Fresh-cut apple
Cider
a Genus unspecified.
In 2015, Graça et al. detected principally mesophilic and psychrotrophic microorganisms on fresh cut apple while coliforms and LAB were isolated on apple flowers [ 24 ]. Focusing on cider apples, Alonso et al. used PCR-DGGE to study the native microbiota of five apple varieties commonly used in the Asturian cider-making process. Predictably, Enterobacteriaceae were present due to the ubiquity in nature of this genus, but bacterial species usually associated with spontaneous fermentation were not [ 27 ]. The apple surface microbiota may not be a determinant in the fermentation process. The microbiota of apple cider is strongly influenced by other factors such as harvest techniques, quality sorting and storage. In 2004, Keller et al. brought to light the influence of picking techniques on the microbiota [ 42 ]. Cider apples picked from the ground after their fall bring more bacterial diversity than those tree harvested. After grinding, no difference between bacteria counts were found, whether they were stored or not. However, significant differences in bacterial counts between apple varieties were identified.
Bacterial starters do not exist yet in cider; thus, Sanchez et al. investigated LAB prevalence during the malolactic fermentation in Asturian cider cellars in order to find the most efficient fermentative strains [ 33 ]. They mostly isolated strains of Lactobacillus brevis and Oenococcus oeni. This last species is already known to be very tolerant to low pH and to the presence of alcohol [ 38 ]. According to a fermentation capacity evaluation of the selected strains, O. oeni strains were the most efficient. Salih et al. also highlighted the importance of O. oeni during the malolactic fermentation, and the presence of Lactobacillus brevis in some of the ciders tested [ 37 ]. Different behaviors of the LAB flora depend on the kind of apples used for cider-making (sweet cider apples, sweet dessert apples, bitter cider apples). The influence of the geographical origins of the indigenous cider LAB was determined by Sanchez et al. using the RAPD (Random Amplification of polymorphic DNA) technique on O. oeni strains. Five distinct groups, specific to only one producing area, were identified and had an identical RAPD profile. This significant result brought to light the link between O. oeni strains and their geographical origin [ 33 ]. A recent study focusing on the biogeography of O. oeni confirmed the importance of genetic adaptation of this species in cider and also highlighted that O. oeni from wine or from cider were genetically different [ 38 ]. The first genome of O. oeni has been sequenced and annotated in 2005 [ 43 ]. Many studies have investigated the genome of this bacterium and have shown that O. oeni strains from wine or cider present a different genomic content [ 44 , 45 , 46 ]. A recent study of Sternes et al. analyzed the pan-genome of O. oeni with 191 strains, of which only four have been isolated from cider [ 46 ]. They showed again that three out of four of the cider isolates cluster closely together. The presence of neighboring wine-derived strains suggests that information from additional strains isolated from cider is required before any conclusion regarding the possibility of a cider-specific subset of O. oeni can be reached. The other source of genomic data from LAB isolated from cider is related to their technological or probiotic potential [ 47 , 48 ].
Lactobacillus sp. and Oenococcus sp. are the most common LAB identified in apple juice byproducts. In apple cider vinegar, which is the result of acetic fermentation, both of them were detected, even if acetic acid bacteria, such as Acetobacter sp., Komagataeibacter sp. or Gluconobacter sp., were the most abundant [ 17 ]. In 2010, Sanchez et al. studied the LAB diversity during malolactic fermentation in an industrial cider [ 13 ]. Using molecular tools, such as 16S rRNA gene sequencing, Lactobacillus collinoides , O. oeni , Pediococcus parvulus and, with minor content, bacteria like L. casei or P. ethanolidurans were identified. Acetic acid bacteria are necessary for vinegar production, but can ruin cider production. In contrast, LAB are essential in malolactic conversion during cider production, but some can damage the product by producing spoilage compounds.
Variations in the microbial ecosystem of ciders are associated with several factors, from the orchards to the final product. First, microbial diversity is determined by the growing conditions of the fruits such as the apple varieties, the climate and the production process. The cultivation practices have an impact on the fruit microbial composition in terms of abundance and diversity. Organic and conventional apple bacterial communities were shown to be significantly different [ 49 , 50 ]. The organic apple phyllosphere displayed higher numbers of bacteria than the conventional apple phyllosphere. A comparison of integrated and organic growing systems for Golden Delicious apple production also revealed significantly higher frequencies of filamentous fungi, greater abundance of total fungi and of taxon diversity in organic apples than in integrated apples [ 51 ]. The crop management methods thus influence the microbial communities associated with the surface of apple fruits used for cider production. The apple variety also has an influence on the microbial composition of the fruits. Keller et al. showed that significant differences exist in total aerobic bacterial and fungal populations among apple varieties in relation to their pH, Brix and titratable acidity [ 42 ]. The apple varieties with the lowest titratable acidity, highest pH and highest Brix have the highest microbial concentrations (≥2.5 log CFU/g). The method of harvesting also plays a role in microbial diversity. Microbial populations on apples, in pomace and in cider are higher when apples are harvested off the ground rather than tree-picked. In the final cider, the average aerobic plate counts for all pooled varieties tested in the ground-harvested group was 4.89 log CFU/g compared with 2.88 log CFU/g for the fresh tree-picked group [ 42 ].
After fruit harvesting, the cider process modulates the microbial composition of ciders. The culling of apples result in ciders with higher microbial numbers than those made from unculled apples [ 42 ]. A strong link exists between the temperature profile of the cider fermentations and the yeast population dynamics of the predominant yeast species, present within the fermentations [ 28 ]. Another piece of research also showed that the musts obtained by pneumatic pressing were dominated by non- Saccharomyces yeasts ( Hanseniaspora genus and Metschnikowia pulcherrima ), whereas in the apple juices obtained by traditional pressing, Saccharomyces together with non- Saccharomyces were always present [ 30 ].
Cider processing facilities and cellars walls, floors and surfaces also constitute reservoirs of bacteria and fungi throughout the cider process. For example, one source of S. cerevisiae yeasts appears to be the process utensils, the press house and the vat-house, in which this resident flora can be found even six months after the last pressing [ 28 ].
