1. Introduction
Sweet potatoes (Ipomoea potatoes) are among the most produced roots in Brazil [1], and their consumption is associated with the development of a low glycemic index. This effect is a consequence of the complex chemical structure of this product, which allows for the slower absorption of carbohydrates that avoid blood glucose peaks; thus, it is of interest to diabetic patients, as it helps to control blood glucose levels and reduces the need for insulin. Also, lower levels of this hormone can decrease the synthesis of cholesterol and triacylglycerols [2].
Starch is the main component in sweet potato roots and is the main source of carbohydrates for humans. Starch is essential in human nutrition, as it offers consumers energy and nutrition to support metabolic activities [3]. Depending on the rate and extent of starch digestion in vitro, it can be classified into three fractions: rapidly digestible starch (RDS), slowly digestible starch (SDS), and resistant starch (RS) [4]. RDS is quickly digested and absorbed in the human small intestine, causing a rapid rise in blood glucose. SDS is arranged as an intermediate starch fraction between the RDS and RS fractions. It is digested slowly throughout the small intestine and provides a sustained release of glucose with low initial glycemia and the slow and extended release of glucose. RS refers to the fraction of starch that cannot be digested in the small intestine but is fermented by bacteria in the large intestine [5]. Several studies have highlighted the importance of consuming slowly digested starch (SDS) in regulating blood sugar levels and the associated mechanisms of energy balance. The moderate glycemic response associated with SDS consumption indicates that it can offer various health benefits by lowering the risk of developing diseases linked to diets high in rapidly digested carbohydrates, which promote hyperglycemia [5,6].
An alternative to increase the fraction of SDS in starches is to modify its structure through annealing, which consists of a physical modification where the starch is incubated in an excess of water for a period of time at a temperature below the gelatinization temperature and higher than the glass transition temperature. It forms new and better-organized helices between the amylose–amylose, amylose–amylopectin, and amylopectin–amylopectin chains [7]. A variation of this modification is called in situ annealing or in vivo annealing, where the treatment takes place directly in the product using its own moisture. This can occur due to the soil temperature during plant development, during cereals’ maceration prior to starch extraction, or even during the storage of tubers and roots before starch extraction [8]. This can easily be achieved in roots or tubers with a moisture content between 60 and 75%. It would be challenging during cereals’ storage since their moisture levels vary between 10 and 12% [9]. The advantage of in situ annealing would be the agility and economy in the modification process, as this is carried out directly in the root before the starch extraction, which can stimulate the realization of this modification at an industrial level.
The benefits of ingesting SDS can be enhanced when associated with the consumption of probiotics. Studies have shown that the combinations of these components can protect against the formation of tumors in the colon, causing the formation of short-chain fatty acids that are beneficial for reducing LDL cholesterol and, consequently, reducing heart disease and increasing mineral absorption [6].
All this suggests that it is possible to improve the digestibility of sweet potato starch via in situ annealing and to use it in a dairy beverage fermented by a probiotic microorganism, bringing health benefits to consumers due to the SDS and probiotics it contains. Therefore, this study aimed to modify the starch of three sweet potato varieties through in situ annealing to obtain a higher SDS content and to evaluate its applications in producing a potentially probiotic dairy beverage.
2. Materials and Methods
2.1. Materials
Sweet potatoes of the Rosada Uruguaiana (RU), Rosada Canadense (RC), and Ligeirinha (L) varieties were obtained from a single producer located in Londrina/PR (latitude: −23.2927, longitude: −51.1732, 23°17′34″ South, 51°10′24″ West). Sweet potatoes were harvested in January 2019 and selected according to the uniformity of their size and the absence of holes and cracks. The samples were stored in a cold chamber at 4 °C for a maximum of 7 days until use. Whole whey powder was purchased from Confepar® (Londrina, Brazil) and stored at 4 °C. Skimmed milk powder from Nestle® Molico (São Paulo, Brazil), mixed fruit pulp with banana, apple, and papaya from Ricaeli (Londrina, Brazil), and honey were acquired in the local commerce of Londrina-PR. Freeze-dried commercial culture of probiotic lineage Lactobacillus casei 01 was acquired from Christian Hansen® (Valinhos, Brazil) and stored at −20 °C. The enzymes lipase (80612), pepsin (P7125), pancreatin (P3292), amyloglucosidase (A9913), α-amylase (A3176), and bile salts (B3883) were all purchased from Sigma-Aldrich (Steinheim, Germany). The kit for determining clinical glucose oxidase was acquired from Glucose Bioliquid (Pinhais, Brazil).
2.2. Modification of Starch by In Situ Annealing
Sweet potatoes were separated into 5 kg batches, washed, and covered individually with a triple layer of 10-micron PVC (polyvinyl chloride) film. The samples were placed in an oven with closed air circulation. Inside the oven were containers with water to avoid the dehydration of sweet potatoes. The modification was carried out in triplicate, simultaneously, using separate ovens, for 72 h at 56 °C. After the incubation period, sweet potatoes were immediately used for starch extraction.
2.3. Extraction of Sweet Potato Starch
The sweet potato starch was extracted using a wet milling methodology [10].
2.4. Scanning Electron Microscopy
Starches were evaluated by scanning electron microscopy (FEI Quanta 200, FEI Company, Eindhoven, The Netherlands) according to Veronese et al. [11].
2.5. Pasting Properties
The pasteurization process of dairy beverages was simulated to observe the paste properties of the starch under these conditions. A viscoamylographic curve was elaborated using a Brabender viscoamylograph with a 10.5% starch suspension (dry base) in 400 mL of distilled water. The suspension was heated from 30 to 65 °C at a rate of 1.5 °C/min, remaining at 65 °C for 30 min.
