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Article

Synergetic Effect of Accentuated Cut Edges (ACE) and Macerating Enzymes on Aroma and Sensory Profiles of Marquette Red Wine

by
Yiliang Cheng
† and
Aude A. Watrelot
*
Department of Food Science and Human Nutrition, Iowa State University, 536 Farm House Lane, Ames, IA 50011, USA
*
Author to whom correspondence should be addressed.
†
Current address: Department of Viticulture and Enology, California State University, Fresno, 2360 E. Barstow Avenue, Fresno, CA 93740, USA.
Fermentation 2024, 10(12), 624; https://doi.org/10.3390/fermentation10120624
Submission received: 1 November 2024 / Revised: 2 December 2024 / Accepted: 3 December 2024 / Published: 6 December 2024
(This article belongs to the Special Issue Science and Technology of Winemaking)
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Abstract

:
This research explored the effects of using Accentuated Cut Edges (ACE) and macerating enzymes on the aroma and sensory profile of Marquette red wines after nine months of aging. The aroma analysis was conducted using gas chromatography-mass spectrometry (GC-MS) with solid-phase microextraction (SPME). The intensity of basic sensory attributes, including color, aroma, taste, and mouthfeel, were evaluated by eight trained panelists through descriptive analysis using 15 cm line scales. ACE treatment affected the aroma compounds profile, as suggested by the increased response ratio of ethyl butanoate, ethyl 2-methylpropanoate, and ethyl 3-methylbutanoate. Statistically, it significantly intensified honey (by 1.6 times) and green apple (by 2.1 times) notes, as perceived by panelists, compared to the control during the sensory descriptive analysis. Regardless of the type of enzymes, combined ACE and enzymes treatment amplified the color intensity of wine by up to 71.4% as observed by panelists, though this was not captured by spectrophotometric measurements (p > 0.05) from the previous study. A lower concentration of ester-derived compounds was found in ACE with enzymes wines, which was associated with the lower intensity of fruity notes during the descriptive analysis. Notably, none of the treatments affected astringency perception, likely due to the low concentration and small molecular weight of condensed tannins, alongside changes in the composition of soluble polysaccharide in Marquette red wines.

1. Introduction

Red wine quality is characterized by the comprehensive attributes of aroma, appearance, taste, and mouthfeel, making it a subject of comprehensive evaluation [1,2,3]. Among these, the aromatic profile of red wine is often the most captivating element for consumers. The aroma of red wines can be categorized into three main types: primary, secondary, and tertiary aromas. Primary aromas, also known as varietal aromas, are derived from the grape cultivar itself and include fruity, floral, and herbaceous notes, e.g., methoxypyrazines revealing vegetal or bell pepper aroma. Secondary aromas are a result of the alcoholic or malolactic fermentation process, primarily produced by yeast metabolism, and are characterized by esters, higher alcohols, and other volatile compounds that contribute to the wine’s complexity. Tertiary aromas, or bouquet, develop during the aging process in the bottle or barrel as a result of aroma extracted from oak or microbial spoilage or chemical tainting, leading to the emergence of more nuanced and sophisticated scents such as spice, earth, and oak [4].
The research on the profile of aroma compounds in cold hardy interspecific grapes and the resulting wine is relatively limited compared to the extensive studies on Vitis vinifera grapes and red wines. For instance, ‘Marquette’ is one of the most popular red wine grape cultivars in the Upper Midwest regions, developed by the University of Minnesota’s grape breeding program. It is an interspecific grape cultivar, resulting from the cross between different Vitis species, including Vitis vinifera and Vitis riparia [5,6]. The Marquette grape is known for its cold hardiness and disease resistance, and its wine is typically characterized by aroma notes including cherry, spice, black pepper, and berry [6]. However, no descriptive sensory evaluation has been conducted on Marquette wine to provide a comprehensive understanding of its sensory attributes. C13-Norisoprenoid and terpenes are primary aroma compounds found in Marquette grapes and wines. C13-Norisoprenoids, such as β-damascenone, contribute to floral and fruity aromas while terpenes, like linalool, are responsible for floral and citrus notes [4,7]. During winemaking, these compounds are developed and released from grape skins, especially during fermentation and maceration, enhancing the wine’s aroma profile. The profile of these compounds can be modified by multiple factors, including fermentation temperature, pH, and the presence of exogenous glucosidases [4].
Ethyl esters and acetate esters are commonly found in Marquette red wines [5,7,8]. The formation of esters in red wine mainly happens during alcoholic fermentation and aging. Specifically, ethyl esters are formed by the esterification of ethanol with various fatty acids. For example, hexanoic acid and octanoic acid are the precursors of ethyl hexanoate and ethyl octanoate, respectively. Ethyl esters typically contribute fruity and floral notes to the wine, with the exception of ethyl acetate, which can provide an undesirable vinegar-like or nail polish remover-like odor at high concentration. On the other hand, acetate esters are formed by the enzymatic acetylation of alcohols during fermentation, such as the reaction between isoamyl alcohol and acetic acid to form isoamyl acetate. Similarly to ethyl esters, they generally impart fruit (like banana and cherry) and floral odors into the wine [4,9].
Higher alcohols are a group of alcohols with more than two carbon atoms and are found in red wine as byproducts of yeast fermentation during winemaking. They can also react with carboxylic acids to form esters, such as the abovementioned isoamyl alcohol. Common higher alcohols in Marquette wine include isobutanol, isoamyl alcohol, and 2-phenylethanol [5,7]. They can positively contribute to the complexity and enhance the overall aroma profile of red wine at moderate concentrations. However, the high concentration of these compounds can induce undesirable solvent-like or pungent odors. Therefore, the balance and concentration of these compounds are important factors in determining the quality and sensory characteristics of the wine [10].
In addition to volatile aroma compounds, phenolic compounds extracted from grape berries and distributed in red wines have been widely related to complex sensory perceptions including appearance and mouthfeel. Anthocyanins and their derivatives are pigments that contribute to red wine color attributes [11]. The initial assessment of a wine, even before aroma and taste, begins with the visual evaluation of appearance and color characteristics, such as hue and color intensity. Hue refers to the color tone of the wine when observed visually from red-tawny to red-purple, indicating the progression of monomeric anthocyanins, copigmentation, and the formation of polymeric pigments during wine aging [12]. Color intensity, on the other hand, assesses the depth or saturation of wine color, influenced by grape variety, winemaking techniques, and the development of stable pigments during aging [13,14]. Both hue and color intensity provide valuable insights into the age of wines and contribute to the overall sensory impression. Hence, the stability of these color attributes in red wine is critical to a consumer’s sensory experience [3].
Condensed tannin is another crucial phenolic compound responsible for the development of stable pigments and wine mouthfeel, which depends on their structural composition and size. They provide balance in the wine’s matrix composition, which includes residual sugars, acids, and polysaccharides, among others [3,15]. Specifically, tannins extracted from grape skins are associated with pleasant and velvety astringency descriptors, positively impacting the overall quality of red wine. In contrast, the extraction of seed tannins may be viewed negatively from a sensory perspective, as seed tannins tend to elicit a more intense bitterness rather than astringency due to their relatively short structure or low degree of polymerization [16].
Given the significant impact of phenolic compounds on red wine quality in terms of mouthfeel and color characteristics, advanced winemaking techniques are focused on improving the extraction of anthocyanin-derived pigments and condensed tannin from grape skin tissues during the fermentation process. Among these techniques, Accentuated Cut Edges (ACE) and the use of macerating enzymes like pectinases are notable examples. ACE mechanically breaks down grape skin structure, while pectinases enzymatically facilitate the cell wall breakdown, both aiming to promote the extraction of phenolic compound extraction during winemaking. For red wines made from Vitis vinifera grapes, ACE treatments significantly improved color density by 68% in cv. Pinot noir red wines, and this was associated with intensified astringency and dark fruit aroma, as perceived by trained panelists [17]. However, while ACE treatment enhanced the perception of astringency in cv. Shiraz red wines, it resulted in an increase in the flavors of earthy and dusty notes and a lesser enhancement in color density of only 17% [18]. These inconsistencies show that the impact of winemaking techniques on red wine quality strongly depends on the grape cultivar and necessitates comprehensive evaluation. The enhancement of color intensity and astringency perception, leading to a better-balanced wine structure, has been widely observed when applying macerating enzymes to V. vinifera wines, including cv. Monastrell wine [12], Shiraz wine [19], and Cabernet Sauvignon wines [20]. In contrast, interspecific cold-hardy grapes (e.g., cv. Marquette and Frontenac), which are extensively grown in the Upper Midwest regions, exhibit unique chemical properties, including high acidity and low astringency sensory properties. There has been limited investigation into the aroma [2,5], color, and sensory characteristics [21] of red wines made from cold-hardy grapes, particularly after the application of winemaking techniques aimed at improving tannin.
In our previous studies, we demonstrated the effect of combining ACE and macerating enzymes on cell wall polysaccharide degradation, thus promoting the extraction of phenolic compounds in Marquette red wines. Overall, the combined treatments resulted in a 20% increase in monomeric phenolics and a 21% increase in tannins after nine months of aging. When applied individually, ACE or enzyme treatments had minimal effect on phenolic extraction in the finished wines [22]. Building on these findings, the present study aimed to determine the potential improvements of wine quality when these winemaking techniques are used in combination. We hypothesized that the synergistic effect of ACE and macerating enzymes on cell wall degradation will enhance the overall quality of Marquette red wines, specifically in terms of aroma compound extraction and color stability, without introducing any earthy/dusty aroma. Furthermore, the rise in tannin concentrations resulting from the use of ACE plus macerating enzymes, as observed in our previous studies [22], is expected to be perceived by trained panelists as an increase in astringency intensity. To evaluate this, a comprehensive evaluation of Marquette red wine quality after nine months of aging was conducted in this study. The profiles of volatile aroma compounds were instrumentally compared across treatments. Additionally, the sensory attributes of red wine subjected to different treatments were analyzed by conducting a descriptive sensory analysis with trained panelists.

