Viability of Probiotic Bacteria in Yogurt Under Cold Storage

Abstract

Probiotic yogurts have many positive health effects, but the number of viable probiotic microorganisms they contain is crucial to their probiotic effect. The viability of probiotic bacteria, which are easily affected by environmental conditions, decreases during processes such as storage, transportation, and preservation of probiotic yogurts. In this study, the viability of probiotic cultures and the physico-chemical changes in yogurts during the shelf life of two different commercial probiotic yogurts (PYA and PYB) and yogurt (PYC) prepared from lyophilized probiotic culture under laboratory conditions were investigated. The experimental setup consisted of three groups with seven samples each, and each sample was analyzed. MRS-galactose and MRS-cysteine media were used to detect Lactobacilli and Bifidobacteria, respectively. Based on the findings obtained, a statistically significant decrease in the number of probiotic bacteria in each sample group was observed during the storage period. In addition, a decrease in the viability of probiotic Lactobacilli and Bifidobacteria in cold stored yogurts was detected until day 22, and a significant decrease on day 28. It was also revealed that the pH in the yogurts decreased during storage, similar to the decrease in the number of probiotic bacteria, reaching the lowest pH value on the 28th day. It was found that the values of dry matter and water activity were similar in all three groups, and with increasing storage time, the value of dry matter increased while the value of water activity decreased. Changes in pH, dry matter, and water activity values were found to influence the viability of probiotic Lactobacilli and Bifidobacteria. In conclusion, considering the physico-chemical changes and viability of bacteria in probiotic yogurts, it is recommended to consume probiotic yogurts with caution after day 22, even if stored in cold conditions, to ensure the expected beneficial effect of these probiotic bacteria.

Keywords

• Bifidobacteria
• lactobacilli
• probiotic yogurt
• viability

Soğuk Koşullarda Muhafaza Edilen Yoğurtlarda Probiyotik Bakterilerin Canlılığı

Öz

Probiyotik yoğurtların sağlık açısından birçok faydalı etkisi bulunmakta, ancak probiyotik etki göstermeleri için içerdikleri probiyotik mikroorganizma miktarının düzeyi önem taşımaktadır. Çevre koşullarından kolaylıkla etkilenen probiyotik bakterilerin canlılığı, probiyotik yoğurtların depolama, transport ve muhafazası gibi işlemler sırasında azalmaktadır. Bu çalışma kapsamında, 2 adet farklı ticari probiyotik yoğurt (PYA ve PYB) ile liyofilize probiyotik kültürden laboratuvar ortamında üretilen yoğurtlardaki (PYC) raf ömrü boyunca probiyotik kültürlerin canlılığı ve yoğurtlardaki fiziko-kimyasal değişimler incelenmiştir. Deneme deseni 3 gruptan tasarlanmış olup her deneme grubu 7 adet örnekten oluşturularak her örnek analize alınmıştır. Laktobasillerin ve Bifidobakterilerin tespiti için sırasıyla MRS-galaktoz ve MRS-sistein besiyerleri kullanılmıştır. Elde edilen bulgular doğrultusunda; her örnek grubundaki probiyotik bakteri sayısında muhafaza süresi boyunca istatistiksel olarak anlamlı bir düşüş saptanmıştır. Ayrıca, soğuk koşullarda muhafaza edilen yoğurtlardaki probiyotik Laktobasillerin ve Bifidobakterilerin canlılığında 22. güne kadar düşme, 28. günde ise önemli düzeyde azalma tespit edilmiştir. Yoğurtlardaki pH seviyelerinin de probiyotik bakteri sayısına benzer şekilde, muhafaza süresince azalma gösterdiği, 28. günde en düşük pH değerine ulaşıldığı ortaya konulmuştur. Kuru madde ve su aktivitesi değerlerinin her 3 grupta benzer şekilde olduğu, muhafaza süresi uzadıkça kuru madde miktarının arttığı, su aktivitesi değerinin ise azaldığı saptanmıştır. pH, kuru madde ve su aktivitesi değerlerinde meydana gelen değişimlerin probiyotik Laktobasillerin ve Bifidobakterilerin canlılığını etkiledikleri belirlenmiştir. Sonuç olarak, probiyotik yoğurtlarda, fiziko-kimyasal değişimler ve bakteri canlılıkları göz önünde bulundurularak, söz konusu probiyotik bakterilerden beklenen faydalı etkilerin görülmesi için soğukta muhafaza edilse dahi, 22nci gün sonrası probiyotik yoğurtların tüketimine dikkat edilmesi önerilmektedir.