2.6. Thermal Properties
Thermal properties were determined as described by Felisberto et al. [12] using a differential scanning calorimeter (DSC-Pyris 1, Perkin Elmer, Norwalk, CT, USA) and Pyris 1 software version 8.0 (Perkin Elmer, Norwalk, CT, USA). Each sample (approximately 2 mg [d.b.] and 6 µL deionized water) was set in an aluminum pan and allowed to stand still for 4 h. Then, it was read at a temperature range of 30 °C to 120 °C, with a heating rate of 5 °C per minute.
2.7. X-ray Diffraction
A PANalitical diffractometer model X’Pert PRO MPD (Almelo, The Netherlands) emitting kα copper radiation (λ = 1.5418 angstrom) was used. Anode radiation was generated at 40 kV, 50 mA, and monochromatized using a current of 20 mA. Measurements were performed from 3 to 35° at 2θ at 1°/min. The relative crystallinity was calculated according to Nara and Komiya [13] using Origin 7.5 (Microcal Inc., Northampton, MA, USA).
2.8. Digestibility
The in vitro digestibility of starches was evaluated according to Englyst et al. [5], with the following modifications. After enzymatic hydrolysis, the content of each starch fraction was determined by the glucose content produced. It was used a kit for clinical glucose oxidase determination. The digestibility profile was obtained after maintaining the starches in a water bath at 65 °C for 30 min and cooling to 37 °C before adding the enzymes. The RDS, SDS, and RS contents were obtained using the following equations:
RDS (%) = [(G20 − FG)/TS] × 0.9 × 100
SDS (%) = [(G120 − G20)/TS] × 0.9 × 100
RS (%) = [(TS − G)/TS] × 0.9 × 100
where G20 and G120 represent the glucose content after 20 and 120 min, respectively. FG represents the free glucose content in the starch, and TS represents the total mass of the starch on a dry basis.
2.9. Preparation of Inoculum and Maintenance of Culture
The inoculum was prepared using 0.1 g of the culture of L. casei in 100 mL of skimmed milk powder reconstituted at 12% (w/v) and pasteurized at 65 °C for 30 min. The mixture was hom*ogenized and fractionated in Falcon tubes with 10 mL of the inoculum and 20% (v/v) sterile glycerol. The tubes were stored at −20 °C. Before its addition to the dairy beverage, the pre-inoculum was obtained through two activations in skimmed milk powder reconstituted at 12% (w/v) and incubated at 37 °C for 18 h.
2.10. Elaboration of Fermented Dairy Beverages
The fermented dairy beverages were prepared based on Cunha et al. [14], with modifications. They were obtained by mixing three preparations: a fermented base, nonfermented base, and sweet base. The fermented base corresponded to 30% of the composition of the dairy beverage. For its preparation, skimmed milk powder reconstituted at 12% (m/v) with distilled water and reconstituted whey at 15% (m/v) with distilled water was used. The mixture was pasteurized at 65 °C for 30 min in a water bath. After cooling to 42 °C, 1% of the inoculum was added. The mixture was fermented at 37 °C until pH 4.7, cooled to 4 °C, and slowly stirred with a glass spatula to break the clot. The unfermented base corresponded to 49% of the composition of the dairy beverage. Its preparation consisted of mixing the modified sweet potato starch with powdered milk, reconstituted 12% with distilled water. It was pasteurized at 65 °C for 30 min in a water bath and refrigerated at 4 °C until use. The sweet base corresponded to 21% of the dairy beverage’s composition, comprising fruit pulp and honey. The mixture of the ingredients was pasteurized in a water bath at 65 °C for 30 min and refrigerated at 4 °C until use.
2.11. Microbiological Analysis
The microbiological quality standards (thermotolerant coliforms and Salmonella spp.) were evaluated according to the methodology described by Da Silva et al. [15]. The method used for the determination of thermotolerant coliform was the most probable number (MPN). To determine Salmonella spp., a selective liquid media of tetrathionate broth and selenite–cystine broth was used, and isolation was carried out in a selective and differential medium using xylose deoxycholate agar (XLD) and Hektoen enteric agar.
2.12. Sensory Analysis
This study was approved by the Research Ethics Committee Involving Humans of the State University of Londrina under the n° 2968537. All subjects signed an informed consent form before the tests. The affective sensory method was performed using a 9-point hybrid hedonic scale [16], evaluating color, flavor, aroma, appearance, and global acceptance attributes. Purchase intent was assessed using a 5-point hedonic scale.
2.13. Stability during Storage
The formulations were stored at 4 °C for 1, 7, and 14 days and evaluated for physical-chemical parameters (total soluble solids, pH, titratable acidity, syneresis, color, water holding capacity, and viscosity) [17], microbiological quality standards (thermotolerant coliforms, and Salmonella), and the determination of viable L. casei cells [18].
2.14. In Vitro Simulation of L. casei Survival in Gastrointestinal Conditions
The simulation was performed at 0 and 30 days of cold storage [19]. The analysis was performed in triplicate.
2.15. In Vitro Digestibility of Starch Contained in Fermented Dairy Beverages
The in vitro digestibility of starch was evaluated according to Englyst et al. [5], with the following modifications: 2 g of the beverage was added to the buffer and heated to 37 °C before adding the enzymes.
2.16. Statistical Analysis
The analyses were performed in triplicate, and the results were evaluated in Statistica 8.0 (StatSoft® Inc., Tulsa, OK, USA, 2008) using analysis of variance (ANOVA). The means were compared using the Tukey test and Student t-test at 5% significance. Pearson’s correlation (r) was used to interpret the correlation between the parameters for the storage analyses [20].