2. Materials and Methods

2.1. Chemicals, Reagents, and Standards

Hexane (≥99%), 1-octanol, sodium chloride, ethyl butanoate, 2-phenylethanol, isoamyl acetate, ethyl octanoate and 4-ethylphenol were purchased from Sigma Aldrich (St. Louis, MO, USA). 200 proof ethanol, L-(+)-tartaric acid, ethyl acetate, and sodium hydroxide were purchased from Fisher Scientific (Santa Clara, CA, USA). 1-hexanol (≥99%) was provided by Alfa Aesar (Haverhill, MA, USA). Milli-Q water used to prepare solutions and reagents was obtained from a Barnstead MicroPure Water Purification System (Thermo scientific®, Waltham, MA, USA).

2.2. Grape Samples and Winemaking

The grape samples and detailed winemaking protocols were previously reported as experiment 2 [22]. Marquette grapes (Vitis spp.) used for this study were harvested from the Iowa State University (ISU) Horticulture Research Station vineyard in Ames, Iowa (42°06′ N; 93°35′ W). The climate is humid continental and defined as USDA Plant Hardiness Zone 5b (https://planthardiness.ars.usda.gov (accessed on 21 November 2024)). The grapes were grown in moderately eroded Clarion loam soil. Chemical substances were used for pest protection, and no fertilizers were applied during the growing season.
Briefly, these grapes were hand-harvested from the ISU Horticulture Research Station, IA on 25 August 2021 (pH 3.01 ± 0.02, TA 10.3 ± 0.0 g/L, 26.7 ± 0.1 °Brix). Following a 30 mg/L sulfur dioxide (SO2) spray, grapes were processed the same day at the ISU Food Science Building winery.
Post-harvest, Marquette grapes were crushed, destemmed, and 10 kg of must was randomly allocated to 18.9 L buckets. Treatments consisted of the control (CTL-21), application of ACE to the must (ACE-20), the addition of ACE combined with 0.022 mL/kg Scottzyme PEC5L (Scott Laboratories, Petaluma, CA, USA) (ACE-PEC-21), and ACE combined with 0.01 g/kg Rapidase Clear Extreme (Scott Laboratories, Petaluma, CA, USA) (ACE-RCE-21). Pectinase PEC and RCE are both commercial macerating enzymes with differing activities, as displayed in Supplementary Table S1.
Post-treatment, the winemaking procedure remained consistent across both experiments with detailed descriptions as previously published [22]. Briefly, treated musts were inoculated with ICV D254 yeast and GoFerm (Scott Laboratories, Petaluma, CA, USA), underwent a seven-day alcoholic fermentation, and were pressed. This was followed by inoculation with Lalvin VP41 lactic acid bacteria, racking, and sulfur dioxide addition. The wines were then argon-flushed, cold stabilized, and bottled. They were stored in a controlled cellar for nine months and then flushed with nitrogen and stored at −20 °C before analysis. After nine months of aging, Marquette wines were opened and analyzed for aroma, color, and sensory attributes. The basic physiochemistry of the aged Marquette were as follows: pH 3.30 ± 0.0, TA 8.3 ± 0.2 g/L, ethanol content 14.9 ± 0.3 vol%. No significant differences in these physicochemical parameters were observed among the treatments.

