Abstract

Ice cream is a product with specific composition and properties that are highly valued by a wide range of consumers. Peculiarities of ice cream composition and production technology make it possible to consider the product as a promising carrier and means of biologically active compounds and useful microorganisms supply. The article reveals morphological, biochemical, physiological, genetic and technological characteristics of L. acidophilus. It systematizes information on the existing methods used for production of ice cream with L. acidophilus. The author shows the influence of various forms of the introduced acidophilus bacteria and methods for their adaptation on ice cream quality indicators. The article provides the data on the properties of ice cream fermented and unfermented with this cultures. It reveals information on the impact of various technological, physicochemical and physiological factors on the survival capacity of pure culture L. acidophilus and its combination with other microorganisms in the process of ice cream production, storage and consumption. The author considers perspective ways of acidophilic ice cream production using various combinations of prebiotics, dietary fibers, replacing refined sugar with honey and unrefined sugars, introducing whey proteins, fruit puree, grain additives and other ingredients. The article presents the data on the influence of functional components on the production process and properties of ice cream containing acidophilus bacteria. The author systematized information on ice cream production using different strains of L. acidophilus and Bifidobacterium spp. replacing cowʼs milk with vegetable analogues. Methods for producing ice cream with L. acidophilus and other starter cultures, including yogurt cultures are described. The review justifies practicability of L. acidophilus application in ice cream production. It reveals trends and issues in the area of functional use ice cream production.

Keywords

Ice cream, L. acidophilus, probiotics, prebiotics, synbiotics

REFERENCES

1. Granato D., Branco G.F., Cruz A.G., Faria J.A.F., Shah N.P. Probiotic dairy products as functional foods. Food Science and Food Safety, 2010, vol. 9, no. 5, pp. 455–470. https://doi.org/10.1111/j.1541-4337.2010.00120.x.
2. Cruz A.G., Antunes A.E.C., Sousa A.L.O.P., Faria J.A.F, Saad S.M.I. Ice cream as a probiotic food carrier. Food Research International, 2009, vol. 42, pp. 1233–1239. https://doi.org/10.1016/j.foodres.2009.03.020.
3. Homayouni A., Alizadeh M., Alikhah H., Zijah V. Functional dairy probiotic food development: trends, concepts, and products. In: E. Rigobelo ed. Probiotics. London: IntechOpen, 2012, pp. 978–953. https://doi.org/10.5772/48797.
4. Soukoulis C., Fisk I.D., Bohn T. Ice cream as a vehicle for incorporating health-promoting ingredients: conceptualization and overview of quality and storage stability aspect. Food Science and Food Safety, 2014, vol. 13, pp. 627–655. https://doi.org/10.1111/1541-4337.12083.
5. Hill C., Guarner F., Reid G., et al. Expert consensus document: the international scientific association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Gastroenterology and Hepatology, 2014, vol. 11, no. 8, pp. 506–514. https://doi.org/10.1038/nrgastro.2014.66.
6. Pandey K.R., Naik S.R., Vakil B.V. Probiotics, prebiotics and synbiotics-a review. Food Science and Technology, 2015, vol. 52, no. 12, pp. 7577–7587. https://doi.org/10.1007/s13197-015-1921-1.
7. Markowiak P., Slizewska K. Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients, 2017, vol. 9, no. 9, pp. 897–908. https://doi.org/10.3390/nu9091021.
8. Kim N., Yun M., Oh Y.J., Choi H.J. Mind-altering with the gut: modulation of the gut-brain axis with probiotics. Journal of Microbiology, 2018, vol. 56, no. 3, pp. 172–182. https://doi.org/10.1007/s12275-018-8032-4.
9. Wan M.L.Y., Ling K.H., El-Nezami H., Wang M.F. Influence of functional food components on gut health. Critical Reviews in Food Science and Nutrition, 2018, pp. 1–10. https://doi.org/10.1080/10408398.2018.1433629.