Even if microbial reservoirs are broad, the microbial diversity and microflora successions also greatly depend on the aptitudes of the bacterial and fungal strains to resist or adapt to the process conditions such as depletion in oxygen levels, sulfites presence, CO 2 and alcohol productions and essential nutrients’ availability. It also depends on the differences in their specific growth rates, in their sugar uptake capabilities, on inter-specific competition, cell death, flocculation and/or natural sedimentation characteristics [ 52 ].
3.1. yeast contribution.
During alcoholic fermentation, many byproducts such as esters, higher alcohols and phenolic compounds are produced as secondary metabolites. Esters provide mainly fruity and floral notes; higher alcohols provide ‘background flavors’; whereas the phenolic compounds can generate interesting or unpleasant aromatic notes. Esters are the main volatile compounds in cider behind ethanol [ 53 ]. They are characterized by a high presence of ethyl acetate, which alone can represent up to 90% of the total esters [ 54 , 55 ]. The amount of acetates produced by yeasts seems to be strongly related to the nature of the strains leading to alcoholic fermentation: Saccharomyces sp. produce fewer acetate amounts than non- Saccharomyces yeasts. Comparing the potential of H. valbyensis and S. cerevisiae to produce volatile compounds, Xu et al. [ 55 ] showed that H. valbyensis yielded higher concentrations of ethyl acetate and 2-phenylethyl acetate, while S. cerevisiae kept more free (non-esterified) isoamyl alcohol and isobutanol. A small variation in the ester concentration of ciders may have significant consequences on their final sensory quality [ 56 ]. Most of the esters are responsible for the fruity characteristics of ciders. However, an excessive amount of ethyl acetate may lead to an unpleasant smell of solvent.
Higher alcohols are directly derived from the metabolism of yeasts. They are synthesized during fermentation from oxo-acids originating in amino acids and sugar metabolism [ 57 ]. In ciders, they are mostly represented by isopentanols (2- and 3-methylbutanol) followed by isobutanol, propanol, butanol or hexanol [ 58 ]. Although they constitute a relatively low amount of the total substances, higher alcohols may greatly influence sensory characteristics. Rapp and Mandery [ 59 ] found the total higher alcohols in wine to be in the range 80 ± 540 mg/mL ; concentrations up to 300 mg/L contribute to pleasant flavor, but concentrations above 400 mg/mL provoke unpleasant flavor and harsh taste. Some higher alcohols, particularly iso-amyl alcohol, contribute to unpleasant flavor [ 60 ], although a positive correlation has been reported between n-butanol and the aroma quality of apple juice [ 61 ].
The third class of secondary products, i.e., the phenolic compounds, also have important effects on the sensory properties of apple ciders by either their content or their profile. These compounds derived from raw material have an impact mainly on color, bitterness, and astringency [ 62 ]. High molecular weight procyanidins in ciders are known to contribute to astringency, whereas the smaller compounds contribute to bitter taste [ 63 , 64 , 65 ]. Simultaneously, they influence the sweetness and sourness, thus further highlighting their importance in overall flavor development [ 64 ]. In addition to the non-volatile phenolic compounds, the volatile phenolics mainly formed by enzymatic decarboxylation during fermentation contribute to aroma [ 66 ].
It has been reported that during the early stages of fermentation, excess growth of the apiculated yeast Kloeckera can generate high levels of esters and volatile acids [ 67 ]. In wine, the aromatic profile is negatively influenced by the yeast Brettanomyces / Dekkera and is characterized by mousy, medicinal, wet wool, burnt plastic or horse sweat smells [ 68 ]. Buron et al. have shown that Brettanomyces / Dekkera cider strains were able to produce 4-ethylcatechol, 4-ethylphenol and 4-ethylguaiacol from caffeic, p -coumaric and ferulic acids, respectively [ 69 ]. These volatile phenols are associated with organoleptic defects. In contrast, in some beers, this yeast is considered essential and beneficial [ 70 ]. In wine- and cider-making on an industrial scale, the control of Brettanomyces / Dekkera is usually achieved through the addition of sulfur dioxide (SO 2 ) to the fermentation medium [ 71 ]. In cider-making, the concentration of SO 2 is in the range of 50–150 mg/mL at pH 3.0–3.8, not exceeding 200 mg/mL in total [ 72 ]. However, some strains of Brettanomyces / Dekkera are naturally resistant to SO 2 , and elimination of this yeast by physical treatments (filtration) has a limited efficiency (due to the cell size of this yeast) and does not prevent subsequent recontamination.
Transformation of malic acid, lowering total acidity, is the major organoleptic change induced by LAB. During MLF, the strong green taste of malic acid is replaced by the less aggressive taste of lactic acid [ 73 ]. However, LAB are also responsible for other changes in aromas increasing flavor complexity, involving changes of fruity, flowery and nutty flavors, as well as the reduction of vegetative/herbaceous aromas by reduction of acetaldehyde metabolism [ 74 , 75 , 76 ].
Lactobacillus , Leuconostoc , Oenococcus and Pediococcus are genera of special interest as they are able to survive cider environments (low pH, high ethanol content and low nutrients). Research focuses on the contribution of O. oeni , but other genera, particularly Lactobacillus species, should not be underestimated [ 77 ]. In wine, it is well known that some varietal aromas revealed during alcoholic fermentation by yeast disappear or change after malolactic fermentation [ 73 ]. For example, the concentration of some esters can be either increased or decreased by MLF, according to the type of bacterial strain used [ 78 ]. Apart from esters, aroma compounds such as higher alcohols, fatty acids, lactones and sulfur and nitrogen compounds can be produced by LAB [ 77 ].
