Probiotics in anthocyanin-rich fruit beverages: research and development for novel synbiotic products

Figures & data

Figure 1. General stages of the development of probiotic fruit beverages.

Table 1. Anthocyanin content of berries commonly used in the production of juices and beverages.

Fruit/Berry	Taxon	Total content of anthocyanins (mg/100 g FW)	Specific identified anthocyanins	Reference
Blackberry	Rubus fructicosus	94.76-199.37	Cy-Glc*, Cy-Xyl, Cy-Myl-Glc, Cy-Dly-Glc, Cy-Smb	(Zia-Ul-Haq et al. 2014 ; Ali et al. 2011; Ponder et al. 2021)
	Rubus glaucus	30.8-175.7	Cy-Rut*, Cy-Glc, Cy-Xyl-Rut	(Horvitz, Chanaguano, and Arozarena 2017)
	Rubus jamaicensis	1673	Cy-Glc*, Cy-Glc-Mle	(Bowen-Forbes, Zhang, and Nair 2010)
Strawberry	Fragaria ananassa	22.68-100.48	Pel-Glc*, Pel-Myl-Glc, Pel-Gal, Cy-Smb, Cy-Ara, Cy-Glc	(Bordonaba, Crespo, and Terry 2011; Veberic et al. 2015)
	Fragaria vesca	69-112.15	Pel-Myl-Glc*, Pel-Glc, Pel-Gal, Cy-Smb, Cy-Ara, Cy-Glc.	(Veberic et al. 2015; Dzhanfezova et al. 2020)
Raspberry	Rubus idaeus	46.76-89.54	Cy-Sph*, Cy-Glc-Rut, Cy-Glc, Cy-Rut, Pel-Glc	(Kubota et al. 2012; Szymanowska, Baraniak, and Bogucka-Kocka 2018 ; Ponder et al. 2021)
	Rubus occidentalis	328.51-1023.03	Cy-Glc*, Cy-Smb, Cy-Xyl-Rut, Cy-Rut.	(Kula and Krauze-Baranowska 2016; Ryu and Koh 2018
	Rubus rosifolius	146-287.4	Pel-Glc*, Pel-Rut, Cy-Glc	(Bowen-Forbes, Zhang, and Nair 2010; Rambaran and Bowen-Forbes 2020)
	Rubus racemosus	1812	Cy-Glc*, Cy-Rut	(Bowen-Forbes, Zhang, and Nair 2010)
Blueberry	Vaccinium floribundum	252.51	Cy-Pen*, Cy-Hex, Del-Hex, Del-Pen	(Reque et al. 2014; Esquivel-Alvarado et al. 2020)
	Vaccinium corymbosum	76.14-84.25	Mal-Gal*, Cy-Gal, Del-Gal	(Ponder et al. 2021)
	Vaccinium myrtillus	438-767.85	Del-Glc*, Del-Gal, Cy-Ara, Del-Ara, Pet-Gal	(Müller, Schantz, and Richling 2012; Veberic et al. 2015)
Mulberry	Morus alba	88.2-556.5	Cy-Glc*, Cy-Rut, Pel-Rut	(Chen et al. 2022)
	Morus nigra	213.38	Cy-Glc*, Cy-Rut, Pel-Glc, Pel-Rut	(Kamiloglu et al. 2013; Veberic et al. 2015)
	Morus rubra	71.05	Cy-Glc*, Cy-Rut, Pel-Glc	(Byamukama et al. 2014; Wang 2014)
Cranberry	Vaccinium macrocarpon	16.7-24.2	Cy-Gal*, Cy-Glc, Cy-Ara	Brown and Shipley 2011; Veberic et al. 2015)
	Vaccinium oxycoccus	186	Cy-Glc*, Cy-Ara, Cy-Gal, Pet-Gal, Peo-Ara	(Brown et al. 2012)
	Vaccinium vitis-idaea	310	Cy-Gal*, Cy-Ara, Cy-Glc.	(Brown et al. 2012)
Elderberry	Sambucus nigra	20.47-801.49	Cy-Glc*, Cy-Smb, Cy-Di-Glc, Cy-Smb-Glc, Cy-Rut, Cy-Gal	(Mikulic-Petkovsek et al. 2014; Veberic et al. 2015)
	Sambucus cerulea	148.63	Cy-Pen-Hex*, Cy-Glc, Cy-Smb.	(Mikulic-Petkovsek et al. 2014)
	Sambucus ebulus	353.37	Cy-Pen-Hex*, Cy-Glc, Cy-Smb.	(Mikulic-Petkovsek et al. 2014)
Agraz or Andean blueberry	Vaccinium meridionale	188.3	Cy-Gal*, Cy-Ara, Del-Hex, Del-Pen, Cy-Glc	(Garzón et al. 2010)
Corozo	Bactris guineensis	156.14	Cy-Rut*, Cy-Glc, Peo-Rut, Cy-Myl-Glc, Cy-Smb, Peo-Glc	(Osorio et al. 2010; Erşan et al. 2020)
Grape	Vitis labrusca	17.5-135.9	Mal-Di-Glc*, Peo-Di-Glc, Pet-Di-Glc, Del-Di-Glc	(Lago-Vanzela et al. 2011; Koyama et al. 2014)
	Vitis vinifera	8.6-379.3	Mal-Gal*, Mal-Gal, Del-Glc, Pet-Glc, Del-Ace-Glc, Pet-Gal, Mal-Ara, Cy-Ara	(Liang et al. 2008; Wu et al. 2012)
Pomegranate	Punica granatum	11-192.5	Pel-Di-Glc*, Cy-Glc, Cy-Di-Glc, Del-Di-Glc, Pel-Glc, Del-Glc.	(Gómez-Caravaca et al., 2013; Fanali et al., 2016)
Blackcurrant	Ribes nigrum	65.57	Del-Rut*, Cy-Rut, Del-Glc, Cy-Glc	(Ali et al. 2011; Veberic et al. 2015)
Juçara	Euterpe edulis	1552.8	Cy-Rut*, Cy-Glc, Pel-Glc	(Vieira et al., 2017)
Açaí	Euterpe oleraceae	8.96-86.03	Cy-Rut*, Cy-Glc, Peo-Rut, Pel-Glc, Pel-Rut, Peo-Glc	(Gouvêa et al., 2012; Mulabagal et al., 2012; Garzón et al., 2017)
Cherry	Prunus cerasus	12.90-96.69	Cy-Glc-Rut*, Cy-Rut, Cy-Sph, Cy-Glc	(Dóka et al., 2011; Okur et al., 2019)
	Cornus mas	96.24	Pel-Glc*, Pel-Rut, Cy-Gal	(Moldovan et al., 2016; David et al., 2019)