2.3. Aroma Analysis by Gas Chromatography-Mass Spectrometry (GC-MS) with Solid-Phase Microextraction (SPME)

Wine samples (4 mL) were transferred into amber vials (10 mL, screw thread headspace vials, Wheaton®, Millville, NJ, USA) with metal screw top lids (headspace cap PTFE/Butyl, Wheaton®, Millville, NJ, USA). Sodium chloride (2 ± 0.05 g) was added into all samples to adjust the ionic strength. The internal standard was added to each 4 mL of wine with a final concentration of 2 mg/L, which was achieved by adding 16 µL of 1-octanol in hexane (500 mg/L), followed with vortex before analysis. The analysis of wine volatile aroma compounds was conducted through an Agilent 7890B gas chromatography (GC) system and equipped with CTC Combi PAL autosampler (LEAP Technologies, Carrboro, NC, USA) and Agilent 5977A mass selective detector (MSD). The optimized sampling and GC-MS system parameters described in previous publications [5,8]. Briefly, solid phase microextraction (SPME) fiber was coated with 50/30 µm Divinylbenzene (DVB)/Carboxen (CAR)/Polydimethylsiloxane (PDMS) (Supelco®, Bellefonte, PA, USA). The fiber was preconditioned (cleaned) and placed through the septa prior to sampling. The fiber was thermally desorbed in a 260 °C GC inlet for 2 min before exposure in sample headspace. Headspace equilibrium was achieved by incubating the sealed vials at 50 °C for 10 min with continuous agitation at 500 rpm. The SPME fiber was then exposed to the vial headspace for 10 min under the same temperature and agitation conditions to ensure consistent adsorption of volatile compounds.
The two-column system was performed firstly with a non-polar column, BPX-5 stationary phase with dimensions 30 m length × 0.53 mm ID × 0.5 µm film thickness (SGE, Austin, TX, USA), followed by the second polar column, SOLGEL-Wax stationary phase with dimensions of 30 m length × 0.53 mm ID × 0.5 µm film thickness (SGE, Austin, TX, USA). The carrier gas was ultra-high purity (99.999%) helium with combination oxygen and moisture in-line gas trap and with the following instrument parameters: GC inlet temperature, 260 °C; FID, 280 °C; column, 40 °C initial, 3.0 min hold, 7 °C per min ramp, 220 °C final, 11.29 min hold. The ionization energy was 70 eV of the electron ionization (EI) mode within the operation of the mass detector.
Aroma compound data were generated using Automated Mass Spectral Deconvolution and Identification System (AMDIS) as described in the previous study [8]. Briefly, the signal of compounds was searched and identified with a target library with at least 80% mass spectral match for compounds identification. The MS full scan range was set from 32 to 450 m/z. The internal standard, 1-octanol, was used to calculate the response ratio of each compound relative to the standard sample. The response ratio was calculated as the ratio of the volatile aroma compound peak area to the 1-octanol internal standard peak area, as described in previous publications [17,23].

2.4. Training Sessions and Descriptive Sensory Evaluation

The panel consisted of 8 members (4 males and 4 females) aged 21 to over 65 trained in descriptive analysis in the Food Science and Human Nutrition Department at Iowa State University. The panelists were first trained in six one-hour-long sessions to narrow down the sensory evaluation descriptors and ensure accuracy and reproducibility. During the training sessions, the researchers of this project led the discussion and guided the panelists to become familiar with the descriptors and make sure they could perceive and agree with all the descriptions from the example Marquette red wines. These sessions allowed the participants to discuss and generate the terms describing the aroma, taste, mouthfeel, and color attributes (Table 1) of the four wine conditions (CTL, ACE, ACE-PEC, and ACE-RCE).
The evaluation session (n = 3) was divided into two parts to analyze color and the remaining attributes of Marquette red wines (vintage 2021, after nine months of aging) separately. The evaluation was performed under controlled conditions in an individual booth. The evaluation of color attributes was performed under natural light with transparent glasses. The color swatch (Hue: purple, ruby, garnet, tawny. Color intensity: pale, medium, deep) used during the training session was also available during the evaluation session in the booth. To avoid the bias from wine color, the evaluation of remaining attributes (aroma, taste, and mouthfeel) was performed in black glasses. Before the second part of the evaluation session, the panelists started with a quiz of aroma, taste, and mouthfeel attributes by providing all these attributes (Table 1) as blind references with code numbers to panelists. During the one-hour evaluation sessions, the participants received and evaluated four wine conditions at each time and repeated this process to finish the evaluation for all conditions in biological triplicate. All wines were provided with 30 mL per wine (measured by pourers) with a 3-digital random number at room temperature. The descriptive analysis was carried out using the 15 cm line scale to measure the intensity of each sensory attribute throughout the Compusense® software (Version v23.0.26998, Compusense Inc., Guelph, ON, Canada).

2.5. Statistical Analysis

All statistical analyses were performed using JMP® Pro 16.1.0 software (SAS, Cary, NC, USA). One-way analysis of variance (ANOVA) and post hoc Tukey’s HSD significant difference test (α = 0.05) were used to analyze the effect of winemaking techniques for GC-MS aroma compounds and spectrophotometric color analysis. Two-way analysis of variance (ANOVA) and post hoc Tukey’s HSD significant difference test (α = 0.05) were used to analyze the effect of winemaking techniques (treatments) and panelists for sensory evaluation.