LAB contribution to aromatic profiles of ciders has been explored less than it has been in wine. A few studies are available, principally linked on the use of O. oeni strains as starters rather than studying LAB metabolism in the cider environment. In wine, LAB contribution is focused on citric acid metabolism that induces the production of compounds linked to buttery descriptors: diacetyl, 2,3-butanediol and acetoin [ 79 ]. Together with acetonic compounds, citric acid degradation involves the production of acetic acid that can significantly modify the aromatic profile. Citric acid metabolism with the production of diacetyl cannot be responsible for the whole panel of flavor modifications, and the mechanisms should be further studied.
Along with the favorable sensory changes that can occur during cider elaboration, LAB can be also responsible for undesirable reactions. The frequent cider alteration known as ‘piqûre acroléique’ is mainly caused by a heterofermentative LAB commonly encountered in cider, Lactobacillus collinoides [ 80 , 81 ]. In apple-derived products, this alteration results from glycerol degradation to 3-hydroxypropionaldehyde (3-HPA) under the action of L. collinoides via the diol-dehydratase enzyme. In addition to L. collinoides , some other cider species, like L. hilgardii [ 34 ] or L. diolivorans [ 82 ], are able to produce 3-HPA. Glycerol is one of the major products of yeasts metabolism during cider alcoholic fermentation and is important for the sensorial quality of fermented beverages. Due to its high instability, during the distillation process, the 3-HPA is transformed by dehydration [ 83 ] in acrolein, a lachrymatory chemical generating a peppery flavor, which can spoil the product, giving a bitter taste [ 84 , 85 ].
One major spoilage microorganism is the Gram-negative, facultative anaerobic bacterium Zymomonas mobilis isolated from various alcoholic beverages, including ciders, beers and perries. Z. mobilis is a remarkable bacterium and a very promising microorganism for industrial ethanol production because its catabolism follows the Entner–Doudoroff pathway, thus giving a near-theoretical yield of ethanol from glucose, fructose and sucrose, the only carbon and energy sources that support its growth [ 40 ]. As a cider spoilage microorganism, growth of Z. mobilis is correlated with the production of large quantities of acetaldehyde along with an almost explosive production of gas and a marked turbidity of the product, an alteration known as ‘framboisé’ in French ciders or ‘cider-sickness’ in English ciders [ 41 , 86 ]. Associated with these symptoms is a marked change in the flavor of the beverage, the original fruity character being lost or hidden by a strong and characteristic taste, reminiscent of raspberry. Malolactic fermentation (MLF) is considered to enhance the risk of ‘framboisé’, and Bauduin et al. [ 41 ] have shown that the relationship between MLF and ‘framboisé’ is mainly associated with the increase of pH correlated with the conversion of malic acid to lactic acid rather than with nutritional factors produced by LAB. In fact, the amount of residual nitrogen in cider appears to be the main factor controlling the growth of Z. mobilis , and thus, a solution for the prevention of this alteration consists of reducing the amount of residual nitrogen as soon as possible [ 41 ].
Therefore, a greater knowledge of cider LAB flora and their metabolisms in a cider environment could provide laboratory and practical cellar tools for a better control of cider quality.
Fermented foods and beverages are known to be safer than unfermented counterparts. The improved food safety arising from fermentation is largely due to LAB, a predominant group of organisms in most fermented foods and beverages. Occasionally, bacterial pathogens such as Salmonella spp., Escherichia coli and Staphylococcus aureus , originating from orchard soil, farm and processing equipment or human sources, may occur in apple juice. However, both apple juice and fermented cider contain organic acids, mainly malic acid (≅5 g/L) in apple juice and lactic acid (3–4 g/L) in fermented cider, generating acidity (pH level ranging from 3.0–3.5 and 3.3–4.0, respectively) that usually prevents the growth of these pathogens, which can survive for only a few hours. The growth and metabolism of LAB usually inhibit the growth of normal spoilage flora of the matrix and of any bacterial pathogens that it may contain. Therefore, apple cider is traditionally not regarded as a potentially hazardous food [ 87 ]. However, the monitoring of food-borne hazards in cider such as the pathogenic bacteria E. coli , protozoan Cryptosporidium , biogenic amines or mycotoxins still requires vigilance on the part of cider producers.
Biogenic amines (BA) are low molecular weight organic bases with an aliphatic, aromatic or heterocyclic structure frequently occurring in foods and beverages involving fermentation or the ripening process. The formation of these molecules is achieved through the removal of the alpha carboxyl group from amino acids [ 88 ]. The most abundant BA found in foods are histamine, tyramine, putrescine, cadaverine and phenyl ethylamine. In fermented beverages, such as beer, wine and cider, production is influenced by microorganisms present [ 88 , 89 ], environmental factors such as pH, ethanol [ 90 , 91 ], sulfur anhydride level [ 92 ], raw material quality and fermentation, as well as technological conditions [ 90 , 93 ]. Consumption of food containing high level of BAs can induce adverse reactions such as headache, hyper- or hypo-tension and rashes. Such disorders may become serious especially for consumers whose detoxification system is impaired either by genetic disorders or medical treatments [ 89 ]. Histamine and tyramine are considered as most toxic and particularly relevant for food safety, while putrescine and cadaverine are known to potentiate these effects [ 94 ].
In cider, as microbiological stabilization is not performed after MLF, indigenous heterofermentative LAB constitute the predominant flora capable of promoting the production of BAs [ 36 , 39 , 95 ]. As shown in Table 2 , among LAB, Oenococcus and Lactobacillus were found to be the most representative genera of BA producers in cider.
Potential bacterial species producers of biogenic amines in Spanish and French ciders.