3. Results and Discussion
3.1. Scanning Electron Microscopy
The granules of native sweet potato starches of the three studied varieties were rounded, polygonal, or convex ends (Figure 1). The granules’ surfaces were smooth, without evidence of cracks or fissures. The starch granule sizes were heterogeneous. All starches showed granules of varying sizes with diameters of approximately 5 to 40 μm. Zhang et al. [21] identified diameters for native sweet potato starches between 5 and 25 µm, with varied shapes, mostly elliptical, spherical, and polygonal, with smooth and shiny surfaces. The granule morphology after treatment with in situ annealing was no different from that of native starches.
These results show that in situ annealing under the studied conditions did not modify the granular morphology of starches. This is quite interesting when studying the digestibility of starches because if fissures or cracks occur on the surface, the digestion speed of this starch could be increased, as these openings would allow for the digestive enzymes to access the granules from inside.
3.2. Evaluation of Viscosity in the Simulated Pasteurization Process
Figure 2 shows the data for the viscosity development of native and modified starches of the RC variety during batch-simulated milk pasteurization conditions; the starches of the other varieties showed the same behavior.
Native sweet potato starch, after reaching 65 °C, reached the maximum viscosity response at 230 BU. For the modified starch, there was no viscosity response during the entire heating profile. Even though the starch suspension was maintained for an extended period at 65 °C, there was no significant swelling of the granules. It was important to ensure that there is no increase in viscosity during pasteurization when using these starches as ingredients to develop dairy beverages, as this could lead to lumps. Also, a visual evaluation of the resulting paste after analysis showed no precipitation of the starch when keeping the suspension immobile for 12 h. Therefore, it is not possible to affirm that gelatinization of the starch granules did not occur. However, it is possible to suggest that only partial gelatinization had occurred, which was not enough to produce a viscosity peak.
These results are promising in terms of texture and starch digestibility. This starch can be used in pasteurized dairy beverages without the precipitation of starch granules. Since processing conditions can influence the digestibility of starches [5], it is possible to intuit that this causes few changes to the content of fractions of SDS and RS since there was no viscosity response. These starch fractions would be more beneficial to health when used in dairy beverages that undergo pasteurization.
3.3. Thermal Properties
The initial gelatinization temperatures (T0) ranged from 58 °C to 69 °C (Table 1). Such differences are probably due to the genetic characteristics of each variety, since they were grown under the same climatic conditions. These differences in the T0 of sweet potato starch were discussed in the literature. Jo et al. [4] found a T0 of 61.7 °C for native starch of the Daeyumi variety in Korea. Huang et al. [22] found 59.28 °C for an unknown sweet potato variety supplied by a Chinese industry. Zhang et al. [21] obtained a T0 of 71.18 °C for native sweet potato starch of a Chinese variety, and Rocha et al. [23] found a T0 of 67.49 °C for an unidentified Brazilian variety. In this study, the annealing temperature was set at 56 °C, as this was 3 °C below the lowest T0 reported in the literature, to avoid the risk of starch gelatinization during in situ annealing.
There was a significant variation in the gelatinization temperature range (ΔT), from 8 to 16 °C, for native starches. A smaller ΔT, such as that of starch from the RU variety, indicates a less heterogeneous distribution of starch crystals [24]. There was no difference in enthalpy variations (ΔH) among the three sweet potato starches that were studied.
The starches showed an increase in T0 after in situ annealing. BeMiller [7] mentions that the alterations most associated with annealing, regardless of botanical origin, are the increase in T0 and peak temperature (Tp), together with the reduction in ΔT, behaviors observed in this study. The T0 is a result of the melting temperature of the crystal with weaker structures. Thus, the increase in T0 after modification by annealing suggests that the bonds between the amylose and amylopectin chains have become more compact, making them more resistant to fusion.
A more pronounced ordering of the starches of the varieties L and RC was noticed. A more significant difference in ΔT was observed before and after annealing. The decrease in ΔT after annealing suggests that there was an increase in the molecular organization within the granules of sweet potato starches [25]. This may have been due to the lower T0 of these native starches. Therefore, the starches of these varieties would have better conditions, allowing for a more expressive ordering of the amylose and amylopectin chains. For ΔH, no significant change was observed after in situ annealing. The enthalpy change is related to the loss of the amylopectin double-helices’ order during the gelatinization process [23]. The non-significative changes in ΔH after in situ annealing may imply that, even with a better organization between amylose and amylopectin chains, which increases the onset temperatures, no better package of amylopectin double helices occurred, which would require more energy during gelatinization.
3.4. X-ray Diffraction and Crystallinity
The peak profile X-ray diffraction observed for sweet potato native starches showed simple peaks at 5 and 18° at 2θ, characteristic peaks of the B-type polymorphism, but also showed simple peaks at 15 and 23° at 2θ, which are characteristic of the A-type polymorphism; thus, all three potato starches had the C-type pattern. This result agrees with the observations of Tortoe et al. [26], who studied the flour of twelve varieties of sweet potatoes.
The crystallinity index of native starches was 35 to 38% (Table 1). The amylopectin chains are mainly responsible for the crystallinity of the starch granules because they have a highly branched structure. The result is double helices that are strongly packaged, forming crystalline and semicrystalline lamellae [23].
The C-type pattern polymorphism remained after in situ annealing for the three sweet potato varieties. However, there was a change in the crystallinity index of the starches; that of RU and L varieties of sweet potato increased, while that of starch RC sweet potato decreased (Table 1).
The increase in the crystallinity index may have occurred due to the plasticizing effect of water [27], where, during annealing, there is an increase in the mobility of the amylose chains at the amorphous regions. This causes an increase in the flow of water into the granules and reversible granular swelling. With the accelerated movement of the molecular chains, there is an increase in pressure in the crystalline regions, and liquidity favors the occurrence of vibrational movements in the crystalline regions, resulting in increased crystal perfection and a crystalline arrangement into the starch granule.