10. Kanauchi O., Andoh A., AbuBakar S.,Yamamoto N. Probiotics and paraprobiotics in viral infection: clinical application and effects on the innate and acquired immune systems. Current Pharmaceutical Design, 2018, vol. 24, pp. 1–8. https://doi.org/10.2174/1381612824666180116163411.
11. Evivie S.E., Huo G.C., Igene J.O., Bian X. Some current applications, limitations and future perspectives of lactic acid bacteria as probiotics. Food and Nutritional Research, 2017, vol. 61, no. 1. https://doi.org/10.1080/16546628.2017.1318034.
12. Bull M., Plummer S., Marchesi J., Mahenthiralingam E. The life history of Lactobacillus acidophilus as a probiotic: a tale of revisionary taxonomy, misidentification and commercial success. FEMS Microbial Letters, 2013, vol. 349, no. 2, pp. 77–87. https://doi.org/10.1111/1574-6968.12293.
13. Homayouni A., Azizi A., Javadi M., Mahdipour S., Ejtahed H. Factors influencing probiotic survival in ice cream: a review. Dairy Science, 2012, vol. 7, pp. 1–10. https://doi.org/10.3923/ijds.2012.1.10.40.
14. Soukoulis C., Lyroni E., Tzia C. Sensory profiling and hedonic judgement of probiotic ice cream as a function of hydrocolloids, yogurt and milk fat content. LWT - Food Science and Technology, 2010, vol. 3, no. 9, pp. 1351–1358. https://doi.org/10.1016/j.lwt.2010.05.006.
15. Linares D.M., Gomez C., Renes E., et al. Lactic acid bacteria and Bifidobacteria with potential to design natural biofunctional health-promoting dairy foods. Frontiers in Microbiology, 2017, vol. 8. https://doi.org/10.3389/fmicb.2017.00846.
16. Fijan S. Microorganisms with claimed probiotic properties: an overview of recent literature. Environmental Research and Public Health, 2014, vol. 11, no. 5, pp. 4745–4767. https://doi.org/10.3390/ijerph110504745.
17. Hammes W.P., Hertel C. The genera Lactobacillus and Carnobacterium, In: Dworkin M., Falkow S., Rosenberg E., Schleifer K.-H., Stackebrandt E. (eds) The Prokaryotes, Vol. 4, 3rd ed. New York: Springer, 2006, pp. 320–403.
18. Altermann E., Russell W.M., Azcarate-Peril M.A. Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proceedings of the National Academy of Sciences of the United States of America, 2005, vol. 102, no. 11, pp. 3906–3912. https://doi.org/10.1073/pnas.0409188102.
19. Shah N.P. Functional cultures and health benefits. International Dairy Journal, 2007, vol. 17, no. 11, pp. 1262–1277. https://doi.org/10.1016/j.idairyj.2007.01.014.
20. Suskovic J., Kos B., Beganovic J., et al. Antimicrobial activity-the most important property of probiotic and starter lactic acid bacteria. Food Technology and Biotechnology, 2010, vol. 48, no. 3, pp. 296–307.
21. Anjum N., Maqsood S., Masud T., et al. Lactobacillus acidophilus: characterization of the species and application in food production. Food Science and Nutrition, 2014, vol. 54, no. 9, pp. 1241–1251. https://doi.org/10.1080/10408398.2011.621169.
22. Sanders M.E., Klaenhammer T.R. Invited review: the scientific basis of Lactobacillus acidophilus NCFM functionality as a probiotic. Dairy Science, 2001, vol. 84, no. 2, pp. 319–331.
23. Registr lekarstvennyh sredstv Rossii. Laktobakterii acidofilʼnye (Lactobacillus acidophilus) [Russian pharmaceutical products register. Lactobacillus acidophilus (Lactobacillus acidophilus)]. Available at: https://www.rlsnet.ru/mnn_index_id_3502.htm. (accessed 3 February 2018).
24. Feklisova L.V. Primeneniye laktozosoderzhashchikh probiotikov: otsenka mnogoletnego ispol’zovaniya Atsipola v pediatricheskoy praktike. [Lactose-containing prebiotics application: evaluation of Acipol long-term application in pediatrics]. Consilium Medicum. Pediatriya (Prilozheniye) [Consilium Medicum. Pediatria (Appendix)], 2007, no. 2, pp. 123–127.
