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Effect of High-Pressure Processing on Quality and Microbiological Properties of a Fermented Beverage Manufactured from Sweet Whey Throughout Refrigerated Storage

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Abstract

The production of fermented beverages is a promising way to valorize by-products of dairy manufacturing. However, the shelf-life of these products is often limited by the post-acidification process that occurs during storage. In this work, we manufactured a fermented beverage from sweet whey by using the starter lactic acid bacteria (SLAB) Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus. High-pressure processing (HPP) at 200 MPa for 10 min or 400 MPa for 1 min were applied after manufacturing. The aim of this study was to evaluate the effect of HPP on the quality of the beverage and on the behavior of the SLAB. Both high hydrostatic pressure treatments preserved flavor and texture attributes until 45 days post-HPP, without affecting chromatic parameters. Plate counts for both species were lower in HPP-treated beverages (HB) than in control beverages (CB), although treatment at 200 MPa maintained optimal amounts of total SLAB (6.6–7.9 log CFU/mL). Conversely, quantitative PCR (qPCR) and reverse transcription-qPCR (RT-qPCR) revealed that bacterial DNA or mRNA levels persisted after HPP (> 1.4 × 105 genome or cDNA copies/mL), even upon 400-MPa treatments. As a whole, this study indicated that HPP preserved the quality of the beverage until 45 days post-HPP, which is longer than the shelf-life of conventional fermented beverages obtained from milk. Moreover, our results obtained with these SLAB in a fermented dairy beverage upon HPP extend previous findings regarding the limitations of culture-dependent methods to assess microbial viability.

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Abbreviations

BOD:

Biochemical oxygen demand

CB:

Control beverages

cDNA:

Complementary DNA

CFU:

Colony forming units

Ct:

Threshold cycle

DGGE:

Denaturing gradient gel electrophoresis

HB:

HPP-treated beverages

HPP:

High-pressure processing

ISO:

International Organization for Standardization

LOD:

Limit of detection

mRNA:

Messenger RNA

qPCR:

Quantitative PCR

RT-qPCR:

Reverse transcription-qPCR

SD:

Standard deviation

SLAB:

Starter lactic acid bacteria

VBNC:

Viable but non-culturable

WI:

Whiteness index

References

  • Ashraf, R., & Shah, N. P. (2011). Selective and differential enumerations of Lactobacillus delbrueckii subsp. bulgaricus, Streptococcus thermophilus, Lactobacillus acidophilus, Lactobacillus casei and Bifidobacterium spp. in yoghurt—a review. International Journal of Food Microbiology, 149(3), 194–208.

    Article  Google Scholar 

  • Božanić, R., Barukčić, I., Jakopović, K. L., & Tratnik, L. (2014). Possibilities of whey utilisation. Austin Journal of Nutrition and Food Sciences, 2(7), 1036.

    Google Scholar 

  • CAA (Argentine Food Code), 2012. Código Alimentario Argentino (Art. 625). Ed. De La Canal & Asociados SRL, Buenos Aires, Argentina.

  • Chawla, R., Patil, G. R., & Singh, A. K. (2011). High hydrostatic pressure technology in dairy processing: a review. Journal of Food Science and Technology, 48(3), 260–268.

    Article  Google Scholar 

  • Cocolin, L., Alessandria, V., Dolci, P., Gorra, R., & Rantsiou, K. (2013). Culture independent methods to assess the diversity and dynamics of microbiota during food fermentation. International Journal of Food Microbiology, 167(1), 29–43.

    Article  CAS  Google Scholar 

  • Codex Alimentarius. (2003). Codex-standard 243–2003: Codex standard for fermented milks. http://www.codexalimentarius.net/input/download/standards/400/CXS_243e.pdf

  • de Ancos, B., Cano, M. P., & Gómez, R. (2000). Characteristics of stirred low-fat yoghurt as affected by high pressure. International Dairy Journal, 10(1-2), 105–111.

    Article  Google Scholar 

  • Denoya, G. I., Nanni, M. S., Apóstolo, N. M., Vaudagna, S. R., & Polenta, G. A. (2016). Biochemical and microstructural assessment of minimally processed peaches subjected to high-pressure processing: implications on the freshness condition. Innovative Food Science & Emerging Technologies, 36, 212–220.

    Article  CAS  Google Scholar 

  • Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., Gonzalez, L., Tablada, M., Robledo, C. W. (2015). Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. URL http://www.infostat.com.ar.

  • Diez, A. M., Urso, R., Rantsiou, K., Jaime, I., Rovira, J., & Cocolin, L. (2008). Spoilage of blood sausages morcilla de Burgos treated with high hydrostatic pressure. International Journal of Food Microbiology, 123(3), 246–253.

    Article  CAS  Google Scholar 

  • Falentin, H., Henaff, N., Le Bivic, P., Deutsch, S. M., Parayre, S., Richoux, R., Sohier, D., Thierry, A., Lortal, S., & Postollec, F. (2012). Reverse transcription quantitative PCR revealed persistency of thermophilic lactic acid bacteria metabolic activity until the end of the ripening of Emmental cheese. Food Microbiology, 29(1), 132–140.