The starches of RU and L varieties had the highest crystallinity indexes, reaching 43.74% and 42.33%, respectively, after in situ annealing, as well as the highest T0 after annealing: 73.12 °C and 71.76 °C. Since no significant changes in ΔH after in situ annealing were observed (Table 1), it is possible to affirm that there was no better packaging of the double helices of amylopectins. However, the higher crystallinity index and the higher T0 indicate a stronger association between amylose and amylopectin chains.
3.5. In Vitro Digestibility of Native Sweet Potato-Modified Starches
Figure 3 shows that, among the native starches, there was a significant difference in the contents of each starch fraction in terms of their digestibility profile. The starch of the RU variety differed from the starches of the other varieties because it had a high RS content (47%). The starch of the RC variety stood out from the others due to its high SDS content (55%). The starch of the L variety had a high RDS content (58%). These results indicate that there are, in fact, significant differences in the structural organization of the starches of different varieties of sweet potatoes. Amaro et al. [28] reported that there are no specific values that can define the starch fractions available in sweet potatoes. The ratio of these fractions is determined by different factors, which vary according to the varieties, the place of cultivation, and the production conditions.
The results observed for these three sweet potato varieties indicate that not all sweet potatoes can be considered a healthy food with a low glycemic load. This is different from what is often proposed in popular culture, in which it is often claimed that sweet potatoes can be consumed without worry due to the low glycemic response after eating. This study proves that sweet potato starch digestibility will depend on the variety and edaphoclimatic conditions of plant growth.
After the in situ annealing of sweet potato, the starch contents of each fraction in the digestibility profile changed. Starches showed a reduction in the RDS fraction, except starch of the RU variety. This demonstrates that treatment via in situ annealing can effectively decrease the content of the RDS fraction.
The starch of the RU variety showed a significant increase in the SDS content after in situ annealing; however, it also showed a reduction in the RS content. This may indicate that the starch of this variety underwent a structural reorganization of the amylose and amylopectin chains so that, even though an increase in the crystallinity index and a decrease in the ΔT can be observed (Table 1), this rearrangement of the chains may have allowed for an increase in the exposure of the amorphous regions of the granules. This fact favors greater access to digestive enzymes; therefore, part of the RS fraction started to be digested slowly, thus increasing the content of the SDS fraction. On the other hand, for starch of the RC variety, there was a reduction in the content of the SDS fraction and an increase in the RS content, and the sum of the two fractions increased from 75 to 79%. For this starch, structural reorganization, which improved the packaging of the amylose and amylopectin chains, resulted in the digestive enzymes struggling to act on the starch.
The sweet potato starch of the L variety showed the most exciting changes in the digestibility profile. In addition to the reduction in the RDS content, there was an increase of 110% in the SDS content and 72% in the RS content. Thus, the sum of the contents of the SDS and RS fractions ranged from 41% to 81% after annealing. The native starch of this variety was the one with the lowest T0 (Table 2); thus, it may have obtained the more significant effects of in situ annealing because annealing was carried out at the sub-gelatinization temperature [29]. Therefore, the most significant increase in the crystallinity index and the most remarkable difference in the ΔT were observed before and after annealing. Thus, the use of this starch in food products is quite promising; in addition to providing extended energy through the slow release of glucose into the bloodstream, it can also result in food with a high fiber content, as the RS can be considered a fiber.
Furthermore, the low digestibility of both SDS and RS increases the viscosity of the intestinal contents, causing a decrease in the rate of gastric emptying, better known as dumping syndrome [30]. A slow-digesting carbohydrate that results in a low glycemic index effectively improves the changes in blood glucose and insulin secretion, increasing satiety [31].
Persons with glucose metabolism disorders must avoid hyperglycemia, and foods with SDS can significantly contribute to this control. One of the benefits of SDS is that it can reach the most distal parts of the intestine. Nutrients in the ileum can result in increased plasma concentrations of Glucagon Like Protein-1 (GLP-1), which is one of the mechanisms proposed to explain the remission of type-2 diabetes after bariatric surgery. According to Zhang and Hamaker [32], SDS offers the advantage of achieving a lower blood glucose with less variation, balanced over a more extended period.
One potential way to control body weight is by activating the hypothalamus–gut axis with functional food components like those containing SDS. These components can activate the expression of GLP-1 and peptide YY (PYY), which are hormones that affect appetite and food intake responses through activities in different regions of the central nervous system, especially the hypothalamus, which plays an active role in controlling food intake [33].
Due to the promising results of the high content of SDS and RS, for the duration of this study, the starch of the L variety, annealed in situ, was used for the preparation of the dairy beverage; from this point on, this will be referred to as modified starch.
3.6. Elaboration of Fermented Dairy Beverages
The formulation of the fermented dairy beverage was based on the sensory aspects of the beverage, such as taste and viscosity. The selected pulp gave the beverage a pleasant taste and color. The proportions of starch that were used were 7% and 10.5%, considering the amount of reconstituted milk necessary to solubilize the modified starch. The addition of honey gave sweetness and a characteristic odor. The formulations (fermented base, nonfermented base, and sweet base) of the two preparations, called the FA and FB formulations, were offered in the sensory analysis. Formulation FC had no modified starch and was used for comparison in a physicochemical analysis (Table 2).
Table 2. Formulations of fermented dairy beverages.
Table 2. Formulations of fermented dairy beverages.
| Ingredients | FA | FB | FC | |
|---|---|---|---|---|
| Fermented base | Pasteurized skimmed milk powder (g) | 2.16 | 2.16 | 2.16 |
| Whey (g) | 1.80 | 1.80 | 1.80 | |
| H2O (mL) | 26.04 | 26.04 | 26.04 | |
| Nonfermented base | Modified starch (g) | 7.00 | 10.5 | - |
| Pasteurized skimmed milk powder (g) | 5.04 | 4.62 | 5.88 | |
| H2O (mL) | 36.96 | 33.88 | 43.12 | |
| Sweet base | Honey (g) | 7.00 | 7.00 | 7.00 |
| Fruit pulp (g) | 14.00 | 14.00 | 14.00 | |
| Total | 100 | 100 | 100 |
Abbreviations: fermented dairy beverages with 7% modified sweet potato starch (FA), fermented dairy beverages with 10.5% modified sweet potato starch (FB), and fermented dairy beverages without the addition of modified sweet potato starch (FC).