* Predominant anthocyanins. FW: fresh weight. Cy: cyanidin. Pel: pelargonidin. Del: delphinidin. Mal: malvidin. Pet: petunidin. Peo: peonidin. Glc: 3-glucoside. Gal: 3-galactoside. Ara: 3-arabinoside. Rut: 3-rutinoside. Smb: 3-sambubioside. Sph: 3-sophoroside. Xyl: 3-xyloside. Myl-Glc: 3-malonylglucoside. Dly-Glc: 3-dioxalylglucoside. Xyl-Rut: 3-xylosylrutinoside. Glc-Mle: 3-glucosylmalonate. Glc-Rut: 3-glucosylrutinoside. Di-Glc: 3,5-diglucoside. Smb-Glc: 3-sambubiosyl-5-glucoside. Pen: pentoside. Hex: hexoside.

Table 2. Studies carried out on the development of probiotics and synbiotic beverages with anthocyanin-rich fruits.

Matrix	Probiotic	Prebiotic	Bioprocess conditions	Viability*	Reference
Without fermentation
Commercial fruit juices of blackcurrant, pomegranate, and strawberry	Bifidobacterium longum	–	Storage at 4 °C for 6 weeks	Initial: 8 log CFU/mL Final: 7.3 log CFU/mL for blackcurrant and ND for pomegranate and strawberry	(Nualkaekul, Salmeron, and Charalampopoulos 2011)
Commercial cranberry juice	Ligilactobacillus salivarius, Lacticaseibacillus paracasei Lacticaseibacillus rhamnosus, Lacticaseibacillus casei and Bifidobacterium animals ssp. lactis	–	Initial pH unadjusted and adjusted to 3.5, 4.5, and 5.5 using NaOH Storage at 4 °C for 9 days	Initial: 8 log CFU/mL Final: ND without pH adjusted and 7 log CFU/mL at higher pH (for L. paracasei )	(Sheehan, Ross, and Fitzgerald 2007)
Banana (40%), strawberry (40%), and juçara (20%) blend beverage	B. animalis subsp. lactis, Lactobacillus acidophilus, L. casei and Lactiplantibacillus plantarum	–	Storage at 4 °C for 90 days	Initial: 8-10 log CFU/mL Final: 7 log CFU/mL (L. casei), 6 log CFU/mL (L. plantarum) and 4 log CFU/mL (L. acidophilus and B. animalis)	(de Oliveira et al. 2020)
Commercial red fruit juice (20% red-orange, 20% blueberry, 10% pomegranate)	Limosilactobacillus reuteri adapted	–	Storage at 4 °C for 22 days Strain adapted in MRS broth supplemented with 5,10 and 50% red fruit juice	Initial: 8-9 log CFU/mL Final: 3-5 log CFU/mL	(Perricone et al. 2014)
Blackberry concentrate (10-12%)	L. casei	Inulin (2.78-3.68%)	Storage at 4 °C for 48 h	Initial: 5.74 − 7.79 log CFU/g Final: 4.15 − 7.13 log CFU/g	(Marín-Arango et al. 2019)
Commercial pomegranate juice	B. animalis subsp. lactis	XOS Obtained from sugar cane bagasse	Storage at 4 °C for 30 days	Initial: 8 log CFU/mL Final: 6 log CFU/mL with XOS and 5 log CFU/mL without XOS	(Hesam et al. 2020)
Juçara sorbet (41-38%)	L. acidophilus and L. paracasei	Polydextrose (8%)	storage at −18 °C for 120 days	Initial: 8.5 log CFU/mL Final: 8.8 log CFU/mL for both microorganisms and with and without polydextrose	(Urbano et al. 2019)
Commercial pomegranate and cranberry juices	L.s plantarum y B. longum encapsulated within alginate or pectin coated with chitosan, gelatin, or glucomannan		Storage at 4 °C for 6 weeks	Initial: 8.5 log CFU/mL Final: >7 log CFU/mL for pomegranate and >5 log CFU/mL for cranberry	(Nualkaekul et al. 2013)
Raspberry juice	L. casei microencapsulated in alginate	–	Storage at 4 °C for 28 days	Initial: 7 log CFU/mL Final: 5 log CFU/mL for microencapsulated and ND for free probiotic	(Olivares et al. 2019)
Commercial pomegranate juice	L. plantarum encapsulated in alginate and chitosan	–	Storage at 4 °C for 6 weeks	Initial: 8.6 log CFU/mL Final: 5.7 − 6.6 log CFU/mL for encapsulated and ND for free probiotic	(Nualkaekul et al. 2012)
Commercial cranberry and pomegranate juices	L. rhamnosus encapsulated in whey protein coated with pectins, alginate, carrageenan, or inulin	inulin	Storage at 4 °C and 25 °C for 14 days	Initial: 9 log CFU/mL Final: > 6 log CFU/mL Coating with apple pectin presented better viability	(Doherty et al. 2012)