3. Results and Discussion

3.1. Wine Aroma Profile by GC-MS

Volatile compounds were detected by GC-MS with headspace solid-phase microextraction (SPME) and reported as the response ratio in Table 2. Compounds are categorized into ethyl esters, acetate esters, higher alcohols, C13-Norisoprenoid, and terpenes. Esters are essential aroma compounds, primarily formed during the early stage of alcoholic fermentation through the esterification of carboxylic acids. These contribute to pleasant aromas in red wines [4,10]. Overall, in Marquette wines, the response ratio of ethyl acetate was the highest at 0.90, followed by ethyl octanoate at 0.64. Ethyl acetate is one of the most dominant esters formed in wine during the esterification of acetic acid, which is the by-product of yeast metabolism [4]. The reaction between ethanol and acetic acid, facilitated by the acidic environment of the wine, leads to the formation of ethyl acetate [9]. A high concentration of ethyl acetate is associated with a vinegar-like odor and is characterized as a wine fault [9]. Particularly, the formation and accumulation of ethyl acetate could be prevented during alcoholic fermentation through careful yeast strain selection, optimization of fermentation conditions (e.g., temperature and nutrient management), and strict oxygen management. These practices help control excessive ethyl acetate production, which can result in undesirable nail polish remover-like flavors in wine [9]. The subsequent ethyl esters mainly contribute to the fruity and sweet odors in red wines, including descriptors like banana, green apple, tropical fruit, and bubble gum [2,10,24]. The treatments of ACE with or without enzymes did not significantly impact the response ratio of ethyl acetate in wines, most likely because the formation of ethyl acetate is primarily influenced by factors such as yeast strain, yeast action during fermentation, and acetic acid bacteria action during aging [25]. Since ACE and enzymes are winemaking techniques that do not directly affect these factors, their impact on ethyl acetate response ratio may not be significant. In general, the application of ACE plus maceration enzymes, regardless of the enzyme type, significantly decreased the response ratio of ethyl butanoate, ethyl 2-methylpropanoate, and ethyl 3-methylbutanoate when compared to the ACE-treated wine, but did not differ from the control. This result suggested that using ACE treatment solely improved the intensity of fruity and pleasant ethyl ester-derived aroma compounds, while the combination of enzyme negatively affected the extraction and perception. A similar trend was observed in a previous study, where ACE-treated wine resulted in a 20% higher ratio of ethyl butanoate and made the wine richer in fruity, peach, and black currant aromas [17]. Regarding acetate esters, isoamyl acetate and isobutyl acetate were not affected by any of the wine treatments.
Rice et al. [5] observed a decline in the concentration of ethyl esters with increasing grape maturity, demonstrated by a lower level of ethyl hexanoate in Marquette wines; 9.5 and 1.3 mg/L made from berries harvested at 22 and 24 °Brix, respectively. A similar trend of decreasing ethyl esters, particularly ethyl hexanoate and octanoate, was noted in the maturation of Cabernet Sauvignon grapes as Brix levels rose from 20.9 to 22.7 [26]. This pattern might explain why many ethyl esters were undetected in this study’s Marquette wine, which was made from berries harvested at higher Brix levels of 26.3 to 26.7. However, previous studies have also pointed out the complexity of the relationship between grape maturity and yeast metabolism of ethyl esters, influenced by various factors such as fermentation temperature, skin contact duration, and yeast strain selection [9,26].
In Marquette red wines, the most abundant higher alcohols identified based on the response ratio were isobutanol at 0.25, isoamyl alcohol at 2.52, and 2-phenylethanol at 0.43. These compounds are primarily produced as byproducts of yeast metabolism from the amino acids valine, leucine, and phenylalanine, respectively [4]. The odor descriptor for isobutanol and isoamyl alcohol include chemical, solvent, and fusel [2,4]. 2-phenylethanol is characterized by a strong rose- and honey-like aroma, and it is considered an important aroma compound in red wines [4,27]. These higher alcohols were present in all Marquette wine samples without significant differences between treatments. Additionally, 1-butanol were not quantified in any of the samples due to the lack of signal and peak area. According to Slegers et al. [7], isoamyl alcohol was only found in trace amounts in Marquette grapes from Quebec and was not detected in the wines produced from those grapes [7]. In contrast, isoamyl alcohol is one of the top five most abundant aroma compounds in Marquette wine made from grapes grown in Iowa, as reported in another study, although the exact concentration was not reported [23].
The last two categories of aroma compounds in Marquette wines are C13-norisoprenoids and terpenes, known for their floral, fruity, and citrus notes [4]. These compounds are typically associated with the primary aromas of wines, which originate from the grape itself rather than fermentation or aging processes. However, in this study, the aroma compounds within these categories, including β-damascenone, linalool, p-cymene, and β-citronellol, were not affected by any of the wine treatments from a statistical standpoint. This suggested that ACE and maceration enzymes did not affect the extraction and perception of primary aromas from grapes. Marquette juice has been reported to contain a large amount of C13-norisoprenoids (11 µg/L, e.g., β-damascenone and α-ionone) and terpenes (5 µg/L, e.g., linalool and geraniol) at harvest in Quebec, Canada [7,28]. After 6 months of aging, the concentration of C13-norisoprenoids dropped to 2 µg/L and terpenes increased to 99 µg/L [7]. However, these compounds were not measured in either grape juice or red wine from Marquette berries grown in Iowa [8,23]. In addition to the growing location, one possible explanation of the low response ratio of both C13-norisoprenoids and terpenes in our study could be due to variations in the winemaking process. For example, the previous study in Quebec included a cold soaking process prior fermentation, which may remarkably enhance the extraction of these aroma compounds, as both C13-norisoprenoids and terpenes are primarily located in grape skins rather than in the juice [7]. Consequently, these inconsistences of aroma profile highlight the impact of winemaking techniques and growing locations on the aroma profile of wines made from the same grape cultivars.
According to Sparrow et al. [17], the use of ACE treatment slightly increased the response ratio of butanol (fruity, fusel, and spirituous odors) and ethyl butanoate (fruity, peach, black currant odors) in Pinot noir wine, while decreasing the ratio of ethyl 2-methylpropanoate, ethyl 2-methylbutanoate, and ethyl 3-methylbutanoate (fruity odors). Overall, the extraction induced by ACE treatment also enhanced the wine aroma profile by increasing the intensity of fruit-like aroma compounds [17]. The observed increase in ethyl ester concentration in ACE-treated Pinot noir wine could be due to improved extraction of nitrogen compounds from the grape pulp and skin, which are thoroughly broken down following ACE treatment. This is important because the production of ethyl esters during fermentation is greatly affected by the concentration of nitrogen compounds and must solids [9]. However, the effect of ACE treatment on yeast assimilable nitrogen (YAN) has not been evaluated in either previous research or our study, as it was not the main point of focus. Furthermore, the variation in yeast strain used in previous study on Pinot noir (Lalvin RC212™) and our study on Marquette (ICV D254 yeast®) could be a contributing factor to the observed differences in the modification of ethyl ester profile during winemaking.
Rollero et al. [29] demonstrated that the enzymatic activity of pectinase, which includes enzymes like polygalacturonases, pectin methylesterases, and pectin lyase, break down pectins of the cell walls. This modification of grape cell walls leads to an increase in the aroma precursors (e.g., hexanoic acid, octanoic acid, and isoamyl alcohol) and consequently results in the increase in aroma compounds (e.g., ethyl hexanoate, ethyl octanoate, isoamyl acetate) in Shiraz wine. The impact of macerating enzymes on the release of aroma compounds varies significantly depending on the grape variety. For example, these enzymes can enhance the release of the free forms of terpenes and C13-norisoprenoids in Albariño white wine, whereas no effect was observed on the release of linalool in Furmint white wine. Linalool was the only monoterpene compound that could be quantified in this previous study [30]. Similarly, the low response ratio of aroma compounds poses challenges in evaluating the effects of different treatments in this studies’ Marquette wines.