3.7. Microbiological Analysis
A microbiological analysis was conducted to guarantee the safety of the subjects who participated in the sensory analysis. The results were within the legal standards established by Resolution No. 12/2001 [34].
3.8. Sensory Analysis
There was no difference (Table 3) between the two formulations for the six attributes evaluated by the subjects of the analysis. The appearance and color parameters obtained average evaluation values, indicating that the subjects “regularly liked” these attributes for both formulations, which are the attributes of the product with the best acceptance. For the aroma, texture, and flavor attributes, the averages obtained were close to 6, which indicates, according to the hedonic scale, that the subjects “slightly liked” these attributes in both fermented dairy beverages.
López et al. [35], evaluating a fermented dairy beverage with the addition of 6% sweet potato flour and 50% whey, obtained an average grade lower than that found in this study. An average of 5.72 was obtained for the appearance attribute, 5.38 for color, and 5.38 for texture. The upper marks attributed to appearance and color in this study may be related to the yellowish coloration that the mix of fruit pulp and honey gave to the fermented dairy beverage, in line with the color of the whey. The texture evaluation that was obtained may be because starch was used instead of sweet potato flour; potato flour could have led to granularity in the product of López et al. [35], while the starch resulted in a smooth texture.
The global acceptance of beverages obtained average scores close to 6, corresponding on the hedonic scale to “I liked it slightly”. The intention to purchase beverages, on the other hand, that was evaluated on a 5-point scale obtained an average close to 3, corresponding to “maybe I would buy/maybe I would not buy”.
The attributes of taste, global acceptance, and purchase intention can be affected by the age and gender of the subjects. Younger consumers prefer sweeter-tasting food, and as age increases, the preference changes to salty foods [36]. In addition, female people tend to prefer sweet foods compared to male consumers, who prefer salty foods [37]. These characteristics of the subjects reinforce the behavior observed in this study, where 61% of the subjects were aged between 18 and 24 years old, 23% between 25 and 29 years old, 9% between 30 and 36 years old, and 7% between 37 and 50 years old; 60% were female and 40% were male. Therefore, it can be concluded that fermented dairy beverages have well-evaluated attributes and satisfactory global acceptance.
The results of the acceptance test indicated that there were no differences between formulations FA and FB. It was decided to use fermented dairy beverage FB to comply with the objective of adding the largest possible amount of modified sweet potato starch with a high SDS content. It was hoped that the higher concentration of SDS in the fermented dairy beverage would increase its health benefits. Thus, this formulation was selected to continue the studies.
3.9. Evaluation of Stability of Physical–Chemical and Microbiological Properties during Storage
There was a difference in the total soluble solids’ content between the FB and FC drinks, regardless of the storage period (Table 4). This difference was expected because the addition of starch led to an increase in the content of soluble solids in the fermented dairy beverage FB. However, there was no change in the total soluble solids content during the storage period for fermented dairy beverage FB, while the content decreased for fermented dairy beverage FC.
Fermented dairy beverages underwent a pH variation, with pH decreasing during the storage period [38]. The pH interferes with the visual aspect of the product, and therefore requires strict control. Thus, possible phase separations do not occur due to the excessive acidification of the product. For titratable acidity, it was possible to observe an increase in the lactic acid content over the storage time of both fermented dairy beverages. However, there were differences in values between formulations FB and FC and between storage days. Marin et al. [39] obtained values close to those found in this study for titratable acidity in dairy beverages with and without added honey. The honey provides more outstanding acid production because it has a high content of fermentable carbohydrates.
Fermented dairy beverage FC presented with higher values of syneresis because, when adding the modified sweet potato starch to the FB beverage, a gel was formed that absorbs and retains water, increasing the storage stability and not allowing for the occurrence of phase separation.
The water retention capacity was more remarkable for the fermented dairy beverage FB than for fermented dairy beverage FC throughout the storage period. At the macroscopic level, the water retention capacity refers to the ability of the matrix of the starch added to fermented dairy beverage FB to physically retain high amounts of water, causing a decrease or inhibition in exudation when subjected to external shear forces. When a starch is placed in environments with higher temperatures, its molecules vibrate, causing intermolecular bonds to break and allowing free bonding sites to participate in hydrogen bonds with water molecules [40].
Fermented dairy beverage FB showed a stable count for Lactobacillus casei in the first 7 days of storage and a slight decrease on the 14th day. For fermented dairy beverage FC, the count was stable throughout the entire storage period.
There was a positive correlation between storage time and titratable acidity, pH, viscosity, and L. casei count for both formulations of fermented dairy beverage (Figure 4). There was also a positive correlation between storage time and total soluble solids content, water retention capacity, and syneresis, although only for fermented dairy beverage FC. In this way, the presence of starch in fermented dairy beverage FB made some of the physicochemical properties of the product more stable in terms of storage time.
Better stability in terms of the water retention capacity and syneresis were observed in fermented dairy beverage FB than in FC because the starch in fermented dairy beverage FB promotes the formation of hydrogen bonds between water and starch chains, avoiding phase separation. The presence of starch may have masked changes in the content of total soluble solids in fermented dairy beverage FB. The decrease in the content of soluble solids in fermented dairy beverage FC may be related to the viability of the microorganism, as shown by Yu et al. [41], where the authors found that when preparing a dairy beverage with the addition of L. casei, the sucrose and lactose content present in the beverage decreased as the fermentation time increased, demonstrating that the microorganism remained viable during storage, and directly reflecting the decrease in the content of soluble solids and pH, and the increase in the titratable acidity.