Biogenic Amine | Producer | References |
---|---|---|
Histamine | [ , , ] | |
Putrescine | [ , ] | |
Tyramine | sp. | [ , , ] |
Studies conducted on commercial cider from Spain and France revealed the presence of BA in almost 90% of the analyzed products with a higher prevalence of tyramine, histamine, putrescine and cadaverine among other amines [ 89 , 95 ]. Nevertheless, BA content of cider seems to be lower than that detected in other fermented foods and beverages [ 88 ]. Some differences in amount and composition were also found between French and Spanish samples. More precisely, cadaverine and putrescine were detected at a maximal concentration of 34 mg/L in 20% and 57% of Spanish cider samples, respectively, while only in trace amounts in only a third of French cider samples (1 mg/L). Tyramine was the most frequently detected BA in French samples (present in 70% of samples in concentrations below 14 mg/L). Histamine was detected at relatively low levels in both French and Spanish samples (26% of total samples, below 16 mg/L) [ 89 , 95 , 96 ]. As mentioned by Ladero et al., the characteristics of the apple variety used and/or the different elaboration processes, as well as possible microbiota differences could explain the differences [ 89 ]. The global amount and profile of BA produced do not appear to be driven by cider-making steps and types of press [ 95 ]. Therefore, some strategies have been proposed to decrease the formation of BA, such as (a) reducing amino acid precursor levels (generally decreasing with fruit ripening), (b) limiting the growth of spoilage bacteria, (c) inoculating starter cultures without amino acid decarboxylase and (d) inoculating biogenic amine-degrading microorganisms [ 94 , 97 ].
Mycotoxins are secondary metabolites of filamentous fungi mainly triggered by Aspergillus , Fusarium and Penicillium genera [ 98 ]. In apple and apple-derived products, patulin represents the most relevant mycotoxin. The toxin is an unsaturated heterocyclic lactone toxin produced by a wide range of mold species [ 99 ]. Among these species, P. expansum, as the main pre-harvest and post-harvest contaminant in pomaceous fruits (apples and pears), is considered as the major source of patulin in these fruits [ 100 ]. The level in food and beverages is regulated in Europe by the European Commission and in the United States by the U.S. Food and Drug Administration (FDA) to a maximum acceptable concentration of 50 µg/L for fruit juices and derived products (including cider) [ 101 ]. Indeed, Michigan apple cider mills were analyzed for patulin concentration. The mycotoxin was detected in almost 20% of cider mill samples with 2% of samples having concentration higher than 50 µg/L [ 102 ]. Temperature, activity of water (a w ) and pH were found to influence P. expansum growth, as well as patulin production. The fungi is able to produce the toxin around 16 °C. P. expansum can produce the mycotoxin only at an a w of 0.99, which is the approximate a w of fresh fruits. Finally, patulin production was found to be optimum at pH 4 [ 103 ]. Apple contains natural acids (citric and malic acids) that lead to the reaching of these optimal conditions (pH of fruit varies from <2.5–5) [ 104 ]. It is commonly admitted that the toxin is generally unstable during fermentation, so that products such as cider are usually free of patulin. In a recent study, the level of patulin in contaminated musts was shown to have decreased six-fold after two days of fermentation [ 105 ]. Reports of patulin in cider are likely due to the adjunction of apple juice to produce ‘sweet cider’ or low-fermented cider [ 102 ].
As previously mentioned, unpasteurized apple cider is historically considered to be a safe product, free of microbial pathogens due to its acidic level and to the fermentation process. However, some bacterial and parasitic pathogens can survive and may remain infectious [ 106 ]. To date, enterohemorrhagic E. coli (EHEC) serotype O157:H7, as well as the protozoan Cryptosporidium parvum have been linked to several outbreaks since the 1980s due to apple cider consumption [ 106 ]. Nevertheless, it is important to notice that such outbreaks only occurred in North America and mainly in unfermented apple ciders [ 106 ]. European apple cider has never been implicated in any outbreaks of this kind due to alcoholic fermentation process byproduct, ethanol, which is toxic for most potential pathogens in cider [ 107 ]. EHEC O157:H7 is known to have a fecal origin and may contaminate apples, juice and cider directly from animal/human feces or by indirect contact (equipment, contaminated water, etc.) [ 108 ]. Cryptosporidium spp. is an intracellular parasite with an infectious stage known as oocysts. Oral transmission of the parasite is facilitated by the ability of oocysts to survive for weeks to months in the environment. The study of contamination sources in unpasteurized apple cider revealed that the parasite is found in washed apples, water, fresh and finished cider [ 108 ]. Kniel et al. studied the potential of malic acid, as well as hydrogen peroxide to reduce the infectivity of C. parvum in apple cider. Interestingly, infectivity was completely inhibited by incubation of oocysts in apple cider plus 0.025% H 2 O 2 and inhibited (up to 88%) by the addition of 5% malic acid [ 109 ].
5.1. control of the microbial ecosystem to improve or modulate cider quality, 5.1.1. rational design of starter cultures.
The selection of appropriate starter strains is key in the control of the cider fermentation process and characteristics of the final beverage. Microbial starters, especially O. oeni , are less used in cider production than in wine production, but their role might be crucial for the quality of the final product [ 110 ]. This leads to many studies focusing on the selection of microbial starters [ 33 , 111 ], their improvement [ 112 , 113 ] and the use of other LAB than O. oeni [ 114 ]. The use of isolated strains of S. cerevisiae is an interesting strategy for maintaining the quality and reproducibility of fermented beverages. This is especially true for the Champenoise method, typical of Asturian PDO ciders, and based on a secondary fermentation in bottle. The screening and the selection of local yeast strains is believed to be more effective than using commercial starters, as these endemic strains are potentially better acclimated to the environmental conditions than industrial starters [ 115 ]. These authors thus proposed a methodology for the rapid screening and selection of autochthonous yeast strains based on their oenological and technological properties. The ciders obtained with the selected yeast strains were scored as good after sensory analysis. The choice in species driving the fermentation is important for technological purposes and also for the aroma profile development in cider. For example, the presence of Hanseniaspora sp. yeast strains during apple fermentation results in the production of considerable amounts of esters and alcohols, contributing to fruity sensory notes, compared with apple musts fermented only with Saccharomyces sp. yeasts, which provide rather neutral sensory notes [ 116 ]. The fermentation performance has also been improved by the use of a hybrid strain between S. eubayanus and S. cerevisiae [ 111 ]. Recently, in order to control the proliferation of Brettanomyces / Dekkera in wine, Ngwekazi et al. [ 71 ] have identified and characterized killer toxins secreted by non- Saccharomyces yeasts related to wine. Their results, although preliminary, show that killer toxins have a high potential to control the population of large numbers of Brettanomyces / Dekkera strains. These results are especially encouraging, as none of the killer toxins characterized inhibit the fermentative yeast Saccharomyces .
