pubs.acs.org/acsfoodscitech Article In Vitro Digestibility and Physicochemical Properties of Potato (Solanum tuberosum) Fermented by Traditional and Alternative Processes under Water Currents Karla Escandón, Juan Carlos Gonzalez-Rojas, María José Carrera Flores, Daniela Guardado Felix, and Marco A. Lazo-Vélez* Downloaded via CSIC on May 10, 2023 at 12:54:17 (UTC). See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles. Cite This: ACS Food Sci. Technol. 2023, 3, 465−469 ACCESS Read Online Metrics & More Article Recommendations ABSTRACT: In vitro digestibility and functional and physicochemical properties of two fermented potato meals under hydric stress procedures were determined by (a) traditional potato meal (TPM) and (b) alternative potato meal (APM) used for potato conservation in the Andean Region. Starches granules were oval-shaped with sizes ranging from 15 to 70 μm in length and from 20 to 100 μm in diameter. The amylose content of APM (28.9%) was significantly higher compared to that of TPM (25.7%). The peak gelatinization temperatures were 65.8 °C for TPM and 68 °C for APM. When raw starches from TPM and APM were gelatinized, rapidly digestible starch increased 3.8- and 3.2-fold, while resistant starch decreased by 2.7- and 2.2-fold, respectively. However, while slowly digestible starch showed a similar percentage at 120 min, it decreased to 8.9-fold in TPM and was not detected in APM at 240 min. The TPM and APM parameters can be used to evaluate and implement these meals in food industrialization processes. KEYWORDS: fermentation, potato meals, resistant starch, starch structure, starch granules, tocosh ■ limit its consumption. According to popular belief, tocosh has been considered effective for treating postpartum, colds, pneumonia, hemorrhoids, gastric ulcers, as well as for healing wounds, as an antibacterial, and to prevent gastrointestinal infections.9 Currently, several industries require novel raw or modified starches that can be widely applied in many different fields, which can withstand the required processing, distribution, and storage conditions. However, to use a novel material, it is important to know its physicochemical, technological, and functional characteristics. There are few reports on the physicochemical properties of fermented potato starch. Xu et al. in 202010 reported the effect of fermentation by Lactobacillus plantarum strain on the physicochemical properties and morphological characteristics of potato starch. Fermentation increased α-amylase activity, starch granule crystallinity, as well as viscosity and gel hardness and chewiness of the potato starch. Likewise, in the case of sweet potato starch spontaneous fermentation by Acetobacter strains, five Bacillus strains and one Gluconacetobacter strain, an increase in amylolytic activity and a decrease in amylose content were demonstrated. The thermal and pasting properties as well as the hardness of the starch gel differed significantly.11,12 INTRODUCTION Potato (Solanum tuberosum) is an energy food due to its high starch content. In fresh potato tubers, the starch content is 13.5%−15% and approximately 75%−80% on a dry weight basis.1,2 Also, it is important to consider the effect of potato starch on human health, which is linked to the nutritional fractions of starch: rapidly digested starch (RDS), slowly digested starch (SDS), and resistant starch (RS), which, in turn, affect starch digestibility and, consequently, blood glycemic levels. A low glycemic index decreases risk factors for diabetes and dyslipidemia.3,4 In general, potatoes are mostly consumed fresh; although they are widely used for starch production and other industrial uses, including alcohol production. However, native starch structure is affected by processing conditions, such as pressure, temperature, and pH, which promote hydrolysis, retrogradation, and syneresis.5 Fermentation under water currents is one of the oldest known processes for the preservation of potatoes and other foods, such as corn, olluco, or arracacha. In Peru, the products obtained from this fermentation process are known as tocosh (meaning wrinkled and fermented). The traditional tocosh is the result of the bacterial fermentation of potato tubers (principally) stored in wells, wrapped in straw or ichu, and mechanically pressed with stones under a stream of spring water for 1−12 months depending on the variety and size of the potatoes, as well as on the water temperature.6,7 Potatoes subjected to this process potentially alter their conventional physicochemical properties and characteristics.8 The unpleasant odor in fermented potato pulp (tocosh) is the first sensory attribute to be perceived, which is a characteristic that does not © 2023 American Chemical Society Received: Revised: Accepted: Published: 465 December 2, 2022 February 12, 2023 February 14, 2023 February 27, 2023 https://doi.org/10.1021/acsfoodscitech.2c00400 ACS Food Sci. Technol. 