There was a very significant correlation between storage time, titratable acidity, and pH, indicating that the increase in the acidification of the medium during storage can be attributed to the continued viability of L. casei. This pH reduction is a natural process in products where lactic acid bacteria are added through the continuous production of lactic acid and other organic acids [42]. The fermented dairy beverages could use hexoses from pulp and honey, which are the primary substrates used for the growth of L. casei fermentative bacteria. L. casei produces lactic acid during cold storage, a phenomenon known as post-acidification, due to the continued activity of Lactobacillus [17].
Thus, lactic acid bacteria preferentially metabolize lactose and other simple sugars that are present in dairy beverages. The sweet potato starch added to the beverage is not an energetic substrate for this class of microorganisms due to the complexity of its chemical structure [38].
3.10. In Vitro Simulation of L. casei Survival under Gastrointestinal Conditions
There was a reduction (p ≤ 0.05) in the count of L. casei for fermented dairy beverage FB during the different stages of simulation of digestion between the 1st and 30th day of storage (Table 5), in which for up to 14 days of storage, the count of L. casei was greater than 9 log CFU/mL for fermented dairy beverage FB; however, after 30 days of storage, the initial count decreased to approximately 8 log CFU/mL. Despite this reduction, the final counts were high, approximately 6 log CFU/mL, regardless of the period of storage of the fermented dairy beverage. These results demonstrated the survival of L. casei and its resistance to gastrointestinal conditions. Even though the initial count of L. casei was lower after 30 days of storage, its survival rate was higher, indicating that the population of the microorganisms remaining in the fermented dairy beverage was the most resistant to the adverse conditions of the digestion process. Thus, fermented dairy beverage FB can be considered an excellent carrier matrix for the L. casei probiotic culture.
These results agree with those of Lamadrid, Bernal, and Morales [43], who found that in lactic acid bacteria, a high percentage of bacteria, ranging from 75% to 99%, adhered to the starch granules of different potato varieties. This association could be a mechanism of protection of these bacteria against the conditions of the gastrointestinal tract.
3.11. In Vitro Digestibility of Modified Sweet Potato Starch
The 10.5% modified sweet potato starch added to fermented dairy beverage FB was analyzed for its digestibility during the storage period. There was an alteration in the content of each fraction of starch in relation to the pure modified starch of sweet potato used in the preparation of the beverage. The modified sweet potato starch had 18.8% RDS, 53.2% SDS, and 27.9% RS (Figure 3). After 1 day of storage, an increase in the RDS content was observed, which implied a decrease in the SDS content and a decrease in the RS content. After 14 days of storage, there was a more significant decrease in the SDS content and an increase in the RDS content; the RS content remained stable (Figure 5).
An increase or maintenance of the SDS content was expected since the presence of other components of the food matrix, such as proteins and lipids, could act protectively, interfering in starch digestion. However, it is possible that the fermentative process continued and resulted in the formation of lactic acid or other organic acids; these weak acids were able to change the chemical structure of starch chains and exposed these chains to the action of digestive enzymes. According to Liljeberg, Åkerberg, and Björck [44], foods that contain some organic acid can promote partial hydrolysis of amylopectin. This hydrolysis may, in fact, occur in a small proportion, enough to cause a decrease in the viscosity of the product. Thus, the amylopectin chains become more susceptible to the action of digestive enzymes.
Putri et al. [45] studied the effect of fermentation via lactic acid bacteria for 48 h on the structural and physicochemical properties of cassava starch. The fermentation process damaged the microstructure of the starch due to the formation of lactic acid, which caused a decrease in the crystallinity provoked by the process of hydrolysis of the amorphous areas of the granular structure. Thus, even when low concentrations of lactic acid were present in fermented dairy beverage FB, with the storage time and due to the partial gelatinization of the modified sweet potato starch, there was a slow process of hydrolysis of the starch chains, which facilitated the action of digestive enzymes, resulting in a 22% decrease in the SDS content in relation to the pure modified sweet potato starch.
After 14 days of storage, the SDS content was 41%. Considering that the portion size of the fermented dairy beverage indicated by Normative Instruction n° 75/2020 [46] is 200 mL, the individual who consumes fermented dairy beverage FB will be ingesting 8.6 g of SDS. This amount of SDS can benefit the health of the consumer. Hasek et al. [33] submitted a group of obese rats to a diet containing high levels of fat and 6.6% SDS and another group of obese rats to a diet containing high levels of fat and 28.3% RDS; the group that ingested SDS reduced the daily amount of food that was ingested due to an increase in satiety. The authors found that SDS digestion occurred in the ileum, which suppressed the expression of appetite-stimulating neuropeptide genes by increasing the plasma concentration of GLP-1. Thus, the consumption of the fermented dairy beverage FB, containing SDS, may have practical preventive or treatment implications for type-2 diabetes and obesity problems.
4. Conclusions
Annealing in situ can be considered a viable alternative to starch modification techniques to increase the content of the slowly digestible starch fraction. This physical modification causes marked changes in the viscosity profile due to an increase in the associative forces of the amylose and amylopectin chains and the better molecular organization of the starch granules. These changes in physicochemical and structural properties result in changes in the digestibility of starches. These physicochemical and structural changes are expected in starches treated by regular annealing. Since this modification was performed in situ, food industries could easily apply it in their production plant. This process only requires the storage of the roots at a certain temperature for some time before starch extraction.