Another characteristic to be considered for the bacterial strains used in the cider fermentation process is their aptitude in resisting bacteriophages (phages). The presence of lytic or lysogenic phages of Oenococcus has previously been described in wine [ 117 ]. Recently, Constanti et al. characterized O. oeni bacteriophages and the related implications for malolactic fermentation in wine [ 118 ]. They reported that pH and ethanol affect the lytic activity of Oenococcus phages, especially when wine alcohol content is low. The presence of phages in cider has not yet been investigated. It is thus a point of interest that should be examined, as anti- Oenococcus phages could be at the origin of cider fermentation problems by disturbing the malolactic fermentation driven by phage-sensitive Oenococcus strains. Still, phages could be used as antimicrobial agents against spoilage and pathogenic bacteria in ciders and therefore help in controlling the safety and quality of these fermented beverages. Phage therapy in the food industry has been extensively studied [ 119 ]. However, phage applications to apple fermented beverages are scarce. One main obstacle to their efficient antimicrobial action would be their potential sensitivity to acidity found in apple products [ 120 ].
Spoilage and pathogenic flora in apple juice and by extension in apple fermented beverage can be reduced by physical methods, which have already been reviewed [ 121 ] and will not be further discussed. The control of the fermentation process parameters such as the time of inoculation of mixed cultures, the temperature of fermentation steps in the process or prefermentative steps is a key element in the modulation of the cider ecosystems throughout processing and thus of the quality of the final product. Aroma production during cider fermentation is greatly dependent on the yeast species in the presence and their sequential succession throughout the process. A study of the co-culture of Wickerhamomyces anomalus and S. cerevisiae showed that the association could help improve the quality and add complexity to the cider [ 122 ]. Controlling the strain association parameters during the fermentation process, i.e., the inoculation time and the sequential or simultaneous mixed cultures, is crucial for the optimization of the desired kind of cider. In the same way, the fermentation of a vegetable juice using a mixed culture of S. cerevisiae and L. plantarum resulting in an enhancement of the nutritional content of the final beverage [ 123 ] emphasizes the feasibility of the chosen co-fermentation by the selection of the right microbial associations for designing new functional apple fermented beverages.
Yeast metabolism is greatly dependent on the temperatures applied during the fermentation process. Peng et al. [ 124 ] have shown that variations of the fermentation temperature have a direct influence on the aromatic profile of the final cider. In their study, the ciders fermented at 20 °C seemed to result in the best acceptance by the consumer and displayed the highest aromatic characteristics. This is probably due to modifications in the microbial metabolism that result in variations in the production of esters, volatile compounds and alcohols according to the fermentation temperatures. Variations in the fermentation temperature are nonetheless to be considered with care, as the increase of temperature can also lead to the formation of undesired compounds by the expression of unsuitable microbial metabolic pathways [ 124 , 125 ]. In the same way, fruit processing, pectinolytic enzyme application, cell yeast immobilization on alginate and the type of fermentation have all a significant influence on the antioxidant capacity, polyphenol profile and volatile composition of ciders [ 126 ]. Prefermentative treatments such as pulp fermentation induced the formation of higher amounts of ethanol, procyanidins B2 and C1, epicatechin and catechin and resulted in a higher antioxidant activity than in non-pulp fermented ciders. Cell immobilization positively affected the ethanol content, but decreased the antioxidant activity of ciders. Ciders obtained with spontaneous fermentation contained more esters and methanol compared to inoculated ciders [ 126 ]. The MLF is also a bottle-neck in the cider production process, and one area of research is looking for strategies to control/improve this natural phenomenon [ 127 ]. Such process parameters can thus be used as levers to modulate the quality of the final product.
Microbial quality is obviously microorganism dependent and is highly affected by chemical, physical and biological factors pertaining to the environment. Maintaining microbiological quality and the maximum sensory and nutritional quality of fermented beverages requires a combination of antimicrobial hurdles in order to limit the growth of undesired microorganisms. By producing organic acids as a fermentation metabolite, antimicrobial peptides and hydrogen peroxide, LAB strains may contribute to improving the quality of apple ciders. Bacteriocins are generated from bacteria and, usually, are inhibitory towards phylogenetically-related species. There are only a few reports about the inhibitory activity of bacteriocins against yeasts [ 128 , 129 , 130 ]. To our knowledge, the effectiveness of bacteriocins from LAB for controlling the growth of undesirable yeasts in cider or wine has never been studied, although bacteriocins produced by LAB have received considerable attention over the years for their possible use as biopreservatives in food, to reduce the use of chemical preservatives. It could therefore be interesting to screen new bacteriocins from LAB isolated from fermented beverages.
