 65(1–2), 137–145.

    Article  Google Scholar 

  • Bezerra, M. F., Souza, D. F. S., & Correia, R. T. P. (2012). Acidification kinetics, physicochemical 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., Brletic, S., & Lovkovic, S. (2008). Influence of temperature and sugar addition on soymilk fermentation by probiotic bacteria. Mljekarstvo, 58(1), 61–68.

    CAS  Google Scholar 

  • Chandan, R. C., & O'Rell, K. R. (2006). Principles of yoghurt processing. In R. C. Chandan, C. H. White, A. Kilara, & Y. H. Hui (Eds.), Manufacturing yoghurt and fermented milks (pp. 195–210). Oxford, UK: Wiley-Blackwell.

    Chapter  Google Scholar 

  • 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 yoghurt 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 

  • Folkenberg, D. M., Dejmek, P., Skriver, A., Guldager, H. S., & Ipsen, R. (2004). Sensory and rheological screening of exopolysaccharide producing strains of bacterial yoghurt cultures. International Dairy Journal, 16(2), 111–118.

    Article  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., 7(5), 2890–2899.

    CAS  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 Bacillus 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 

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

    Article  CAS  Google Scholar 

  • Hidalgo-Cantabrana, C., Sanchez, B., Moine, D., Berger, B., de Los Reyes-Gavilán, C. G., Sánchez, B., et al. (2013). Insights into the ropy phenotype of the exopolysaccharide-producing strain Bifidobacterium animalis subsp. lactis A1dOxR. Applied and environmental microbiology, 79(12), 3870–3874.

    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 

  • Laligant, A., Famelart, M. H., Paquet, D., & Brule, G. (2003). Fermentation by lactic bacteria at two temperatures of pre-heated reconstituted milk. II—dynamic approach of the gel construction. Le Lait, 83(4), 307–320.

    Article  CAS  Google Scholar 

  • Lee, W. J., & Lucey, J. A. (2003). Rheological properties, whey separation, and microstructure in set-style yoghurt: 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. (2004). Structure and physical properties of yoghurt gels: effect of inoculation rate and incubation temperature. Journal of Dairy Science, 87(10), 3153–3164.

    Article  CAS  Google Scholar 

  • Leivers, S., Hidalgo-Cantabrana, C., Robinson, G., Margolles, A., Ruas-Madiedo, P., & Laws, A. P. (2011). Structure of the high molecular weight exopolysaccharide produced by Bifidobacterium animalis subsp lactis IPLA-R1 and sequence analysis of its putative eps cluster. Carbohydrate Research, 346(17), 2710–2717.

    Article  CAS  Google Scholar 

  • Lucey, J., Tamehana, M., Singh, H., & Munro, P. (1998a). 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 

  • Lucey, J. A., & Singh, H. (1997). Formation and physical properties of acid milk gels: a review. Food Research International, 30(7), 529–542.

    Article  CAS  Google Scholar 

  • Lucey, J. A., Tamehana, M., Singh, H., & Munro, P. A. (1998b). Effect of interactions between denatured whey proteins and casein micelles on the formation and rheological properties of acid skim milk gels. Journal of Dairy Research, 65(4), 555–567.

    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 

  • Martin, N. C., Skokanova, J., Latrille, E., Beal, C., & Corrieu, G. (1999). Influence of fermentation and storage conditions on the sensory properties of plain low fat stirred yoghurts. Journal of Sensory Studies, 14(2), 139–160.

    Article  Google Scholar 

  • McClements, D. J. (2007). Understanding and controlling the microstructure of complex foods. Understanding and controlling the microstructure of complex foods. Cambridge, England: Woodhead.

    Book  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 

  • Murga, M. L. F., Cabrera, G. M., de Valdez, G. F., Disalvo, A., & Seldes, A. M. (2000). Influence of growth temperature on cryotolerance and lipid composition of Lactobacillus acidophilus. Journal of Applied Microbiology, 88(2), 342–348.

    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) prepared from cow, goat and buffalo milk. International Journal of Dairy Science., 2(3), 260–267.