Anahtar Kelimeler

• Bifidobakter
• canlılık
• laktobasil
• probiyotik yoğurt

Kaynakça

1. Vural A. (2004). Fonksiyonel Gıdalar ve Sağlık Üzerine Etkileri. Gıda Yem Bil Teknol. 6: 51-58.
2. Terpou A, Papadaki A, Lappa IK, Kachrimanidou V, Bosnea LA, Kopsahelis N. (2019). Probiotics in Food Systems: Significance and Emerging Strategies Towards Improved Viability and Delivery of Enhanced Beneficial Value. Nutrients. 11(7): 1591.
3. Egbuna C, Dable-Tupas G. (2020). Functional Foods and Nutraceuticals. Springer Nature Switzerland AG, Switzerland.
4. Nyanzi R, Jooste PJ, Buys EM. (2021). Invited Review: Probiotic Yogurt Quality Criteria, Regulatory Framework, Clinical Evidence, and Analytical Aspects. J Dairy Sci. 104(1): 1-19.
5. Anonim (2022). Türk Gıda Kodeksi Fermente Süt Ürünleri Tebliği (Tebliğ No: 2022/44) Tarım ve Orman Bakanlığı. 30 Kasım 2022 tarih ve 32029 sayılı Resmi Gazete, Ankara.
6. Reid G. (2010). The Potential Role for Probiotic Yogurt for People Living with HIV/AIDS. Gut Microbes. 1(6): 411-414.
7. Kaur Sidhu M, Lyu F, Sharkie TP, Ajlouni S, Ranadheera CS. (2020). Probiotic Yogurt Fortified with Chickpea Flour: Physico-Chemical Properties and Probiotic Survival During Storage and Simulated Gastrointestinal Transit. Foods. 9(9): 1144.
8. Yadav A, Jaiswal P, Jaiswal M, et al. (2015). Concise Review: Importance of Probiotics Yogurt for Human Health Improvement. IOSR J Environ Sci Toxicol Food Technol. 9(7): 25-30.