Bacteriocins could also be effective against spoilage bacteria. L. collinoides exhibits natural resistance to conditions encountered during the fermentative process [ 131 ]. In order to avoid this alteration, the bacteriocin enterocin AS-48, a broad-spectrum antimicrobial peptide produced by Enterococcus faecalis [ 132 ], was tested against two 3-HPA-producing L. collinoides strains causing apple cider spoilage. The two L. collinoides strains tested were rapidly inactivated by low concentrations of enterocin AS-48 in fresh apple juice (2.5 µg/mL) and also in Basque cider (2.5–5 µg/mL) [ 133 ]. Another classical disorder, which does not affect flavor, is known as ‘ropiness’. This microbiological problem arises when certain bacteria synthesize exopolysaccharides (EPS), thus increasing the viscosity of the cider [ 134 ]. The EPS show a large variation in composition, molecular mass and structure and, once secreted into the medium, play an important role in the rheology and texture of fermented beverages, enhancing naturally the texture and viscosity [ 135 ]. As a consequence of the increase of viscosity, the cider flows like oil; hence the term ‘ropiness’. In addition to being a biothickener, prebiotic effects of several EPS have been demonstrated [ 136 ]; however, despite these interesting properties, a high level of EPS production in cider is unwanted, as it is prejudicial to the organoleptic quality of the product. Although ropiness is mainly caused by some strains of LAB [ 137 , 138 , 139 ], it has been shown that one strain belonging to the Bacillus genus can be responsible for this alteration [ 140 ]. Among the alternative methods suggested to avoid this alteration in beverages, Grande et al. [ 141 ] have tested the efficacy of the E. faecalis enterocin AS-48 against a slime-producing B. licheniformis strain in apple cider. Their results show that enterocin AS-48 is also active against the EPS-producing strain either in culture medium or in apple cider, suggesting a possible use of this enterocin to prevent ropiness. These results are of great interest for the development of tools allowing for the control of undesired bacteria in fermented apple cider.
Thanks to amino oxidase enzymatic activity, some species of LAB appear to be of great interest for the potential control of BA-related health risk. Hitherto, many studies have been conducted with the purpose to identify LAB isolated from fermented foods with BA degrading capability, but only a few concern fermented beverages. To our knowledge, no study has been conducted on LAB isolated from cider. A collection of 85 LAB isolated from wines, must and lees was screened for their ability to degrade histamine, tyramine and/or putrescine. Twenty-five percent of the LAB were able to degrade histamine, 18% tyramine and 18% putrescine. The strains with highest activity belonged to Lactobacillus and Pediococcus groups, and most of them were able to degrade simultaneously at least two BAs [ 108 ]. In the future, it might be of interest to screen the potential of cider-associated LAB to reduce potential BA level in this beverage.
Large numbers of studies attribute antifungal activity to LAB strains thanks to the production of various organic acids (such as lactic, acetic, caproic, formic, propionic, phenyl lactic and butyric), fatty acids and peptides [ 142 , 143 ]. LAB may represent interesting biological control agents in apple fermented beverages by means other than bacteriocin. The detoxification of patulin through binding to bacterial surface proteins is an example [ 144 , 145 ]. Recently, Zoghi et al. identified two probiotic strains of L. acidophilus and L. plantarum able to catch the toxin through their surface layer proteins (fructooligosaccharide content). In the best conditions and after six weeks of refrigerated storage, more than 90% of initial patulin were removed from apple juice with no significant difference in organoleptic properties [ 144 ].
Fermented beverages and especially non-dairy probiotic beverages are believed to be the next functional foods for probiotic delivery. Likely candidates are chilled fruit juices or fermented vegetable juices [ 146 ]. For the consumer, they present the advantages of lacking dairy allergens such as lactose, containing low cholesterol and having a vegan-friendly status [ 147 ]. The health benefits of fermented beverages have been described. The improvement of gastrointestinal health associated with the microbial content of fermented beverage is thought to be responsible for perceived health outcomes. Evidence of the direct or indirect action of the beverage microbiota on gastrointestinal health have been given over the years, even if the mechanisms involved are still unclear for the most part [ 148 ]. The health benefits of apple beverages have been the subject of much scrutiny, for many years. For example, apple beverages, including cider, have been shown to have anti-viral properties [ 149 ]. Some apple juices are already used as vectors of probiotic lactobacilli strains [ 150 , 151 ]. Several traditional cereal and vegetal fermented beverages are the source of probiotic bacteria [ 152 ]. Apple fermented beverages can therefore be sources and vectors of probiotics. Spent cider yeast, a by-product of the fermentation process, was used as a dietary supplementation in a piglet model. This supplementation proved to enhance gut functions and to reduce Salmonella and Escherichia carriage in porcine gut [ 153 ]. Some probiotic potential has also been demonstrated for lactobacilli [ 48 ] or pediococci [ 47 , 154 ]. A probiotic beverage from apple fermented with L. casei has recently been developed for human consumption [ 151 ].
A recent review detailed the role of LAB as an efficient cell factory for the production of functional biomolecules and food ingredients to enhance the quality of cereal-based beverages [ 155 ]. These LAB assets could be transposed to apple fermented beverages. They encompass the LAB-mediated inhibition of spoilage or pathogenic microorganisms through antibacterial compound production, the reduction of potential antinutritive factors, the amelioration of the apple fermented beverage nutritional value, the LAB aroma and flavor compound production, the production of EPS related to texture development, organoleptic changes and the prebiotic nature of those beverages, the production of nutraceutical compounds and anti-allergenic biomolecules. Some LAB, isolated from wine or cider, also showed potential intrinsic (without grape/apple matrix) health benefits [ 156 ]. For example, O. oeni can harbor anti-inflammatory potential [ 157 ] or produce EPS [ 158 ]. This EPS production could even help with the industrial production of food products containing lyophilized O. oeni strains [ 158 ]. The EPS production by LAB could also be related to industrial perspectives such as viscosity and mouth feel enhancement properties [ 159 ].
The development of functional apple fermented beverages is promising. For example, strategies combining apple juice and a novel whey-based beverage fermented by kefir grains have already been designed [ 160 ]. The combination of apple juice and kefir grains resulted in a beverage with high total phenolic content and antioxidant activity.
This review emphasized the microbial ecosystem of musts and showed how mastering the quality and the safety of cider production is reliant on a better understanding of the mechanisms of LAB and yeast metabolism involved in the transformation of precursors into potent flavor components. The present review further paved the way for the optimization of the industrial scale-up for artisanal cider production using the integrated metabolomics and molecular phylogeny approaches to identify and select strains of LAB, particularly O. oeni , to improve the flavor/aroma profiles of ciders. Indeed, although considerable efforts have been made in recent decades to optimize and improve the production of cider, cider remains a product with a great variability related in particular to the notion of ‘terroir’ that can be defined as a homogeneous territory from a soil and climate point of view. Therefore, pedoclimate factors together with indigenous microorganisms may significantly influence the quality and typicity of the cider produced in a specific location. The apple benefits from a good and healthy image that could be combined with new microbial characteristics with a special focus on LAB. Specific research on microbiomes using ‘omics’ tools will give rapid insights into the potential of strains associated with these products. For these reasons, studies on apple fermentation beverages comprise a promising field of research with great potential for available new, healthy and pleasant products on the market.