    Article  CAS  Google Scholar 

  • Nguyen, H. T. H., Ong, L., Lefevre, C., Kentish, S. E., & Gras, S. L. (2013). The microstructure and physicochemical properties of probiotic buffalo yoghurt during fermentation and storage: a comparison with bovine yoghurt. Food and Bioprocess Technology. doi:10.1007/s/1947-013.1082z.

    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. (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 

  • 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 

  • Paseephol, T., Small, D. M., & Sherkat, F. (2008). Rheology and texture of set yogurt as affected by inulin addition. Journal of Texture Studies, 39(6), 617–634.

    Article  Google Scholar 

  • Pesce, M. A., & Strande, C. S. (1973). New micromethod for determination of protein in cerebrospinal-fluid and urine. Clinical Chemistry, 19(11), 1265–1267.

    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 

  • 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 

  • 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 

  • Sahai, D. (1996). Buffalo milk: chemistry and processing technology (p. 276). New Delhi, India: Karnal.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sfakianakis, P. & Tzia, C (2011). Yoghurt from ultrasound treated milk: monitoring of fermentation process and evaluation of product quality characteristics. In: Taoukis PS, Stoforos NG, Karathanos VT & Saravacos GD (eds) The 11th International Congress on Engineering and Food (ICEF11): Food process engineering in a changing world. Comosware, Athens, Greece.

  • Shafiee, G., Mortazavian, A. M., Mohammadifar, M. A., Koushki, M. R., Mohammadi, A., & Mohammadi, R. (2010). Combined effects of dry matter content, incubation temperature and final pH of fermentation on biochemical and microbiological characteristics of probiotic fermented milk. African Journal of Microbiology Research, 4(12), 1265–1274.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sodini, I., Remeuf, F., Haddad, S., & Corrieu, G. (2004). The relative effect of milk base, starter, and process on yogurt texture: a review. Critical Reviews in Food Science and Nutrition, 44(2), 113–137.

    Article  Google Scholar 

  • Tamime, A. Y., & Robinson, R. K. (2007). Background to manufacturing practice. Yoghurt: science and technology (Vol. 140). Cambridge: Woodhead.

    Google Scholar 

  • Wang, Y., Corrieu, G., & Béal, C. (2005a). Fermentation pH and temperature influence the cryotolerance of Lactobacillus acidophilus RD758. Journal of Dairy Science, 88(1), 21–29.

    Article  CAS  Google Scholar 

  • Wang, Y., Delettre, M., Guillot, A., Corrieu, G., & Beal, C. (2005b). Influence of cooling temperature and duration on cold adaptation of Lactobacillus acidophilus RD758. Cryobiology, 50(3), 294–307.

    Article  CAS  Google Scholar 

  • Wu, S., Li, D., Li, S. J., Bhandari, B., Yang, B. L., Chen, X. D., et al. (2009). Effects of incubation temperature, starter culture level and total solids content on the rheological properties of yoghurt. International Journal of Food Engineering, 5(2), 1–17.

    Article  Google Scholar 

  • Xu, S. Y., Stanley, D. W., Goff, H. D., Davidson, V. J., & Lemaguer, M. (1992). Hydrocolloid milk gel formation and properties. Journal of Food Science, 57(1), 96–102.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zhang, S. & Zhang, L. (2012). Effect of exopolysaccharide producing lactic acid bacterial on the gelation and texture properties of yogurt. In: Chen R, Sun D & Sung WP (eds) International Conference on Frontiers of Advanced Materials and Engineering Technology, vol 430–432. p^pp 890–893. Trans Tech Publication LTD, Zurich, Switzerland, Xiamen, China.

Download references

Acknowledgements

The authors would like to acknowledge the Australian Government for providing the Australian Postgraduate Award (International) (APA—International) scholarship, the 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 Molecular Science and Technology Institute for access the equipment, Mr Roger Curtain for his help in operating the cryo-SEM and Dr Sandy Clarke (Department of Mathematics and Statistics, University of Melbourne) for her assistance in statistical analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sally L. Gras.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nguyen, H.T.H., Ong, L., Kentish, S.E. et al. The Effect of Fermentation Temperature on the Microstructure, Physicochemical and Rheological Properties of Probiotic Buffalo Yoghurt. Food Bioprocess Technol 7, 2538–2548 (2014). https://doi.org/10.1007/s11947-014-1278-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11947-014-1278-x

Keywords

Navigation