Hawthorn berry tea (2%)	L. rhamnosus microencapsulated with a mixture of alginate, pectin, and flaxseed mucilage	flaxseed mucilage	Storage at 4 °C and 25 °C for 4 weeks	Initial: 10 log CFU/mL Final: 6 log CFU/mL (4 ° C) and 2 log CFU/mL (25 ° C) in free probiotic and 9 log CFU/mL (4 ° C) and 8 log CFU/mL (25 ° C) in encapsulated probiotic	(Lai, How, and Pui 2020)
with fermentation
Red smoothie (26% cherries, 8% tomatoes, 5% blackberries, 31% prunes, 20% grape juice, and 10% Aloe vera)	Pediococcus pentosaceus, L. plantarum and Weissella cibaria isolated from different fruits conglomerate	–	Fermentation at 25 °C for 24 h Storage at 4 °C for 30 days	Initial: 7 log CFU/mL At the end of fermentation: 9.5 log CFU/mL At the end of storage: 9 log CFU/mL	(di Cagno et al. 2011)
Blueberry pomace in distilled water (5%)	One culture of L. rhamnosus and two of L. plantarum axenic and conglomerate	–	Addition of glucose, fructose, maltose and sucrose. Initial pH adjusted to 6.2 with Na2CO3. Fermentation at 37 °C for 24 h	Initial: 7.5 log CFU/mL At the end of fermentation: >10 log CFU/mL	(Yan et al. 2019)
Blueberry and blackberry juices	L. plantarum, Streptococcus thermophilus, and Bifidobacterium bifidum	–	Initial pH adjusted to 3 with Na2CO3 Fermentation at 37 °C for 48 h	Initial: 7 log CFU/mL Final: 8 log CFU/mL	(Wu et al. 2021)
Pomegranate juice	L. casei	–	Fermentation at 37 °C for 24 h	Initial: 10.4 log CFU/mL Final: 10.3 log CFU/mL	(Mustafa, Chua, and El-Enshasy 2019)
Pomegranate juice	L. casei	–	Fermentation at 37 °C for 48 h with 5% CO2	Initial: 4-5 log CFU/mL Final: 6-8 log CFU/mL	(Fazeli et al. 2011)
Pomegranate juice	L. plantarum, Lactobacillus. delbruekii , L. paracasei and L. acidophilus	–	Fermentation at 30 °C for 72 h Storage at 4 °C for 2 weeks	Initial: 7 log CFU/mL At the end of fermentation: 8 log CFU/mL At the end of storage: 5 log CFU/mL (L plantarum and L. delbrueckii)	(Mousavi et al. 2011)
Red fruit beverage (20% strawberry, 10% blackberry, 5% papaya)	L. casei subsp. rhamnosus	Inulin (1%)	Fermentation at 37 °C for 50 h Strain adapted in MRS broth supplemented with 10% red fruit beverage	Initial: 6.6 log CFU/mL At the end of fermentation: 6.7 log CFU/mL (without inulin) and 7 log CFU/mL (with inulin)	(Bernal-Castro, Díaz-Moreno, and Gutiérrez-Cortés 2019)
Commercial grape juice	L. rhamnosus	Short chain (SC) inulin or long chain (LC) inulin (4%)	Fermentation at 37 °C for 24, 48 and 72 h Storage at 4 °C for 30 days	Initial: 7 log CFU/mL At the end of fermentation: 7 log CFU/mL At the end of storage: 7 log CFU/mL (without inulin) and ND (SC and LC)	(White and Hekmat 2018)
Açaí (35%) juice with sucrose	L. casei	FOS	Fermentation at 28 °C for 22 h Storage at 4 °C for 42 days	Initial: 7 log CFU/mL At the end of fermentation: 9.7 log CFU/mL At the end of storage: 8.9 log CFU/mL	(Freitas et al. 2021)
Pomegranate juice	L. paracasei immobilized on delignified wheat bran	Delignified wheat bran	Fermentation at 30 °C for 24 h with adjusted pH Storage at 4 °C for 28 days	Initial: 8.5 log CFU/mL At the end of fermentation: 8.8 log CFU/mL for lower pH and 9.8 log CFU/mL for higher pH At the end of storage: 9.9 log CFU/mL for lower pH and 11.8 log CFU/mL for higher pH	(Mantzourani et al. 2020)
Cornelian cherry juice	L. paracasei immobilized on delignified wheat bran	Delignified wheat bran	Fermentation at 30 °C for 24 h with adjusted pH Storage at 4 °C for 28 days	Initial: 11 log CFU/mL At the end of storage: 8.6 log CFU/mL for free and 9.7 log CFU/mL for immobilized	(Mantzourani et al. 2019)
Berry juice	Saccharomyces cerevisiae boulardii microencapsulated with alginate, inulin, and xanthan gum	Inulin (1%)	Fermentation at 37 °C for 24 h Storage at 4 °C for 28 days	Initial: > 6 log CFU/mL At the end of fermentation: 7.5 log CFU/mL At the end of storage: 7 log CFU/mL	(Fratianni et al. 2014)