3.2. Wine Aroma Profile by Descriptive Sensory Analysis

The attribute used to describe the Marquette wines after nine months of aging were displayed in Figure 1 with the mean score to evaluate the aroma intensity perceived by the trained panelists (n = 8). The most dominant aroma attributes in the CTL wine were alcohol, cider, and acetone, with mean scores of 3.8, 3.5, and 2, respectively, on a 15 cm line scale. The descriptor of fruit-related attributes were grape jelly, black cherry, black currant, and green apple, with mean scores of 2.9, 2.0, 2.0, and 1.2 out of 15 cm line scale, respectively. Marquette red wine is commonly associated with distinct flavor profiles of cherry, spice, black pepper, and berry [6]. The fruity notes were identified as consensus attributes by the panelists during the training session, including strawberry and black cherry. No descriptive sensory analysis has been conducted specifically on Marquette red wines in the past, which makes it challenging to compare.
Based on the analysis of aroma compounds as reported in Table 2, the key aroma compounds in Marquette red wine after 9 months of aging were ethyl acetate, ethyl hexanoate, isobutanol, isoamyl alcohol, and 2-phenylethanol. These compounds are associated with odor descriptions such as nail polish remover, green apple, alcohol, fusel, and honey, respectively [4,10]. The presence of these aroma compounds can partially explain the detection of aroma descriptors including acetone, green apple, alcohol, and honey by trained panelists in Figure 1. Although only trace amounts of other ethyl esters (e.g., ethyl octanoate) could be detected in Marquette wine by GC-MS, these various aroma compounds contribute to the perception of fruity and sweet odor descriptions such as strawberry and candy fruit [4,10].
The aroma attributes of Marquette wines made with different winemaking techniques significantly altered the intensity of certain attributes, including honey and green apple (p < 0.05). The perception of a honey-like aroma could be attributed to certain aroma compounds such as 2-phenylethanol, 2-phenylethyl acetate, and 2-phenylacetaldehyde [7,31], of which only 2-phenylethanol was detected during the measurement of volatile aroma compounds by GC-MS. Despite the lack of significant difference in the response ratio of 2-phenylethanol between treatment groups, the trained panelists perceived a stronger honey-like aroma note from the wine treated with ACE alone compared to the wines treated with ACE-PEC and ACE-RCE. Similarly, the ACE-treated wine exhibited a significantly higher intensity of green apple notes compared to the ACE-PEC and ACE-RCE wines, despite having a similar level of ethyl hexanoate as the control. This difference could be due to interactions between 2-phenylethanol or ethyl hexanoate and other aroma compounds, which might alter the overall perception of the green apple aroma. Given the complexity of wine aroma and the potential for synergistic effects, the presence or response ratio of a single compound does not always directly translate to sensory perception. Other volatile compounds, even in small amounts, may interact with 2-phenylethanol or ethyl hexanoate, changing their aromatic impact [32].
Furthermore, the use of ACE in combination with macerating enzymes had no impact on the intensity of aroma descriptors, which was in line with the results of the GC-MS measurements. In addition, Kang et al. [18] found that Shiraz red wine treated with ACE exhibited an elevated intensity of earthy/dusty flavor profiles. However, this characteristic was not detected in Marquette wine during the training session, which may be attributed to differences in the grape varieties used.