The authors declare no conflict of interest.
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This Study Was Aimed At Investigating The Suitability Of Two Fruits (Pineapple And Soursop) As
Acta Scientifci Nutritional Health
Folasade Adeboyejo
Constance C Ezemba
This research was carried out to produce wine from banana (Musa sapientum) pulp using yeast (Saccharomyces cerevisiae) isolated from grape (Vitis vinifera).The fermentation of the banana wine lasted for 21 days. Physico-chemical parameters were determined during fermentation using standard procedures. Liquor of the fermenting must was removed for every 48 hours from the fermentor for analysis of pH, titratable acidity, specific gravity and reducing sugar using standard procedures. The results from the experiment showed that specific gravity of the wine was observed to reduce drastically as the fermentation progressed. The pH of the banana wine during fermentation increased from 4.16-4.22 at day to the last day while the titrable acidity (% w/v tartaric acid) of the banana wine produced increased from 1.05-1.77. The alcohol content of the wine increased with time. The specific gravity values were observed to range from 1.266 to 1.184 kg/m 3 which gradually decreased throughout the period of fermentation. At the end of the fermentation,
SpringerPlus
Chukwuma Stephen Ezeonu
PRODUCTION OF WINE FROM THE FERMENTATION OF ORANGE JUICE BY Saccharomyces cerevisiae
Oladimeji ishaq Hassan
The fermentation of orange juice by Saccharomyces cerevisiae isolated from palm wine was carried out. The fermentation was done in two phases; the aerobic phase which lasted for 5 days and the anaerobic phase which lasted for 9 days. Some physicochemical parameters were monitored during the aerobic and anaerobic phase of fermentation. These were pH, titratable acidity, specific gravity, sugar content and alcohol concentration. The result of the physicochemical analysis showed that during aerobic fermentation there was a decline in the pH from 3.6 to 2.4; an increase in titratbable acidity from 9.10 to 16.8g/l. During anaerobic phase the pH increased from 3.0 to 4.3 while the titratable acidity decreased from 16.4 to 9.7g/l. The yeast counts increased from 5.5 ×106 to 6.9×106 cells/ml; alcohol content increased from 0 to 5.4% during aerobic fermentation, while during anaerobic there was a drop in yeast counts from 7.1×106cells/ml to 6.3×106 cells/ml; and the alcohol content increased from 5.8 to 9.6%. The sugar content and specific gravity in the wine dropped throughout during aerobic and anaerobic fermentation with sugar content dropping from initial value of 50.80 mg/ml to 2.87 mg/ml, while the Specific gravity dropped from 1.040 to 0.980osp.gr. On the 9th day of the anaerobic phase the fermentation was terminated by opening the fermentation tank, the wine was then clarified, racked and bottled.
The study was aimed at the production of apple (Malus pumila) fruit wine with the use of yeast Saccharomyces cerevisiae isolated from palm wine. Both primary and secondary fermentation of the apple lasted 28 days. Aliquot samples were removed and used daily from the fermentation tank for analysis of alcohol content, specific gravity, pH, titratable acidity, and reducing sugar using standard procedures. During fermentation, pH of the fruit must range from 5.0 to 3.2. There was an increase in alcohol content, which was observed with time. Finally at the end of the 28 th day's fermentation, the alcohol concentration in the fruit wine was observed to be 3.2%. Also titratable acidity concentration of the wine shows steady increase with time throughout the fermentation period. This study has revealed that much acceptable wine with quality could be produced from apple with Saccharomyces cerevisiae isolated from palm wine. Sensory evaluation results showed there were no significant differences (p > 0.05) in flavor, taste, clarity and overall acceptability between apple wine and a reference wine. The apple wine was generally accepted.
Journal of Food Science and Engineering 9 (2019) 199-209
Caroline Ebere
The aim of this study was to produce and evaluate table wine from two different varieties of pawpaw (rose red and yellow pawpaw). The must was evaluated for physicochemical and microbiological changes during fermentation while the wine was analyzed for physicochemical characteristics, microbiological quality and sensory properties and compared with commercial grape wine. Specific gravity of the “must” during fermentation decreased from 1.059-0.995 for rose red pawpaw and 1.005-0.990 for yellow pawpaw. The sugar content decreased from 13-3% on the 14th day of fermentation for rose red pawpaw while yellow pawpaw “must” decreased from 12.5-3%. pH drop for the yellow pawpaw “must” was 4.7-3.4 on the 14th day and 4.0-3.4 for rose red pawpaw “must”. Titratable acidity of the pawpaw “must” increased from 0.16-0.32% for rose red pawpaw “must” and 0.20-0.52% for yellow pawpaw “must”. Microbial analysis of the “must” during fermentation showed that yeast count increased from no growth to 3.0 × 106 cfu/mL for yellow pawpaw must and 4.0 × 106 cfu/mL for rose red pawpaw, respectively while total bacterial count decreased from 5.4 × 107-l.5 × 107 cfu/mL for yellow pawpaw must and 5.2 × 107-1.2 × l07 cfu/mL for rose red pawpaw “must”. Coliform recorded no growth throughout the period of fermentation. Physicochemical analysis of the wine showed that the yellow pawpaw wine has a specific gravity of 0.999, alcohol content 8.00%, titratable acidity of 0.59%, pH of 3.5 and sugar content of 3%. The rose red pawpaw wine had sugar content of 3%, titratable acidity of 0.38%, alcohol content 7.69%, specific gravity 0.997 and pH of 3.5. Microbial analysis of the wine showed no growth of coliform and yeast while bacterial count was 1.0 × 106 cfu/mL for both wines. Sensory results for the pawpaw wine showed no significant (p > 0.05) difference in the clarity and overall acceptability from the commercial wine.