2023, 3, 465−469 ACS Food Science & Technology pubs.acs.org/acsfoodscitech Article microscope with a vacuum and observed under two magnifications (50 and 200 μm). 2.5. Pasting and Thermal Properties. A differential scanning calorimeter (DSC) (ZL-3047A, Guangdong, China) was used to generate thermograms of both samples. A 1:2 starch−water suspension was prepared and hydrated for 18 h at room temperature. Then, 10 μg of this solution was weighed in aluminum trays and sealed tightly. Each sample was exposed to a temperature range of 40−110 °C, at a heating rate of 4 °C/min. In addition, an empty tray was used as a reference. The transition temperatures reported were the onset temperature (Ti), peak temperature (Tp), final temperature (Tf), and gelatinization enthalpy (ΔH). On the other hand, gelatinization properties of fermented potato meals were measured using a Rapid Visco analyzer (RVA) 4500 (Perten Instruments, Sweden) according to AACCI 76-21.01.11 Minimum viscosity, gel instability, final viscosity, gel stability, peak time, and gelatinization temperature were determined. 2.6. Functional Properties. The functional analyses of water absorption index (WAI), solubility index (SI), swelling power (SP), and paste clarity (PC) were conducted using the techniques described by Aristizábal and Sánchez in 2007.13 The syneresis analysis was conducted according to Bello-Pérez et al. in 2002.14 2.7. Statistical Analysis. Minitab statistical software (State College, PA) was used for data analysis. Results were expressed as means ± standard deviation of three independent replicates (n = 3), unless otherwise indicated. For statistical analysis, a one-factor analysis (ANOVA), followed by the Tukey−Kramer test, was performed to evaluate significant differences between treatments, at a significance level of α = 0.05. Physicochemical properties are mainly influenced by the changes in the amylose content, amylopectin chain-length distribution, as well as the average molecular weight of starch. Starch fermentation is a good strategy to expand its industrial applications in foods. There is not enough information on the characteristics of fermented potato starches processed under water currents, especially on their nutritionally important starch fractions. Hence, this research determined the physicochemical and functional properties of fermented potato meal from traditional (TPM) and alternative (APM) fermentation under water current procedures. 2. MATERIALS AND METHODS 2.1. Fermented Potato Meal Samples. The following fermented potato meal samples were donated by the International Federation of Scientific Societies, Foundation FISS (Cuenca, Ecuador, https://www.fissnet.org/jfiss/index.php/queesfiss): traditional fermented potato meal (TPM) (12.83% moisture; 3.29% protein; 1.14% fat; 0.26% ash; 3.57% crude fiber; and nitrogen free extract 78.94%) and alternative fermented potato meal (APM) (12.97% moisture; 4.2% protein; 0.92% fat; 0.36% ash; 3.3% crude fiber and nitrogen free extract 78.3%). TPM was a commercial sample, while APM was obtained from an organic crop, from tillage to harvest; its process was conducted in plastic tanks with spring water flow from the Tutupali region, in the province of Azuay, Ecuador (−2.9932796, −79.0810738). Both meals were stored under refrigeration (4−10 °C) prior to analysis. 2.2. Starch Chemical Composition. Total starch, amylose/ amylopectin, and D-glucose contents were quantified by colorimetric methods using commercial kits from the Megazyme brand (Megazyme International Ireland, Bry, Ireland). Tests were carried out by following the guidelines of the provider. The total starch assay kit is based on incubation of the starch sample with thermostable αamylase and amyloglucosidase enzymes. The amylose/amylopectin assay kit is based on the separation of amylose and amylopectin, precipitating the latter with the addition of concanavalin-A and removing it by centrifugation. The D-glucose assay kit uses high purity glucose oxidase and peroxidase to determine glucose. Finally, the damaged starch test kit, from the Megazyme, which is in accordance with AACC method 76-31.01, was performed following the supplier’s guidelines. Briefly, 100 mg of fermented potato (tocosh) flour was incubated at 40 °C for 10 min with 1 mL of fungal αamylase solution (50 U/mL). At the end of the time, 8 mL of dilute sulfuric acid solution (0.2%) was added to end the enzymatic reaction. The solution was centrifuged at 3000 rpm for 5 min and filtered (Whatman N°1). To 0.1 mL of the filtrate, 0.1 mL of amyloglucosidase solution (2U) was added, shaken, and incubated at 40 °C for 10 min. Finally, 4.0 mL of GPOD reagent solution was added and incubated at 40 °C for 20 min, and the absorbance of the solution at 510 nm against a reagent blank was determined. 