3.3. Wine Color Attributes by Instrumental and Sensory Analysis

The color properties of Marquette red wine after 9 months of aging were measured using sensory analysis, as shown in Table 3. Panelists perceived higher color intensity values in both ACE-PEC and ACE-RCE wines, scoring 4.8 on the 15 cm line scale, compared to the control wine (2.8) and the ACE wine (3.0). This suggests that the ACE-PEC and ACE-RCE wines exhibited a deeper and more saturated color. Interestingly, no significant differences in hue between Marquette red wines after aging was perceived by either the panelists in this study or by spectrophotometry, as reported previously [22]. This suggested that the use of ACE with or without enzymes did not affect the hue of the Marquette red wines. The phenolic compound and pigment profiles of Marquette red wine were previously measured [22]. According to our previous analysis, the combination of ACE and macerating enzymes significantly increased the concentration of non-anthocyanin phenolics and resulted in a higher amount of small polymeric pigment (1.8–1.9) compared to the control and ACE wine (both 1.7). Despite the lack of significant variation in polymeric pigments detected by the instrument [22], the trained panelists were more sensitive in perceiving changes in color intensity induced by the synergistic effect of ACE plus macerating enzymes, regardless of the enzyme type.
Sparrow et al. found that ACE-treated Pinot noir wine contained a 1.7-fold higher value in color density and received significantly higher sensory scores for its red appearance compared to the control [17]. However, the effect of ACE treatment on color attributes of Marquette wines was not perceived in our study. A possible explanation could be that Marquette red wine contains anthocyanin in various forms (predominantly in diglucoside forms) and is low in condensed tannins needed to form stable pigments [33]. The inconsistency in the effect of ACE treatment on color attributes was also observed between Pinot noir and Shiraz. A previous study found that ACE treatment did not lead to color changes in Shiraz wine when using CIELab color measurement. The authors explained that this could be due to the grape varieties, as Shiraz grapes naturally have more red pigments and a darker color than Pinot noir [18]. Similarly, in an additional project, we observed varietal differences between Pinot noir and Marquette. Marquette’s thinner grape skin may enhance anthocyanin extraction, and the presence of pigments in the pulp could also contribute to these differences (Supplementary Figure S1).
An earlier study revealed that using macerating enzymes (including polygalacturonase, pectin esterase, pectin lyase, hemicellulase, and cellulase) resulted in similar color attributes (color intensity and tint) in Monastrell wine after eight months of aging when compared to the control. However, in the same study, trained panelists rated the enzyme-treated wine with higher mean scores in color intensity and purple tint, suggesting that macerating enzymes changed the chromatic characteristics as part of the sensory properties [12]. The positive effect on color could be attributed to the increased degradation of pulp tissues by macerating enzymes, which promotes the extraction of phenolic acids and flavonols to form stable pigments (i.e., co-pigmentation phenomenon) over aging [12,34]. This effect is particularly relevant in Marquette grapes, which contain pigments in their pulp tissues as shown in Supplementary Figure S1 and further contributing to color development due to pulp degradation. Similarly, in the study by Bautista-Ortin et al. [12], panelists scored a higher color intensity in enzyme-treated Monastrell wine after aging than in the control, despite no differences being detected instrumentally when calculating the sum of absorbance at 420, 520, and 620 nm [22]. This aligns with our observations in aged Marquette wine. As explained by Fan et al. [35], human perception of red wine color is comprehensive, considering the full spectrum of color and lightness. Instruments provide objective and repeatable results based on specific absorbance wavelengths, while panelists evaluate wine color intensity by considering complex visual information, including lightness with the assistance of a color swatch to reduce bias. This highlights the importance of sensory evaluation in capturing the subtleties of wine color attributes that instruments may overlook.
Di Profio et al. [34] suggested that the change in color attributes could also be due to the decrease in pH induced by macerating enzymes (with endopolygalacturonase, pectin methyl esterase, endo-pectinlyase, and protease), therefore affecting the anthocyanin chemistry by shifting to the flavylium ion forms of anthocyanins. However, this effect could be ruled out in our study as there was no treatment effect on the pH value among all samples (average 3.3, as presented in Supplementary Table S2). Depending on the cultivars and enzyme types, the addition of macerating enzyme (containing predominantly polygalacturonase activity with arabinose side activity) may also have no effect on the color density and formation of the stable pigments in Shiraz wine, and no difference in color can be perceived by trained panelists [19].

3.4. Wine Sensory Attributes of Taste and Mouthfeel

The most prominent taste attribute in the control wines was sourness, which showed the highest average score (5.7), followed by bitterness (2.6), sweetness (1.2), and saltiness (0.3) on a 15 cm line scale (Figure 2). The high intensity of sourness perceived in the Marquette wines could be related to their high titratable acidity (averaged at 8.3 g/L), as it was noted in an earlier part of this study (Supplementary Table S2) [22]. Wines made from cold-hardy grape varieties, compared to those from Vitis vinifera, are generally characterized by greater titratable acidity [36]. As for the mouthfeel properties, astringency (3.0) and hotness (3.1) were the two primary attributes, followed by viscosity (2.7) and tingly (1.2). No significant difference was observed among the treatment groups for these attributes. The hotness was associated with the high alcohol concentration (14.9 vol%) in Marquette wines, as the value reported in Supplementary Table S2. The perception of bitterness and astringency in wines is mainly attributed to the presence of phenolic compounds, notably monomeric or polymeric flavan-3-ols. Our previous study revealed that Marquette red wines treated with ACE-PEC and ACE-RCE exhibited significantly higher concentrations of (+)-catechin, (−)-epicatechin, and condensed tannins. Furthermore, the mean degree of polymerization of condensed tannins, as determined in our previous analysis, averaged at 2.6, implying that these compounds were primarily present as dimers or trimers. These compounds tend to impart more bitterness than astringency [16]. Despite the differences in phenolic compound concentrations resulting from the various treatments, no significant effects were observed on the taste or mouthfeel attributes. In contrast, ACE treatment of Pinot noir grapes during winemaking led to a nearly 7-fold increase in the concentration of condensed tannins compared to the control after aging, which in turn led to an increased intensity of both astringency and bitterness during sensory evaluation [17]. A similar improvement in tannin concentrations and astringency intensity was also observed in ACE-treated Shiraz red wines [18]. In addition to bitterness and astringency, ACE treatment did not significantly affect the perception of other taste and mouthfeel attributes, including sourness, sweetness, hotness, and viscosity in studies conducted on both Pinot noir [17] and Shiraz wines [18].
Moreover, previous studies have indicated that using macerating enzymes, which mainly contain endo-polygalacturonase, can improve Cabernet Sauvignon wine quality by promoting the extraction of condensed tannins, resulting in a 13% increase in astringency intensity [20]. However, the same prior study also noted that enzyme treatment shifted the descriptors of astringency from positive (velvety and soft) to negative (grippy and chalky) [20]. It is worth noting that the concentrations of condensed tannins in these previous studies under control conditions (310 mg/L in Shiraz and 800–1200 mg/L in Cabernet Sauvignon red wines) were significantly higher than the concentration found in Marquette red wines (70 mg/L).
In comparison, the use of ACE treatment only triggered a slight modification in the composition of soluble polysaccharides in Marquette red wines, whereas macerating enzymes significantly degraded the structure of Polysaccharides Rich in Arabinose and Galactose (PRAG), by removing the arabinose side chains and promoting the release of rhamnogalacturonan (RG)-II. These trends have been observed from our prior measurements of this study and are consistent with previously published studies in enzyme-treated Carignan red wines [13] and Merlot red wines [37]. Previous studies with descriptive sensory analysis have demonstrated that RG-II significantly decreased the intensity of astringency in terms of multiple descriptors, including roughness, chalkiness, dryness, puckering, coarseness, and fullness. These studies also explained that potential mechanisms behind this reduction in astringency are either that RG-II may have co-aggregated with astringency-triggering compounds, i.e., condensed tannin, or that it provided additional lubrication in the mouth to alleviate the perception of dryness [38,39,40]. Despite measuring up to 22% higher tannin concentrations in ACE with macerating enzymes treated wines as previously reported [22], panelists did not perceive increased astringency. This could be due to the release of RG-II, which may offset the astringency from higher tannins, and the naturally low tannin levels in Marquette grapes, making it challenging to detect treatment effects on astringency.
Despite these insightful findings, several limitations must be acknowledged. The sensory evaluation was conducted with a relatively small panel of eight trained panelists which may limit the generalizability of the results. Additionally, the experimental conditions were highly controlled, which might not fully represent the variability encountered in commercial winemaking settings. Future research should aim to include a larger and more diverse sensory panel and conduct experiments under scaled-up winemaking conditions to enhance the robustness and external validity of the outcomes. Furthermore, exploring the long-term stability of the aromatic and sensory profiles during wine aging (over one year) could provide a more comprehensive understanding of the lasting impacts of ACE and maceration enzymes.