The use of sweet potato starch annealed in situ in a fermented dairy beverage demonstrated satisfactory results, observed through the analyses carried out during storage, without compromising the viability of the probiotic microorganism L. casei. The amount of SDS remaining in the fermented dairy beverage indicates the potential of the product to provide extended energy, the potential for increased satiety, and the possibility of decreasing the risk of developing type-2 diabetes. Therefore, the development of a fermented dairy beverage with L. casei supplemented with modified sweet potato starch with a high SDS content proved to be feasible in technological and sensorial terms and could be an option for a functional dairy beverage that can provide beneficial effects on consumers’ health.
Author Contributions
L.S.d.O.: conceptualization, methodology, research, formal analysis, writing—original draft, writing—review, and editing. A.D.C.C.: research, formal analysis. M.d.B.: formal analysis, writing—original draft, visualization. P.H.F.C.: writing—review and editing. A.A.B.T.: conceptualization, methodology, research, formal analysis, writing—draft. T.d.S.R.: conceptualization, methodology, investigation, writing—original draft, writing—review and editing, supervision, resources, financing acquisition. All authors have read and agreed to the published version of the manuscript.
Funding
The author, Luma Sarai de Oliveira, was supported by the National Council for Research and Technological Development (CNPq) (grant number 132041/2018-9).
Institutional Review Board Statement
The study was approved at 18 October 2018 by the Research Ethics Committee Involving Humans of the State Unniversity of Londrina under the nº 2968537.
Informed Consent Statement
Informed consent was obtained from all subjects involved in the study.
Data Availability Statement
The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.
Acknowledgments
The authors thank the Laboratory of Scanning and Microanalysis Electron Microscopy—LMEM, the Laboratory of Thin Films and Materials—FILMAT for the X-ray analysis, and the Sao Paulo State University (UNESP) for the DSC analysis.
Conflicts of Interest
The authors declare no conflicts of interest.
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Figure 1. Scanning electron micrographs of native and modified starches of different varieties of sweet potato (2000× magnification). (A) Rosada Uruguaiana native; (B) Rosada Uruguaiana after annealing; (C) Rosada Canadense native; (D) Rosada Canadense after annealing; (E) Ligeirinha native; (F) Ligerinha after annealing.
Figure 1. Scanning electron micrographs of native and modified starches of different varieties of sweet potato (2000× magnification). (A) Rosada Uruguaiana native; (B) Rosada Uruguaiana after annealing; (C) Rosada Canadense native; (D) Rosada Canadense after annealing; (E) Ligeirinha native; (F) Ligerinha after annealing.
Figure 2. Viscoamylograph profile simulating the batch milk pasteurization process (65 °C, 30 min) for native and modified Rosada Canadense sweet potato starch.
Figure 2. Viscoamylograph profile simulating the batch milk pasteurization process (65 °C, 30 min) for native and modified Rosada Canadense sweet potato starch.
Figure 3. In vitro digestibility profile for the starches of sweet potato from Rosada Uruguaiana, Rosada Canadense, and Ligeirinha varieties. Abbreviations: rapidly digestible starch (RDS); slowly digestible starch (SDS); resistant starch (RS). a–f Values followed by the same letter for each fraction of starch do not differ significantly by the Tukey test (p < 0.05).
Figure 3. In vitro digestibility profile for the starches of sweet potato from Rosada Uruguaiana, Rosada Canadense, and Ligeirinha varieties. Abbreviations: rapidly digestible starch (RDS); slowly digestible starch (SDS); resistant starch (RS). a–f Values followed by the same letter for each fraction of starch do not differ significantly by the Tukey test (p < 0.05).
Figure 4. Pearson’s coefficient for physicochemical properties and L. casei count for fermented dairy beverages (a) FB and (b) FC. Abbreviations: (FB) fermented dairy beverage with the addition of 10.5% modified sweet potato starch; (FC) control fermented dairy beverage; (TA) titratable acidity, (Day) days; (SS) total soluble solids; (pH) pH; (Visc) viscosity; (L. casei) Lactobacillus casei; (CRA) water holding capacity; (SIN) syneresis.
Figure 4. Pearson’s coefficient for physicochemical properties and L. casei count for fermented dairy beverages (a) FB and (b) FC. Abbreviations: (FB) fermented dairy beverage with the addition of 10.5% modified sweet potato starch; (FC) control fermented dairy beverage; (TA) titratable acidity, (Day) days; (SS) total soluble solids; (pH) pH; (Visc) viscosity; (L. casei) Lactobacillus casei; (CRA) water holding capacity; (SIN) syneresis.
Figure 5. In vitro digestibility profile for the modified sweet potato starch added to the fermented dairy beverage. Abbreviations: (RDS) rapidly digestible starch; (SDS) slowly digestible starch; (RS) resistant starch. a,b Values followed by the same letter for each starch fraction do not differ significantly according to Student’s t-test (p < 0.05).
Figure 5. In vitro digestibility profile for the modified sweet potato starch added to the fermented dairy beverage. Abbreviations: (RDS) rapidly digestible starch; (SDS) slowly digestible starch; (RS) resistant starch. a,b Values followed by the same letter for each starch fraction do not differ significantly according to Student’s t-test (p < 0.05).
Table 1. Thermal properties and crystallinity index of native and modified sweet potato starches.