2.3. In Vitro Digestibility. The analysis of in vitro digestibility was performed in raw and in gelatinized starches using the digestible starch and resistant starch assay kit from Megazyme, according to the procedures determined by McCleary et al. in 20194 and following the guidelines of the provider. Aliquots of the reaction solution were removed at 20 min to measure rapidly digestible starch (RDS) digested within 20 min; at 120 min to measure slowly digestible starch digested between 20 and 120 min (SDS120); at 240 min to measure slowly digestible starch digested between 120 and 240 min (SDS240); and resistant starch (RS) undigested after 240 min. 2.4. Starch Morphological Properties. Scanning electron micrographs (SEMs) were obtained with a Tescan MIRA3 microscope (Brno, Czech Republic) at 15 kV. Starch samples were placed on an electron microscopy sample holder, which was previously coated with double-sided carbon tape and specimens were covered with a 20 nm gold layer. Then, samples were placed under the 3. RESULTS AND DISCUSSION 3.1. Starch Chemical Composition. Total starch content was similar in both samples, while amylose values in TPM (25.7%) and APM (28.9%) (Table 1) were within those previously reported for potato starch of various cultivars, which typically contain 20%−33% amylose on a total starch basis.1 Differences in amylose content have been related to different factors, such as potato genotype, environmental conditions, Table 1. Chemical Composition of Raw and Gelatinized Starches of Fermented Potato Meals (DW)a Fermented potato meals Parameters TPM APM % Starch chemical composition (raw) Total starch 83.93 ± 5.68a 84.44 ± 1.30a Amylose 25.68 ± 1.56b 28.91 ± 1.10a b Damage starch 0.52 ± 0.03 0.87 ± 0.10a In vitro digestion (%) Raw starch RDS 17.90 ± 2.28a 17.12 ± 0.38a b SDS120 min 14.09 ± 1.02 39.45 ± 1.05a SDS240 min 37.73 ± 5.13a 4.38 ± 0.89b RS 30.27 ± 1.84b 40.67 ± 4.63a Gelatinized starch RDS 68.82 ± 1.38a 55.54 ± 1.62b SDS120 min 15.92 ± 3.45b 33.17 ± 2.00a SDS240 min 4.24 ± 1.86a ndb a RS 11.02 ± 0.21 11.30 ± 0.38a a Data are mean ± standard deviation of three replicates. Values with the same letters in the same row are not significantly different at p < 0.05. Abbreviations: DW, dry weight; TPM, traditional fermented potato meal, APM, alternative fermented potato meal; RDS, rapidly digested starch; SDS120, slowly digested starch at 120 min, SDS240, slowly digested starch at 240 min; RS, resistant starch. 466 https://doi.org/10.1021/acsfoodscitech.2c00400 ACS Food Sci. Technol. 2023, 3, 465−469 ACS Food Science & Technology pubs.acs.org/acsfoodscitech cultural practice, activity of enzymes-plant development, among others.15 Regarding the damaged starch, the APM sample showed more damaged starch (0.35%) than its traditional counterpart (TPM) (Table 1), which may be due to the mechanical forces applied during the milling process. 3.2. In Vitro Digestibility of Potato Starches. As expected, when raw starch from TPM and APM was gelatinized, RDS increased by 3.8- and 3.2-fold while resistant starch decreased by 2.7- and 2.2-fold, respectively (Table 1). RS in raw starch was higher in APM than in TPM, while achieving similar values in gelatinized starches (Table 1). It is reported that RDS levels in potato starch after gelatinization can be as much as 53%−86%;1,3 the RDS percentages obtained for both APM (55.5%) and for TPM (68.8%) were within the range. Englyst et al. in 19923 related the content of total digestible starch to mechanical damage since it increased digestibility. However, this will depend on the conditions during fermentation and whether it undergoes a cooking process. RS has been reported to be higher in raw potatoes than in cooked potatoes,16 and when raw potatoes are cooked, RS decreased to about 5%−10%.3 The values of SDS120 in raw starch were approximately 2.6-fold higher in APM than in TPM. However, while SDS120 had a similar percentage in gelatinized starch, SDS240 decreased drastically by 8.9-fold; in the case of APM, these were not detected. According to review information from Dupuis and Liu in 2019,1 SDS levels of cooked potatoes ranged between 1% and 45%, depending on the type of product, the cooking process, or the application of the cooling treatment. 