25. Ivashkina N.Yu., Botina S.G. Original’nyy otechestvennyy probiotik atsipol: molekulyarno-biologicheskiye i metabolicheskiye kharakteristiki [Original Russian probiotic Acipol: molecular-biologic and metabolic characteristics]. Rossiyskiy zhurnal gastroenterologii, gepatologii, koloproktologii [The Russian Journal of Gastroenterology, Hepatology, Coloproctology], 2009, no. 2, pp. 58–64.
26. Kneifel W., Bonaparte C. Acidophilus milk. Encyclopedia of food sciences and nutrition. 2nd ed. San Diego: Academic Press, 2003. 6406 p.
27. Bannikova L.A., Koroleva N.S., Semenihina V.F. Mikrobiologicheskie osnovy molochnogo proizvodstva [Microbiological basics of dairy products production]. Moscow: Agropromizdat Publ., 1987. 400 p.
28. Polyanskaya I.S., Stoyanova L.G., Semenihina V.F. Antagonisticheskaya aktivnost’ probioticheskikh shtammov: faktory regulirovaniya [Antagonitic activity of probiotic strains: factors of regulation]. Molochnaya promyshlennostʼ [Dairy Industry], 2017, no. 1, pp. 42–44.
29. Grunskaya V.A., Koneva D.A. Tvorozhnyye produkty, obogashchennyye probioticheskoy mikrofloroy [Curds products enriched with probiotic microflora]. Molochnaya promyshlennostʼ [Dairy Industry], 2017, no. 8, pp. 41–43.
30. Donskaya G.A., Drozhzhin V.M., Morozova V.V. Napitki kislomolochnyye, obogashchennyye syvorotochnymi belkami [Fermented milks fortified with whey proteins]. Molochnaya promyshlennostʼ [Dairy Industry], 2017, no. 6, pp. 68–70
31. Akhmedova V.R., Ryabtseva S.A., Shpak M.A. Nauchnoye obosnovaniye sposoba polucheniya kislomolochnogo morozhenogo s prebioticheskimi komponentami [Scientific rationale for producing fermented ice cream with prebiotic components]. Tekhnika i tekhnologiya pishchevykh proizvodstv [Food Processing: Techniques and Technology], 2015, no. 4, pp. 5–11.
32. Dianawati D., Lim S.F., Ooi Y.B., Shah N.P. Effect of type of protein-based microcapsules and storage at various ambient temperatures on the survival and heat tolerance of spray dried Lactobacillus acidophilus. Food Science, 2017, vol. 82, no. 9, pp. 2134–2141. https://doi.org/10.1111/1750-3841.13820.
33. Barat A., Ozcan T. Growth of probiotic bacteria and characteristics of fermented milk containing fruit matrices. Dairy Technology, 2017, vol. 116, no. 1, pp. 174–181. https://doi.org/10.1111/1471-0307.12391.
34. Ozcan T., Yilmaz-Ersan L., Akpinar-Bayizit A., Delikanli B. Antioxidant properties of probiotic fermented milk supplemented with chestnut flour (Castanea sativa Mill). Food Processing Preservation, 2017, vol. 41, no. 5, pp. 1–9. https://doi.org/10.1111/jfpp.13156.
35. Neish A.S. Probiotics of the acidophilus group: Lactobacillus acidophilus, Delbrueckii subsp. bulgaricus and Johnsonii. The Microbiota in Gastrointestinal Pathophysiology, 2017, pp. 71–78. https://doi.org/10.1016/B978-0-12-804024-9.00006-9.
36. Crovesy L., Ostrowski M., Ferreira D.M.T.P., Rosado E.L., Soares-Mota M. Effect of Lactobacillus on body weight and body fat in overweight subjects: a systematic review of randomized controlled clinical trials. Obesity Reviews, 2017, vol. 41, no. 11, pp. 1607–1614. https://doi.org/10.1038/ijo.2017.161.