* ND: not detected

Table 3. Evidence of beneficial health effects provided by combinations of anthocyanin-rich matrixes and probiotics.

Matrix	Probiotic	Health effect	Reference
Commercial wine phenolic extract	L. plantarum and P. pentosaceus	Inhibition of the adhesion of E. coli to the intestinal cells	(González et al. 2017)
Blueberry pomace	L. casei	Increase of phenolic antioxidant, improvement of fecal microbiota community structure and production of SCFA	(Cheng et al. 2020)
Pomegranate juice with inulin	L. rhamnosus, Bacillus koagolans and Bacillus indicous	Improvement of insulin resistance, testosterone level, BMI, weight and waist circumference in PCOS (Polycystic Ovarian Syndrome) women	(Esmaeilinezhad et al. 2019)
Blueberry pomace liquid	L. rhamnosus and L. plantarum	Cholesterol clearance and anti-fatigue properties	(Yan at al., 2019)
Blueberry juice	Mix of Bifidobacterium, Lactobacillus bulgaricus and Streptococcus thermophilus	Reduce apoptosis of alcoholic fatty liver disease (AFLD)	(Zhu et al., 2016)
Pomegranate juice	L. plantarum	Inhibition of Bacillus  megaterium F6 and E. coli DSM 30083. Inhibition of immune-mediator with pro-inflammatory activity (IL-4, IL-6, IL-17a and TNFα). Stimulation of cytokines and growth factors with anti-inflammatory activity (IL-2 and G-CSF, respectively).	(Filannino et al. 2013)

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