Table 1. Thermal properties and crystallinity index of native and modified sweet potato starches.
| Sample | T0 (°C) | Tp (°C) | Tf (°C) | ΔT (°C) | ΔH (J/g) | CI (%) |
|---|---|---|---|---|---|---|
| RU-Native | 69.43 ± 0.44 c | 73.92 ± 0.00 b | 78.05 ± 0.02 b | 8.62 ± 0.42 c | 14.96 ± 0.18 ns | 38.91 ± 0.93 a |
| RU-annealed | 73.12 ± 0.10 a | 76.23 ± 0.00 a | 79.63 ± 0.14 a | 6.51 ± 0.04 d | 15.90 ± 0.01 ns | 43.74 ± 0.22 b |
| RC-Native | 64.50 ± 0.64 e | 69.94 ± 0.45 c | 75.76 ± 0.55 c | 11.26 ± 0.08 b | 14.26 ± 0.04 ns | 38.87 ± 0.48 a |
| RC-annealed | 68.10 ± 0.12 d | 71.33 ± 0.10 c | 74.49 ± 0.04 d | 6.43 ± 0.08 d | 13.82 ± 1.97 ns | 36.02 ± 0.33 c |
| L-Native | 58.00 ± 0.00 f | 65.36 ± 0.95 d | 74.53 ± 0.08 d | 16.53 ± 0.20 a | 13.92 ± 0.75 ns | 35.00 ± 1.00 c |
| L-annealed | 71.76 ± 0.16 b | 74.56 ± 0.23 ab | 78.2 b ± 0.33 b | 6.53 d ± 0.17 d | 15.75 ± 1.69 ns | 42.33 ± 1.53 b |
a–f Equal lowercase letters in the same column do not differ significantly according to the Tukey test (p < 0.05). Abbreviations: initial temperature (T0); peak temperature (Tp); final temperature (Tf); temperature variation (ΔT = Tf − T0); enthalpy variation (ΔH); not significant (ns); CI = crystallinity index.
Table 3. Evaluation of acceptance and purchase intention for fermented dairy beverages.
Table 3. Evaluation of acceptance and purchase intention for fermented dairy beverages.
| Attribute | FA * | FB * |
|---|---|---|
| Appearance 1 | 7.08 ± 1.51 | 7.10 ± 1.50 |
| Color 1 | 7.42 ± 1.41 | 7.21 ± 1.50 |
| Aroma 1 | 6.04 ± 1.86 | 6.32 ± 1.65 |
| Flavor 1 | 5.75 ± 2.17 | 5.98 ± 2.03 |
| Texture 1 | 6.57 ± 1.99 | 6.08 ± 2.15 |
| Global acceptance 1 | 6.11 ± 1.71 | 6.19 ± 1.77 |
| Purchase intention 2 | 3.22 ± 1.78 | 3.18 ± 0.75 |
* There were no significant differences between the attributes of each formulation according to the Student’s t-test (p < 0.05). Equal lowercase numbers in the same row do not differ significantly according to the Tukey test (p < 0.05). Abbreviations: (FA) fermented dairy beverage with 7% modified sweet potato starch; (FB) fermented dairy beverage with 10.5% modified sweet potato starch.
Table 4. Physicochemical properties and L. casei count for fermented dairy beverages during storage.
Table 4. Physicochemical properties and L. casei count for fermented dairy beverages during storage.
| Formulation | Day 1 | Day 7 | Day 14 |
|---|---|---|---|
| Total soluble solids (° Brix) | |||
| FB | 20.53 ± 0.65 a | 20.76 ± 0.40 a | 20.66 ± 0.25 a |
| FC | 17.64 ± 0.26 b | 15.24 ± 0.26 c | 8.06 ± 0.06 d |
| pH | |||
| FB | 5.28 ± 0.04 b | 4.82 ± 0.12 c | 4.39 ± 0.02 d |
| FC | 5.66 ± 0.01 a | 4.77 ± 0.02 c | 4.48 ± 0.02 d |
| Titratable acidity (% lactic acid) | |||
| FB | 0.48 ± 0.01 e | 0.63 ± 0.02 d | 0.90 ± 0.02 a |
| FC | 0.43 ± 0.01 f | 0.69 ± 0.02 c | 0.83 ± 0.01 b |
| Water holding capacity (%) | |||
| FB | 47.30 ± 2.48 a | 31.63 ± 2.56 b | 47.76 ± 1.37 a |
| FC | 12.43 ± 1.23 e | 20.44 ± 0.75 c | 18.83 ± 0.40 d |
| Syneresis (%) | |||
| FB | 42.32 ± 0.21 e | 34.81 ± 0.59 f | 44.68 ± 0.36 d |
| FC | 89.88 ± 0.96 a | 72.25 ± 1.32 b | 71.99 ± 0.34 c |
| Lactobacillus casei count (Log CFU/mL) | |||
| FB | 9.925 ± 0.140 a | 9.817 ± 0.057 a | 9.336 ± 0.199 a |
| FC | 9.287 ± 0.032 b | 9.489 ± 0.124 b | 9.505 ± 0.129 b |
Abbreviations: (FB) fermented dairy beverage with the addition of 10.5% modified sweet potato starch, (FC) control fermented dairy beverage. a–f Values followed by the same letter for each parameter did not differ significantly according to the Tukey test (p ≤ 0.05).
Table 5. L. casei count and survival rate after simulation of gastrointestinal digestion of the FB drink.
Table 5. L. casei count and survival rate after simulation of gastrointestinal digestion of the FB drink.
| Microorganism | Time (Day) | Initial (CFU/mL) | Gastric Phase (CFU/mL) | Enteric Phase I (CFU/mL) | Enteric Phase II (CFU/mL) | Survival Rate (%) (CFU/mL) |
|---|---|---|---|---|---|---|
| L. casei | 1 | 8.96 ± 0.01 a | 6.84 ± 0.01 c | 6.73 ± 0.03 d | 6.34 ± 0.03 f | 70.76 ± 0.18 b |
| 30 | 7.92 ± 0.01 b | 6.66 ± 0.02 e | 6.15 ± 0.03 g | 5.94 ± 0.00 h | 75.00 ± 0.17 a |
a–h Lowercase letters in the same column do not differ significantly according to the Tukey test (p < 0.05). Uppercase letters in the same column do not differ significantly according to Student’s t-test (p < 0.05). CFU/mL: log colony-forming unit per mL. L. casei: Lactobacillus casei.
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