37. Wu Z., Wang G., Wang W., et al. Proteomics analysis of the adhesion activity of Lactobacillus acidophilus ATCC 4356 upon growth in an intestine-like pH environment. Proteomics, 2018, vol. 18, no. 5-6. https://doi.org/10.1002/pmic.201700308.
38. Yang K., Duley M.L., Zhu J. Metabolomics study reveals enhanced inhibition and metabolic dysregulation in Escherichia coli induced by Lactobacillus acidophilus-fermented black tea extract. Agricultural and Food Chemistry, 2018, vol. 6, pp. 1386–1393. https://doi.org/10.1021/acs.jafc.7b04752.
39. Chung W.H., Kang J., Lim M.Y., et al. Complete genome sequence and genomic characterization of Lactobacillus acidophilus LA-1 (11869BP). Frontiers in Pharmacology, 2018, vol. 9, no. 83. https://doi.org/10.3389/fphar.2018.00083.
40. El-Deeb N.M., Yassin A.M., Al-Madboly L.A., El-Hawiet A. A novel purified Lactobacillus acidophilus 20079 exopolysaccharide, LA-EPS-20079, molecularly regulates both apoptotic and NF-kB inflammatory pathways in human colon cancer. Microbial Cell Factories, 2018, vol. 17, no. 29. https://doi.org/10.1186/s12934-018-0877-z.
41. Homayouni A., Ehsani M.R, Azizi A, Razavi S.H., Yarmand M.S. Growth and survival of some probiotic strains in simulated ice cream conditions. Applied Sciences, 2008, vol. 8, no. 2, pp. 379–382. https://doi.org/10.3923/jas.2008.379.382.
42. Senaka R.C., Evansa C.A., Adams M.C., Baines S.K. In vitro analysis of gastrointestinal tolerance and intestinal cell adhesion of probiotics in goatʼs milk ice cream and yogurt. Food Research International, 2012, vol. 49, no. 2, pp. 619–625. https://doi.org/10.1016/j.foodres.2012.09.007.
43. Chiquetti R.L., Castro E.M., Valerio G.D., et al. Viability of the probiotic Lactobacillus acidophilus LA-5 in ice cream: effect of lactose hydrolysis and overrun. Food Research International, 2016, vol. 23, no. 6, pp. 2631–2637.
44. Chaikham P., Rattanasena P. Combined effects of low-fat ice cream supplemented with probiotics on colon microfloral communities and their metabolites during fermentation in a human gut reactor. Food Bioscience, 2017, vol. 17, pp. 35–41. https://doi.org/10.1016/j.fbio.2016.12.005.
45. Nousia F.G., Androulakis P.I., Fletouris D.J. Survival of Lactobacillus acidophilus LMGP-21381 in probiotic ice cream and its influence on sensory acceptability. Dairy Technology, 2011, vol. 64, pp. 130–136. https://doi.org/10.1111/j.1471-0307.2010.00645.x.
46. Arslan A.A., Gocer E.M.C., Demir M., et al. Viability of Lactobacillus acidophilus ATCC 4356 incorporated into icecream using three different methods. Dairy Science and Technology, 2016, vol. 96, pp. 477–487. https://doi.org/10.1007/s13594-016-0282-5.
47. Ergina F., Atamer Z., Arslan A.A., et al. Application of cold-and heat-adapted Lactobacillus acidophilus in the manufacture of ice cream. International Dairy Journal, 2016, vol. 59, pp. 72–79. https://doi.org/10.1016/j.idairyj.2016.03.004.
48. Abghari A., Sheikh-Zeinoddin M., Soleimanian-Zad S. Nonfermented ice cream as a carrier for Lactobacillus acidophilus and Lactobacillus rhamnosus. Food Science and Technology, 2011, vol. 46, pp. 84–92. https://doi.org/10.1111/j.1365-2621.2010.02453.x
49. Ferraz J.L., Cruz A.G., Cadena R.S., et al. Sensory acceptance and survival of probiotic bacteria in ice cream produced with different overrun levels. Food Science, 2012, vol. 71, pp. 24–28. https://doi.org/10.1111/j.1750-3841.2011.02508.x.