3.3. Morphological Properties. Scanning electron microscope analysis (Figure 1) revealed that the TPM and APM did not show relevant damage to their granules, which had a smooth surface. This can be related to the percentage of Article damaged starch (DS), which was less than 0.6%, obtained in both samples (Table 1). Starch granules were different in size: larger granules had an oval-shaped structure, while smaller granules had a round-shaped structure. Size variations were more significant in APM than in TPM. Granule sizes ranged from 15 to 70 μm in length and from 20 to 100 μm in diameter. Dupuis and Liu in 20191 reviewed that native starch granules have a mean diameter of approximately 40−50 μm, with a range of 10−110 μm, and typical ovoid and spherical shapes. Information, which coincides with the micrographs showed herein (Figure 1), suggesting that the fermentation process applied in TPM and APM was not significantly affecting this pattern. Additionally, Dupuis and Liu1 reported that the structure of starch granules is influenced by genetic factors governing starch biosynthesis. 3.4. Pasting and Thermal Properties. The data for Ti, Tp, and Tf of the fermented potato meals can be observed in Table 2. These values were similar for both samples. ΔH in Table 2. Thermal and Gelatinization Properties of Fermented Potato Mealsa Fermented potato meals Parameters TPM Thermal properties Ti (°C) 62.69 ± 0.84a Tp (°C) 66,09 ± 0.84a Tf (°C) 67.64 ± 1.20a ΔH (J/g) 5.53 ± 0.12b Gelatinized properties Maximum viscosity (Pa·s) 82.54 ± 1.42a Gel instability (Pa·s) 55.14 ± 1.7a Final viscosity (Pa·s) 36.09 ± 0.07a Gel stability (Pa·s) 8.70 ± 0.22a Peak time (min) 4.31 ± 0.07a Pasting temperature (°C) 65.78 ± 0.59a APM 64.44 66.24 67.49 6.04 ± ± ± ± 1.34a 0.63a 0.70a 0.36a 68.31 45.93 31.19 8.81 4.25 68.00 ± ± ± ± ± ± 3.73b 3.20b 0.75b 0.13a 0.04a 0.47b a Data are mean ± standard deviation of minimum three replicates. Values with the same letters in the same row are not significantly different at p < 0.05. Abbreviations: TPM, traditional fermented potato meal; APM, alternative fermented potato meal. TPM and APM indicated values more distant from each other but close to a ΔH of 6. (Table 2). Pineda-Gómez et al. in 201017 reported that starch gelatinization enthalpies (corn starch) can decrease by increasing sample moisture and it will depend on the heating rate. On the other hand, RVA values (Table 2) were statistically different from each other, except for gel stability and peak time. These changes occurred during starch gelatinization as a consequence of heating in excess water under constant shear stress. In a study by Zaidul et al. in 200718 on potato starch, the following results were obtained: 65.26 Pa·s maximum viscosity; 19.84 Pa·s minimum viscosity; 45.42 Pa·s gel instability; 24.57 Pa·s final viscosity; 4.72 Pa·s gel stability; 3 min peak time; and 69.1 °C gelatinization temperature. These values are very close to those obtained herein for the APM sample (Table 2); however, in the samples of this investigation, gel stability results were higher than the 1.32 Pa·s reported by Alvis et al. in 200819 in their study on potato. Similar findings were earlier been reported by Montoya et al. in 201420 that the higher the amylose content, the higher the gel stability. As for the peak time of the TPM and APM samples, it exceeded the time of 3.40 min reported by Alvis et al. in Figure 1. Photography by scanning electron microscopy of traditional fermented potato meal (TPM) and alternative fermented potato meal (APM), observed to (A and C) 50 μm and (B and D) 200 μm, respectively. 467 https://doi.org/10.1021/acsfoodscitech.2c00400 ACS Food Sci. Technol. 2023, 3, 465−469 ACS Food Science & Technology pubs.acs.org/acsfoodscitech Article 200819 for potato starch. As longer times are needed for the starch gelatinization process to start swelling.20 As per the data shown in Table 2, the TPM was having lower amylose content (25.68%) than APM (28.91%). It reconfirms the findings of Zaidul et al. in 200718 that the amylose content is associated with higher peak viscosity and lower gelatinization temperature. Finally, gelatinization temperatures of 65.7 and 68 °C were obtained in TPM and APM samples, respectively. These values concur with those reported by Alvis et al. in 200819 with 66 ± 2 °C for potato starch. 