4. Conclusions

This study evaluated the impact of Accentuated Cut Edges (ACE) and macerating enzymes on the aroma, color, and sensory attributes of Marquette red wines after nine months of aging. Applying ACE treatment at crushing produced Marquette red wines that were graded with highest intensity score in honey (1.6 times higher) and green apple notes (2.1 times higher) compared to the control wines. These results of the sensory evaluation suggest a nuanced enhancement in the pleasant aromatic profile. However, ACE treatment did not impact the color of red wines. When compared with ACE treatment, both macerating enzymes, PEC and RCE, enhanced the color intensity of Marquette red wines as evaluated by trained panelists, while spectrophotometry did not detect this trend, likely due to the distinct mechanisms of the methods between the human visual sensation and spectrophotometric measurement. Moreover, it seems the combination of ACE and enzymes treatments resulted in a decrease in fruity and sweet odor, as suggested by the result from both GC-MS measurement and descriptive analysis. Most importantly, no treatment had an impact on the intensity of astringency perception, which could be due to the low concentration and small molecular weight of condensed tannins present in Marquette red wines after nine months of aging.
Overall, while ACE treatment offers targeted sensory benefits, its influence on overall wine quality is limited when used independently. Its utility optimized in combination with macerating enzymes to achieve specific quality improvements in visual and sensory attributes, depending on winemaking objectives. Future research should explore these treatments under commercial winemaking conditions and investigate their long-term effects on wine aging to fully elucidate their impact on wine quality.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/fermentation10120624/s1, Table S1: Compositions of Pectinase Scottzyme® PEC5L and Rapidase® Clear Extreme; Table S2: Chemical characteristics of Marquette wines after aging 9 months. Data collected and reported in Part 1 of this study; Figure S1: Variety comparison between Pinot noir and Marquette.

Author Contributions

Conceptualization, A.A.W.; methodology, A.A.W. and Y.C.; software, A.A.W. and Y.C.; validation, A.A.W. and Y.C.; formal analysis, A.A.W. and Y.C.; investigation, A.A.W. and Y.C.; resources, A.A.W. and Y.C.; data curation, A.A.W. and Y.C.; writing—original draft preparation, Y.C.; writing—review and editing, A.A.W. and Y.C.; visualization, A.A.W. and Y.C.; supervision, A.A.W. All authors have read and agreed to the published version of the manuscript.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board (or Ethics Committee) of Iowa State University (IRB ID 22-128 and approval date: 5 October 2022) for studies involving humans.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study. Written informed consent has been obtained from the patient(s) to publish this paper.

Data Availability Statement

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

Acknowledgments

The authors would like to thank Brandon Carpenter, Nick Howell, and Olivia Meyer from the Iowa State University Horticulture Research Station for their assistance in vineyard management. We would like to thank Somchai Rice, former member of the Midwest Grape and Wine Industry Institute for her help with the use of the GC-MS; Terri Boylston from the department of Food Science and Human Nutrition for her advice on aroma compounds analysis and Ken Prusa on the sensory descriptive analysis evaluation set up. This work is a product of the Iowa Agriculture and Home Economics Experiment Station, Ames, Iowa, USA, project No. IOW05647, which is sponsored by State of Iowa funds.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relations that could have appeared to influence the work reported in this paper.