50. Arsen’yeva T.P. Spravochnik tekhnologa molochnogo proizvodstva. Tekhnologiya i retseptury. T. 4. Morozhenoye [Dairy production engineer reference book. Technology and recipes. Vol. 4. Ice Cream]. St.Petersburg: GIORD Publ., 2002. 184 p.
51. Akhmedova V.R., Ryabtseva S.A., Evdokimov I.A., Anisimov G.S. Vliyaniye vida zakvasochnoy mikroflory na svoystva smesi dlya kislomolochnogo morozhenogo [Influence of type starter culture on the properties of the fermented ice cream mixture]. Vestnik Severo-Kavkazskogo federalʼnogo universiteta [Newsletter of North-Caucasus State Technical University], 2013, no. 6, pp. 84–87.
52. Khramtsov A.G., Ryabtseva S.A., Budkevich R.O., et al. Prebiotiki kak funktsional’nyye pishchevyye ingrediyenty: terminologiya, kriterii vybora i sravnitel’noy otsenki, klassifikatsiya [Prebiotics as functional food ingredients: terminology, choice and comparative evaluation criteria, classification]. Voprosy pitaniya [Nutricion Problems], 2018, vol. 87, no. 1, pp. 5–17.
53. Pandiyan C., Annal Villi R., Kumaresan G., Murugan B, Gopalakrishnamurthy T.R. In vivo and in vitro effect of Lactobacillus acidophilus in synbiotic ice cream enriched with whey protein concentrate. International Food Research Journal, 2012, vol. 19, no. 2, pp. 441–446.
54. Senanayake S.A., Fernando S., Bamunuarachchi A., Arsekularatne M. Application of Lactobacillus acidophilus (LA-5) strain in fruit-based ice cream. Food Science and Nutrition, 2013, vol. 1, no. 6, pp. 428–431. https://doi.org/10.1002/fsn3.66.
55. Greenbaum A., Aryana K.J. Effect of honey a natural sweetener with several medicinal properties on the attributes of a frozen dessert containing the probiotic Lactobacillus acidophilus. Open Journal of Medical Microbiology, 2013, vol. 3, no. 2, pp. 95–99. https://doi.org/10.4236/ojmm.2013.32015.
56. Low R.H.P., Baba A.S., Aboulfazli F. Effects of different levels of refined cane sugar and unrefined coconut palm sugar on the survivability of Lactobacillus acidophilus in probiotic ice cream and its sensory and antioxidant properties. Food Science and Technology Research, 2015, vol. 21, no. 6, pp. 857–862. https://doi.org/10.3136/fstr.21.857.
57. Parussoloa G., Busatto R.T., Schmitt J., et al. Synbiotic ice cream containing yacon flour and Lactobacillus acidophilus NCFM LWT. Food Science and Technology, 2017, vol. 82, pp. 192–198. https://doi.org/10.1016/j.lwt.2017.04.049.
58. Hekmat S., McMahon D.J. Survival of Lactobacillus acidophilus and Bifidobacterium bifidum in ice cream for use as a probiotic food. Dairy Science, 1992, vol. 75, no. 6, pp. 1415–1422. https://doi.org/10.3168/jds.S0022-0302(92)77895-3.
59. Corrales A., Henderson M., Morales I. Survival of probiotic microorganisms Lactobacillus acidophilus and Bifidobacterium lactis in whipped ice cream. Revista Chilena de Nutrición, 2007, vol. 34, no. 2, pp. 157–163.
60. Akalın A.S., Erisir D. Effects of inulin and oligofructose on the rheological characteristics and probiotic culture survival in low-fat probiotic ice cream. Food Science, 2008, vol. 73, no. 4, pp. 184–188. https://doi.org/10.1111/j.1750-3841.2008.00728.x.