9. Rezazadeh L, Alipour B, Jafarabadi MA, Gargari BP. (2020). Evaluation of the Effects of Probiotic Yoghurt on Inflammation and Cardiometabolic Risk Factors in Subjects with Metabolic Syndrome: A Randomised Controlled Trial. Int J Dairy Technol. 101: 104577.
10. Mousavi SN, Saboori S, Asbaghi O. (2020). Effect of Daily Probiotic Yogurt Consumption on Inflammation: A Systematic Review and Meta-Analysis of Randomized Controlled Clinical Trials. Obes Med. 18: 100221.
11. Pourrajab B, Fatahi S, Dehnad A, Varkaneh HK, Shidfar F. (2020). The Impact of Probiotic Yogurt Consumption on Lipid Profiles in Subjects with Mild to Moderate Hypercholesterolemia: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutr Metab Cardiovasc Dis. 30(1): 11-22.
12. Rezazadeh L, Gargari BP, Jafarabadi MA, Alipour B. (2019). Effects of Probiotic Yogurt on Glycemic Indexes and Endothelial Dysfunction Markers in Patients with Metabolic Syndrome. Nutrition. 62: 162-168.
13. Hadjimbei E, Botsaris G, Chrysostomou S. (2022). Beneficial Effects of Yoghurts and Probiotic Fermented Milks and Their Functional Food Potential. Foods. 11(17): 2691.
14. FAO, WHO (2002). Guidelines fort he Evaluation of Probiotics in Food. Food and Agriculture Organization and World Health Organization, London.
15. Boyle RJ, Tang MLK. (2006). The Role of Probiotics in the Management of Allergic Disease. Clin Exp Allergy. 36(5): 568-576.
16. Barengolts E, Smith ED, Reutrakul S, Tonucci L, Anothaisintawee T. (2019). The Effect of Probiotic Yogurt on Glycemic Control in Type 2 Diabetes or Obesity: A Meta-Analysis of Nine Randomized Controlled Trials. Nutrients. 11(3): 671.
17. Afzaal M, Khan AU, Saeed F, et al. (2019). Functional Exploration of Free and Encapsulated Probiotic Bacteria in Yogurt and Simulated Gastrointestinal Conditions. Food Sci Nutr. 7(12): 3931-3940.
18. Lourens-Hattingh A, Viljoen BC. (2001). Yogurt as Probiotic Carrier Food. Int Dairy J. 11(1-2): 1-17.
19. Plessas S, Bosnea L, Alexopoulos A, Bezirtzoglou E. (2012). Potential Effects of Probiotics in Cheese and Yogurt Production: A Review. Eng L ife Sci. 12(4): 433-440.
20. Meybodi NM, Mortazavian AM, Arab M, Nematollahi A. (2020). Probiotic Viability in Yoghurt: A Review of Influential Factors. Int Dairy J, 109: 104793.
21. Hussein ZEH, Silva JM, Alves ES, et al. (2021). Technological Advances in Probiotic Stability in Yogurt: A Review. Res Soc Dev. 10(12): e449101220646-e449101220646.
22. Keshavarzi M, Sharifan A, Yasini Ardakani SA. (2021). Effect of the Ethanolic Extract and Essential Oil of Ferulago angulata (Schlecht.) Boiss. on Protein, Physicochemical, Sensory, and Microbial Characteristics of Probiotic Yogurt During Storage Time. Food Sci Nutr. 9(1): 197-208.
23. Veselá K, Kumherová M, Klojdová I, Solichová K, Horáčková Š, Plocková M. (2019). Selective Culture Medium for the Enumeration of Lactobacillus plantarum in the Presence of Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus Thermophilus. LWT. 114: 108365.
24. Zinedine A, Faid M. (2007). Isolation and Characterization of Strains of Bifidobacteria with Probiotic Proprieties in Vitro. World J Dairy Food Sci. 2(1): 28-34.
25. Shirani K, Falah F, Vasiee A, Yazdi FT, Behbahani BA, Zanganeh, H. (2022). Effects of Incorporation of Echinops setifer Extract on Quality, Functionality, and Viability of Strains in Probiotic Yogurt. J Food Meas Charact. 16(4): 2899-2907.
26. Shortt C. (1999). The Probiotic Century: Historical and Current Perspectives. Trends Food Sci Technol.10(12): 411-417.
27. Arab R, Hano C, Oomah D, et al. (2022). Impact of Carob (Ceratonia Ciliqua L.) Pulp Flour Supplementation on Probiotic Viability, Milk Fermentation and Antioxidant Capacity During Yogurt Storage. NAJFNR. 6(14): 154-164.
28. Tamime AY, Saarela M, Wszolek M, Ghoddousi H, Linares DM, Shah NP. (2018). Production and Maintaining Viability of Probiotic Micro‐Organisms in Dairy Products. In: Probiotic Dairy Products. Tamime AY, Thomas LV (eds). 2nd ed. pp. 67-164. John Wiley & Sons, USA.
29. Soni R, Jain NK, Shah V, Soni J, Suthar D, Gohel P. (2020). Development of Probiotic Yogurt: Effect of Strain Combination on Nutritional, Rheological, Organoleptic and Probiotic Properties. J Food Sci Technol. 57: 2038-2050.
30. Mortazavian AM, Ehsani MR, Mousavi SM, Rezaei K, Sohrabvandi S, Reinheimer JA. (2007). Effect of Refrigerated Storage Temperature on the Viability of Probiotic Micro‐Organisms in Yogurt. Int J Dairy Technol. 60(2): 123-127.
31. Yalçın H, Polat Z. (2023). Lactobacillus acidophilus LA-5 ile Üretilen Probiyotik Yoğurdun Fonksiyonel Özelliği ve Bakteri Canlılığının Uzun Süreli (12 Hafta) Depolamada İncelenmesi. Van Vet J. 34(1): 1-6.
32. Kamel DG, Hammam AR, Alsaleem KA, Osman DM. (2021). Addition of Inulin to Probiotic Yogurt: Viability of Probiotic Bacteria (Bifidobacterium bifidum) and Sensory Characteristics. Food Sci Nutr. 9(3): 1743-1749.
33. Pradeep Prasanna PH, Charalampopoulos D. (2019). Encapsulation in an Alginate–Goats’ Milk–Inulin Matrix Improves Survival of Probiotic Bifidobacterium in Simulated Gastrointestinal Conditions and Goats’ Milk Yoghurt. Int J Dairy Technol. 72(1): 132-141.
34. Shah NP, Lankaputhra WE, Britz ML, Kyle WS. (1995). Survival of Lactobacillus acidophilus and Bifidobacterium bifidum in Commercial Yoghurt During Refrigerated Storage. Int Dairy J. 5(5): 515-521.
35. Ghalemousiani Z, Pourahmad R, Eshaghi MR. (2017). Effect of Aqueous Extracts of Ocimum basilicum and Satureia montana L. on the Survival of Lactobacillus paracasei and Physicochemical Properties of Probiotic Yogurt. J Food Sci Technol. 10(4): 55-63.
36. Ersan LY, Topçuoğlu E. (2019). Badem Sütü ile Zenginleştirilmiş Probiyotik Yoğurtların Mikrobiyolojik ve Bazı Fiziko-Kimyasal Özellikleri. Bursa Uludag Üniv Ziraat Fak Derg. 33(2): 321-339.
37. Karaca OB, Güzeler N, Tangüler H, Yaşar K, Akın MB. (2019). Effects of Apricot Fibre on the Physicochemical Characteristics, the Sensory Properties and Bacterial Viability of Nonfat Probiotic Yoghurts. Foods. 8(1): 33.
38. Shah NP, Ravula RR. (2000). Influence of Water Activity on Fermentation, Organic Acids Production and Viability of Yogurt and Probiotic Bacteria. Aust J of Dairy Technol. 55(3): 127.
39. Suraweera D, Wichchukit S. (2020). Physico-Chemical and Rheological Properties of Plain Yogurt Made From Goat’s Milk During Refrigerated Storage. E3S Web Conf. 187: 04012