3.5. Functional Properties. The results for water absorption index (WAI), water solubility index (WSI), swelling power (SP), and paste clarity (PC) were significantly different from each other (p < 0.05) (Table 3). There were slight starch, which is related to the reduction of digestibility. The results of the thermal properties are within the ranges established in standards and in bibliographic references, which determine the ease of adaptation of these meals to industrial food processes. Finally, it is recommended to conduct further research to complete the functional and toxicological studies and their effect on the human health. Table 3. Functional Properties of Fermented Potato Mealsa Authors ■ Corresponding Author Marco A. Lazo-Vélez − NutriOmics Research Group, Universidad del Azuay, Apartado 0101981 Cuenca, Ecuador; orcid.org/0000-0003-2857-7664; Email: malv@uazuay.edu.ec Karla Escandón − NutriOmics Research Group, Universidad del Azuay, Apartado 0101981 Cuenca, Ecuador Juan Carlos Gonzalez-Rojas − Laboratorio de Principios Activos y Seguridad Alimentaria, Universidad Católica de Cuenca − CIITT, Ricaurte 010108 Cuenca, Ecuador María José Carrera Flores − Laboratorio de Microbiología, Universidad Católica de Cuenca − CIITT, Ricaurte 010108 Cuenca, Ecuador Daniela Guardado Felix − Programa Regional de Posgrado en Biotecnología, Facultad de Ciencias Químico-Biológicas, Universidad Autónoma de Sinaloa, FCQB-UAS, AP 1354, CP 80000 Culiacán, Sinaloa, México; orcid.org/00000001-5983-5780 Complete contact information is available at: https://pubs.acs.org/10.1021/acsfoodscitech.2c00400 Fermented potato meals Parameters TPM Waters absorption index (g gel/flour) 7.95 Waters solubility index (%) 10.91 Swelling power 8.39 Paste clarity (% transmittance) 41.74 Syneresis (%) Cycle 1 51.35 Cycle 2 52.76 Cycle 3 55.34 ± ± ± ± 0.16a 0.44a 0.19a 1.51a ± 1.72a ± 2.56a ± 2.59a APM 6.61 12.12 7.00 10.54 ± ± ± ± AUTHOR INFORMATION 0.32b 0.00b 0.35b 0.18b 51,37 ± 0.96a 54.63 ± 0.82a 57.69 ± 2.30a a Data are mean ± standard deviation of minimum three replicates. Values with the same letters in the same row are not significantly different at p < 0.05. Abbreviations: TPM, traditional fermented potato meal; APM, alternative fermented potato meal. Funding differences in all functional properties, except in paste clarity. It has earlier been reported that different extraction techniques, potato varieties, storage conditions, and packaging affect structural and composition of potato starch, which also significantly impacted its WAI, WSI, SP, and syneresis.15 The paste clarity, however, has been reported to be negatively correlated with amylose content.21 Similarly, in the present investigation also, TPM had less amylose and more PC than APM (Table 1). Aristizábal and Sánchez in 200713 indicate that reference values for paste clarity (PC) in starches vary between 12.5% and 95% and starch pastes, with a transmittance lower than 40%, are considered opaque or turbid (Table 3). On the other hand, the water released in both samples was not significantly different from each other (p < 0.05). This value increased marginally as the number of freezing and thawing cycles increased for 3 days. The syneresis observed in TPM and APM (Table 3) was higher than those reported by Solarte-Montúfar et al. in 2019.22 The high percentage of syneresis observed in the present investigation can be is related to the amylose content. According to Aristizábal and Sánchez in 2007,13 retrogradation is associated with the amylose fraction, where high amylose concentrations resulted in the formation of opaque gels that undergo syneresis. Finally, a better understanding of the molecular and structural changes that occur in fermented potato meals would enable effective control of their functional behavior during food industrialization processes and consumption, as well as in the better knowledge of its health benefits. These meals show resistant starch contents than those of potato This research was supported by the NutriOmics Research Chair of Universidad del Azuay, Ecuador: project 2018-0052, and Universidad Católica de Cuenca, Ecuador: project PICVII19-73. Notes The authors declare no competing financial interest. ■ ACKNOWLEDGMENTS This research was supported by the NutriOmics Research Chair of Universidad del Azuay, Ecuador: project 2018-0052, and Universidad Católica de Cuenca, Ecuador: project PICVII19-73. Special thanks to the International Federation of Scientific Societies (FISS) and, on their behalf, to Santiago Agü i-Mendoza and Fabian A. Avila for donating and authorizing the use of commercial fermented potato samples (tocosh) and a fermented potato meal produced by the engineers; as well as to Granotec, Ecuador for performing the RVA; and finally, to Diego Panata and Lourdes Reinoso for their help during the experimental phase. ■ REFERENCES (1) Dupuis, J. H.; Liu, Q. 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