    Article  CAS  Google Scholar 

  • Guarner, F., Perdigon, G., Corthier, G., Salminen, S., Koletzko, B., & Morelli, L. (2005). Should yoghurt cultures be considered probiotic? British Journal of Nutrition, 93(6), 783–786.

    Article  CAS  Google Scholar 

  • Harte, F., Luedecke, L., Swanson, B., & Barbosa-Canovas, G. V. (2003). Low-fat set yogurt made from milk subjected to combinations of high hydrostatic pressure and thermal processing. Journal of Dairy Science, 86(4), 1074–1082.

    Article  CAS  Google Scholar 

  • ISO 22935–2:2009 (IDF 99–2:2009). Milk and milk products—sensory analysis—part 2: recommended methods for sensory evaluation.

  • Jankowska, A., Reps, A., Proszek, A., & Krasowska, M. (2005). Effect of high pressure on microflora and sensory characteristics of yoghurt. Polish Journal of Food and Nutrition Sciences, 14/55(1), 79–84.

    Google Scholar 

  • Jankowska, A., Grześkiewicz, A., Wiśniewska, K., & Reps, A. (2012). Examining the possibilities of applying high pressure to preserve yoghurt supplemented with probiotic bacteria. High Pressure Research: An International Journal, 32(3), 339–346.

    Article  CAS  Google Scholar 

  • Jany, J. L., & Barbier, G. (2008). Culture-independent methods for identifying microbial communities in cheese. Food Microbiology, 25(7), 839–848.

    Article  CAS  Google Scholar 

  • Krasowska, M., Reps, A., & Jankowska, A. (2005). Effect of high pressures on the activity of selected strains of lactic acid bacteria. Milchwissenschaft, 60, 382–385.

    CAS  Google Scholar 

  • López-Fandiño, R. (2006). High pressure-induced changes in milk proteins and possible applications in dairy technology. International Dairy Journal, 16(10), 1119–1131.

    Article  Google Scholar 

  • Martínez-Onandi, N., Castioni, A., San Martín, E., Rivas-Cañedo, A., Nuñez, M., Torriani, S., & Picon, A. (2017). Microbiota of high-pressure-processed serrano ham investigated by culture-dependent and culture-independent methods. International Journal of Food Microbiology, 241, 298–307.

    Article  Google Scholar 

  • Miller, D. M., Dudley, E. G., & Roberts, R. F. (2012). Technical note: development of a quantitative PCR method for monitoring strain dynamics during yogurt manufacture. Journal of Dairy Science, 95(9), 4868–4872.

    Article  CAS  Google Scholar 

  • Overney, A., Jacques-André-Coquin, J., Ng, P., Carpentier, B., Guillier, L., & Firmesse, O. (2016). Impact of environmental factors on the culturability and viability of Listeria monocytogenes under conditions encountered in food processing plants. International Journal of Food Microbiology, 244, 74–81.

    Article  Google Scholar 

  • Panesar, P. S., & Kennedy, J. F. (2012). Biotechnological approaches for the value addition of whey. Critical Reviews in Biotechnology, 32(4), 327–348.

    Article  CAS  Google Scholar 

  • Patel, S. (2015). Emerging trends in nutraceutical applications of whey protein and its derivatives. Journal of Food Science and Technology, 52(11), 6847–6858.

    Article  CAS  Google Scholar 

  • Pega, J., Rizzo, S., Pérez, C. D., Rossetti, L., Díaz, G., Ruzal, S. M., Nanni, M., & Descalzo, A. M. (2016). Effect of the addition of phytosterols and tocopherols on Streptococcus thermophilus robustness during industrial manufacture and ripening of a functional cheese as evaluated by qPCR and RT-qPCR. International Journal of Food Microbiology, 232, 117–125.

    Article  CAS  Google Scholar 

  • Pega, J., Rizzo, S., Rossetti, L., Pérez, C. D., Díaz, G., Descalzo, A. M., & Nanni, M. (2017). Impact of extracellular nucleic acids from lactic acid bacteria on qPCR and RT-qPCR results in dairy matrices: implications for defining molecular markers of cell integrity. LWT-Food Science and Technology, 80, 416–422.

    Article  CAS  Google Scholar 

  • Pérez Pulido, R., Grande Burgos, M. J., Gálvez, A., & Lucas, R. (2017). Changes in bacterial diversity of refrigerated mango pulp before and after treatment by high hydrostatic pressure. LWT – Food Science and Technology, 78, 289–295.

    Article  Google Scholar 

  • Prazeres, A. R., Carvalho, F., & Rivas, J. (2012). Cheese whey management: a review. Journal of Environmental Management, 110, 48–68.

    Article  CAS  Google Scholar 

  • Reps, A., Jankowska, & Wiśniewska, K. (2008). The effect of high pressures on the yoghurt from milk with the stabilizer. Journal of Physics: Conference Series, 121(14), 142007.