61. Golestani M., Pourahmad R. Comparison of three treatments (two fermented treatments and one nonfermented treatment) in production of synbiotic ice cream. Food Processing and Preservation, 2016, vol. 41, no. 2, pp. 128–139. https://doi.org/10.1111/jfpp.12839.
62. Ayar A., Sicramaz H., Ozturk S., Ozturk Y.S. Probiotic properties of ice creams produced with dietary fibres from by-products of the food industry. Dairy Technology, 2017, vol. 71, no. 1, pp. 174–182. https://doi.org/10.1111/1471-0307.12387.
63. Akalin A.S., Kesenkas H., Dinkci N., et al. Enrichment of probiotic ice cream with different dietary fibers: structural characteristics and culture viability. Dairy Science, 2018, vol. 101, no. 1, pp. 37–46. https://doi.org/10.3168/jds.2017-13468.
64. Vasconcelos B.G., Martinez R.C.R., Alves de Castro I., Saad S.M.I. Innovative açaí (Euterpe oleracea, Mart., Arecaceae) functional frozen dessert exhibits high probiotic viability throughout shelf-life and supplementation with inulin improves sensory acceptance. Food Science and Biotechnology, 2014, vol. 23, no. 6, pp 1843–1849. https://doi.org/10.1007/s10068-014-0252-8.
65. Aboulfazli F., Baba A.S. Effect of vegetable milk on survival of probiotics in fermented ice cream under gastrointestinal conditions. Food Science and Technology Research, 2015, vol. 21, no. 3, pp. 391–397. https://doi.org/10.3136/fstr.21.391.
66. Aboulfazli F., Shori A.B., Baba A.S. Effects of the replacement of cow milk with vegetable milk on the count of probiotics and changes in sugar and amino acid contents in fermented ice creams. Food Science and Technology, 2016, vol. 70, pp. 261–270. https://doi.org/10.1016/j.lwt.2016.02.056.
67. Matias N.S., Padilha M, Bedani R., Saad S.M.I. In vitro gastrointestinal resistance of Lactobacillus acidophilus LA-5 and Bifidobacterium animalis BB-12 in soy and/or milk-based synbiotic apple ice creams. Food Microbiology, 2016, vol. 234, pp. 83–93.
68. Akin M.B., Akin M.S., Kirmaci Z. Effects of inulin and sugar levels on the viability of yogurt and probiotic bacteria and the physical and sensory characteristics in probiotic ice cream. Food Chemistry. 2007, vol. 104, no. 1, pp. 93–99. https://doi.org/10.1016/j.foodchem.2006.11.030.
69. Ranadheera S., Evans C.A., Adams M.C., Baines S.K. Production of probiotic ice cream from goatʼs milk and effect of packaging materials on product quality. Small Ruminant Research, 2013, vol. 112, pp. 174–180. https://doi.org/10.1016/j.smallrumres.2012.12.020.
70. Rezaei R., Khomeiri M., Aalami M., Kashaninejad M. Effect of inulin on the physicochemical properties, flow behavior and probiotic survival of frozen yogurt. Food Science and Technology, 2014, vol. 51, no. 10, pp. 2809–2814. https://doi.org/10.1007/s13197-012-0751-7.
71. Pandiyan C., Annal V.R., Kumaresan G., Murugan B., Gopalakrishnamurthy T.R. Development of synbiotic ice cream incorporating Lactobacillus acidophilus and Saccharomyces boulardii. International Food Research Journal, 2012, vol. 19, no. 3, pp. 1233–1239.
72. Ahmadi A., Milani E., Madadlou A., et al. Synbiotic yogurt-ice cream produced via incorporation of microencapsulated Lactobacillus acidophilus (LA-5) and fructooligosaccharide. Food Science and Technology, 2014, vol. 51, no. 8, pp. 1568–1574. https://doi.org/10.1007/s13197-012-0679-y.
73. Phuapaiboon P. Immobilization of probiotic bacteria with banana flour and effect on quality of synbiotic ice cream and survival under simulated gastrointestinal conditions. Carpathian journal of food science and technology, 2016, vol. 8, no. 4, pp. 33–46.