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Fermentation 10 00624 g001
Figure 1. Sensory analysis: the intensity of aroma attributes of Marquette red wines after nine months of aging. Different letters within the same attribute indicated statistically significant differences (p < 0.05) by two-way ANOVA (Treatment across Panelist) following Tukey’s test.
Figure 1. Sensory analysis: the intensity of aroma attributes of Marquette red wines after nine months of aging. Different letters within the same attribute indicated statistically significant differences (p < 0.05) by two-way ANOVA (Treatment across Panelist) following Tukey’s test.
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Figure 2. Sensory analysis: taste and mouthfeel attributes of Marquette red wines after nine months of aging.
Figure 2. Sensory analysis: taste and mouthfeel attributes of Marquette red wines after nine months of aging.
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Table 1. Preparation of sensory evaluation standards used during the training and evaluation sessions.
Table 1. Preparation of sensory evaluation standards used during the training and evaluation sessions.
Standard AttributesPreparation
Aroma (prepared in black wine glasses)
Grape jellyHy-Vee® Concord Grape Jelly—25 g
StrawberrySmucker’s® Jam Seedless Strawberry Jam—25 g
PlumSmucker’s® Jam Red Plum—25 g
Black cherryTillen Farms® Bada Bing cherries—2 pieces (cut-off)
BlackcurrantLe Nez Du Vin Mater aroma kit, Blackcurrant—2 drops dilute with 4 mL purified drinking water (Great Value®)
HoneyFischer’s® Clover Honey—25 g
Dry figGreat Value® Dried Figs—2 pieces (cut-off)
Candy fruitTrader Joe’s Dried Baby Sweet Pineapple—2 pieces (cut-off)
Green appleFreshly cut-off Granny Smith Apples
CiderRedd’s® Hard Apple Fruit Beer, 5% ABV—4 mL
GrassFreshly tall fescue collected from local lawn
FloralLe Nez Du Vin Mater aroma kit, Rose—2 drops dilute with 4 mL purified drinking water
WoodyHouse Blend French Oak Chips—5 pieces with 8 mL purified drinking water
RaisinGreat Value® Sun-dried Raisins—5 pieces (cut-off)
Alcohol13% v/v ethanol (diluted from Everclear® Grain Alcohol, 75.5% Alc/vol, 151 proof) in purified drinking water—30 mL
AcetoneOnyx Professional® 100% Acetone Nail Polish Remover (dilution factor = 5)
Taste (prepared in clear plastic portion cup)
SweetnessSucrose (C&H® pure cane sugar) in purified drinking water (40 g/L)
SournessTartaric acid (Presque Isle Wine Cellars®) in purified drinking water (1.5 g/L)
BitternessCaffeine (Sigma-Aldrich®, anhydrous, 99%) in purified drinking water (1 g/L)
SaltnessTable salt (Morton®) in purified drinking water (4 g/L)
Mouthfeel (prepared in clear plastic portion cup)
AstringencyAlum (Tone’s®) in purified drinking water (1 g/L)
Hotness13% v/v ethanol (diluted from Everclear® Grain Alcohol, 75.5% Alc/vol, 151 proof) in purified drinking water
ViscosityStarch (Great Value®, corn starch) in purified drinking water (boiled, 5 g/L)
TinglyLaCroix® Sparkling water, pure
Table 2. Response ratio (ratio of the compound peak area to the related internal standard peak area) of volatile aroma compounds from Marquette wine made after 9 months of aging.
Table 2. Response ratio (ratio of the compound peak area to the related internal standard peak area) of volatile aroma compounds from Marquette wine made after 9 months of aging.
CTLACEACE-PECACE-RCEp-Value
Ethyl esters
Ethyl acetate0.90 ± 0.091.10 ± 0.180.86 ± 0.050.97 ± 0.3ns
Ethyl butanoate0.06 ± 0.00 ab0.07 ± 0.01 a0.06 ± 0.00 b0.05 ± 0.01 b0.0206
Ethyl hexanoate0.52 ± 0.090.56 ± 0.110.41 ± 0.050.38 ± 0.02ns
Ethyl octanoate0.64 ± 0.370.67 ± 0.270.39 ± 0.100.43 ± 0.14ns
Ethyl decanoate0.08 ± 0.040.08 ± 0.020.07 ± 0.010.08 ± 0.04ns
Ethyl lactate0.12 ± 0.020.12 ± 0.020.14 ± 0.000.13 ± 0.03ns
Ethyl 2-methylpropanoate0.03 ± 0.00 ab0.03 ± 0.00 a0.03 ± 0.00 b0.02 ± 0.00 b0.0167
Ethyl 2-methylbutanoate0.01 ± 0.000.01 ± 0.000.01 ± 0.000.01 ± 0.00ns
Ethyl 3-methylbutanoate0.01 ± 0.00 ab0.01 ± 0.00 a0.01 ± 0.00 b0.01 ± 0.00 b0.0218
Acetate esters
Isoamyl acetate0.24 ± 0.020.25 ± 0.030.22 ± 0.040.19 ± 0.07ns
Isobutyl acetate0.01 ± 00.01 ± 00.01 ± 00.01 ± 0ns
Higher alcohols
Isobutanol0.25 ± 0.030.27 ± 0.040.29 ± 0.010.27 ± 0.06ns
Isoamyl alcohol2.52 ± 0.112.81 ± 0.312.72 ± 0.062.71 ± 0.47ns
2-phenylethanol0.43 ± 0.030.44 ± 0.070.42 ± 0.030.44 ± 0.05ns
1-hexanol0.09 ± 00.11 ± 0.010.1 ± 0.010.1 ± 0.01ns
1-butanoltrtrtrtr-
C13-Norisoprenoid
β-Damascenone0.01 ± 0.000.01 ± 0.000.00 ± 0.000.00 ± 0.00ns
Terpenes
Linalool0.01 ± 0.000.01 ± 0.000.01 ± 0.000.01 ± 0.00ns
p-cymene trtrtrtr-
β-citronellol trtrtrtr-
Values are mean ± standard deviation (n = 3). Different letters within the same aroma compound indicated statistically significant differences (p < 0.05) by one-way ANOVA following Tukey’s test. ns: not significant. tr: compound signal cannot be found in most samples.
Table 3. Color properties measured by instrumental (published in [22]) and sensory analysis.
Table 3. Color properties measured by instrumental (published in [22]) and sensory analysis.
TreatmentInstrumental Measurement (Published in [22])Sensory Analysis
HueColor IntensityHueColor Intensity
CTL0.6 ± 0.011.3 ± 0.11.9 ± 2.92.8 ± 2.0 B
ACE0.6 ± 0.011.4 ± 0.42.4 ± 3.73.0 ± 2.8 B
ACE-PEC0.6 ± 0.012.4 ± 0.63.0 ± 4.74.8 ± 3.5 A
ACE-RCE0.6 ± 0.011.3 ± 0.62.5 ± 3.84.8 ± 3.1 A
p-value
Treatment0.76130.06120.13380.0009
Panelist--<0.0001<0.0001
Hue (instrumental measurement): calculated as the ratio of the absorbance value at 420 nm to that at 520 nm. Different letters within the same parameter indicated statistically significant differences (p < 0.05) by one-way ANOVA following Tukey’s test.
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Cheng, Y.; Watrelot, A.A. Synergetic Effect of Accentuated Cut Edges (ACE) and Macerating Enzymes on Aroma and Sensory Profiles of Marquette Red Wine. Fermentation 2024, 10, 624. https://doi.org/10.3390/fermentation10120624

AMA Style

Cheng Y, Watrelot AA. Synergetic Effect of Accentuated Cut Edges (ACE) and Macerating Enzymes on Aroma and Sensory Profiles of Marquette Red Wine. Fermentation. 2024; 10(12):624. https://doi.org/10.3390/fermentation10120624

Chicago/Turabian Style

Cheng, Yiliang, and Aude A. Watrelot. 2024. "Synergetic Effect of Accentuated Cut Edges (ACE) and Macerating Enzymes on Aroma and Sensory Profiles of Marquette Red Wine" Fermentation 10, no. 12: 624. https://doi.org/10.3390/fermentation10120624

APA Style

Cheng, Y., & Watrelot, A. A. (2024). Synergetic Effect of Accentuated Cut Edges (ACE) and Macerating Enzymes on Aroma and Sensory Profiles of Marquette Red Wine. Fermentation, 10(12), 624. https://doi.org/10.3390/fermentation10120624

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