    Google Scholar 

  • Reps, A., Warminska-Radyko, I., & Dajnowiec, F. (1999). Effect of high pressure on yoghurt. In H. Ludwig (Ed.), Advances in high pressure bioscience and biotechnology (pp. 453–456). Heidelberg: Springer.

    Chapter  Google Scholar 

  • Ruggirello, M., Cocolin, L., & Dolci, P. (2016). Fate of Lactococcus lactis starter cultures during late ripening in cheese models. Food Microbiology, 59, 112–118.

    Article  CAS  Google Scholar 

  • Samaranayake, C. P., & Sastry, S. K. (2013). In-situ pH measurement of selected liquid foods under high pressure. Innovative Food Science and Emerging Technologies, 17, 22–26.

    Article  CAS  Google Scholar 

  • Shah, N. P., Tsangalis, D., Donkor, O. N., & Versteeg, C. (2008). Effect of high pressure treatment on viability of Lactobacillus delbrueckii ssp. bulgaricus, Streptococcus thermophilus, and L. acidophilus and the pH of fermented milk. Milk Science International, 63(1), 11–14.

    CAS  Google Scholar 

  • Sohier, D., Pavan, S., Riou, A., Combrisson, J., & Postollec, F. (2014). Evolution of microbial analytical methods for dairy industry needs. Frontiers in Microbiology, 5, 16.

    Article  Google Scholar 

  • Trujillo, A. J., Capellas, M., Saldo, J., Gervilla, R., & Guamis, B. (2002). Applications of high-hydrostatic pressure on milk and dairy products: a review. Innovative Food Science and Emerging Technologies, 3(4), 295–307.

    Article  Google Scholar 

  • Ulmer, H. M., Gänzle, M. G., & Vogel, R. F. (2000). Effects of high pressure on survival and metabolic activity of Lactobacillus plantarum TMW1. 460. Applied and Environmental Microbiology, 66(9), 3966–3973.

    Article  CAS  Google Scholar 

  • Vargas, M., Cháfer, M., Albors, A., Chiralt, A., & González-Martínez, C. (2008). Physicochemical and sensory characteristics of yoghurt produced from mixtures of cows’ and goats’ milk. International Dairy Journal, 18(12), 1146–1152.

    Article  CAS  Google Scholar 

  • Vogel, R., & Ehrmann, M. (2008). In C. Michiels, D. Bartlett, & A. Aersten (Eds.), Chapter 7: effects of pressure on lactic acid bacteria. Washington DC: ASM Press. https://doi.org/10.1128/9781555815646.ch7.

    Google Scholar 

  • Walker, M. K., Farkas, D. F., Loveridge, V., & Meunier-Goddik, L. (2006). Fruit yogurt processed with high pressure. International Journal of Food Science & Technology, 41(4), 464–467.

    Article  CAS  Google Scholar 

  • Wang, C. Y., Huang, H. W., Hsu, C. P., & Yang, B. B. (2016). Recent advances in food processing using high hydrostatic pressure technology. Critical Reviews in Food Science and Nutrition, 56(4), 527–540.

    Article  Google Scholar 

  • Zhao, F., Wang, Y., An, H., Hao, Y., Hu, X., & Liao, X. (2016). New insights into the formation of viable but nonculturable Escherichia coli O157: H7 induced by high-pressure CO2. MBio, 7(4), e00961–e00916.

    Article  CAS  Google Scholar 

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Acknowledgments

This work was funded by the INTA-PNAIyAV-1130043 project “Strategies for the food differentiation and for the development of novel food products” and by the INTA-PNAIyAV-1130033 project “Preservation technologies of food and utilization of food by-products.”

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Authors and Affiliations

  1. Instituto Tecnología de Alimentos, Centro de Investigación de Agroindustria, Instituto Nacional de Tecnología Agropecuaria (INTA), Aristizábal y De La Tradición s/n, 1686, Hurlingham, Buenos Aires, Argentina

    Juan Pega, G. I. Denoya, S. R. Vaudagna & M. Nanni

  2. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Av. Rivadavia, 1917, Caba, Argentina

    Juan Pega & S. R. Vaudagna

  3. Centro de Investigaciones Tecnológicas para la Industria Láctea, Instituto Nacional de Tecnología Industrial (INTI Lácteos), Av. General Paz 5445, San Martín, Buenos Aires, Argentina

    M. L. Castells, S. Sarquis & G. F. Aranibar

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  1. Juan Pega
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  2. G. I. Denoya
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Correspondence to Juan Pega.

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Pega, J., Denoya, G.I., Castells, M.L. et al. Effect of High-Pressure Processing on Quality and Microbiological Properties of a Fermented Beverage Manufactured from Sweet Whey Throughout Refrigerated Storage. Food Bioprocess Technol 11, 1101–1110 (2018). https://doi.org/10.1007/s11947-018-2078-5

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  • DOI: https://doi.org/10.1007/s11947-018-2078-5

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