Integrative Food, Nutrition and Metabolism
Pratap Chandran
Kehinde P Akinrotoye
The effect of fermented palm wine tapped from Raphia palm tree (Raphia hookeri) on the growth of some common diarrhoeagenic bacteria such as Staphylococcus aureus, Escherichia coli, Salmonella typhi, Shigella dysentariae and Esherichia coli 0157:H7 was carried out using agar diffusion method. The palm wine used had growth inhibitory effect on all the test organisms with diameter of zones of inhibition ranging from 2.20mm to 28.20mm. Palm wine subjected to fermentation for 168hours (7 days) exerted the highest growth inhibitory effect on all the test bacteria. The inhibition mediated by this palm wine was superior to that of some conventional antibiotics used such as tetracycline, ampiclox and ampicillin. It is conceivable therefore that palm wine subjected to natural fermentation or freshly tapped could be used to treat diarrhoea caused by these organisms.
Chigozie E Ofoedu
Physicochemical and sensory acceptability of wine made from soursop (Annonamuricata) were evaluated. A “must” (soursop juice before or during fermentation) sample of the soursop pulp was prepared and replicated. Its replica is referred to as sample B in this work. The “must” samples were treated with 0.543/litre of sodium metabisulphite, inoculated with 5grams reconstituted active baker’s yeast and allowed to ferment. The fermentation lasted for 11days. The wine sample produced had a final alcohol content of 12.99%, pH of 3.42, and total acidity of 0.82%. The green wine (young) was aged for 12weeks to reduce the acidity and to develop a characteristic bouquet. It was packaged and presented for sensory evaluation using Don Morris white wine as a standard. The sample wine compared favorably with the standard with no significant difference (p>0.05) in odor and taste but with a significant difference (p<0.05)in color acceptability. The green wine was also compared with the replica and no significant difference obtained. The wine at 9months old was tested again and 3.35, 0.9826, 13.95% and 2.15% for pH, specific gravity, alcohol content and titratable acidity respectively was obtained. Sensory evaluation at 9months old was also carried out and result obtained was used in evaluating analysis of variance. No significant difference existed in color, odor, taste and acceptability.
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Chemical Science Review and Letters
EZENWA MARTINS
Enya Emmanuel
Pr. Roger DJOULDE Darman
International Journal of Current Microbiology and Applied Sciences
Pooja Nikhanj
Victor S I N G H Ayam
International Journal of Microbiological Research
Dr. P. Saranraj
ighedi israel
priya sekar
Journal of Food Processing & Technology
harmeet chauhan
Indian Journal of …
Newitchaya Wutthinithisanand
Oranusi Solomon
Runu Chakraborty
Journal of Applied …
Karan Bagde , pranali waghdhare
konfo Christian
J M Noel MUNYANEZA
Oluwatoyin Olugbemi
Journal of Applied Biology & Biotechnology
vandana ranganathan
UMYU Journal of Microbiology Research
Adebare J. Adeleke
Paul Osei-fosu , Henry Mensah-Brown
La Granja: Revista de Ciencias de la Vida
Plant Foods for Human Nutrition (Formerly Qualitas …
MOHAMMAD AIZAT JAMALUDIN , Mohd Anuar Ramli
Fred O.J. Oboh
Iyamenye Nibeho Clet
Antonella Pasqualone
Nausheen Saba
Piyush Kashyap
IMAGES
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Abstract. The study was aimed at the production of apple (Malus pumila) fruit wine with the use of yeast Saccharomyces cerevisiae isolated from palm wine. Both primary and secondary fermentation ...
Fruit Wine Production: A Review. Shrikant Baslingappa Swami*, N.J. Thakor. and A.D. Divate. Department of Agricultural Process Engineering, College of Agricultural Engineering and Technology, Dr ...
This study has revealed that much acceptable wine with quality could be produced from apple with Saccharomyces cerevisiae isolated from palm wine. Sensory evaluation results showed there were no significant differences (p > 0.05) in flavor, taste, clarity and overall acceptability between apple wine and a reference wine.
This paper provides a production technology to process Golden Delicious apple cultivar to apple wine using a local yeast isolate from apple. Materials and methods Apple juice extracted from apples (cultivar Golden Delicious) having brix of 9.6 ± 1.5 °B and pH of 3.5 ± 0.2 was procured from local market during 2015 and 2016.
The present study was conducted to optimize fermentation parameters for apple wine production using Golden Delicious apples. Physicochemical analysis of the cultivar revealed a °Brix-acid ratio of 24.61 with ample amount of total and reducing sugars (9.6 and 6.03% w/v); making it a suitable substrate to produce ethanol. Microbiological analysis lead to isolation of a yeast strain (namely A2 ...
Current Journal of Applied Science and Technology 41(3): 1-6, 2022; Article no.CJAST.57683 ISSN: 2457-1024 (Past name: British Journal of Applied Science & Technology, Past ISSN: 2231-0843, NLM ID: 101664541) Wine Production from Apple (Malus pumila) Using Yeast Isolated from Palmwine C. C. Ezemba a*, V. N. Anakwenze b and A. S. Ezemba b a ...
Jagtap and Bapat (2014), evaluated the potential of custard apple in the production of a beverage fermented using S. cerevisiae (NCIM 3282) yeast and assessed the antioxidant capacity, total phenolic content and DNA damage-protecting activity of custard apple fruit wine. Custard apple wine showed free radicle scavenging activity towards DPPH ...
production of wines from available fruits could reduce the level of post harvest losses and also increase variety of wines [12,9,8]. Amerine and Kunkee, [13] observed that the type of wine to be produced dictates and strain of yeast to be involved and also the fruit to be used. Some of the preservatives used in wine making
The study was aimed at the production of apple (Malus pumila) fruit wine with the use of yeast Saccharomyces cerevisiae isolated from palm wine. Both primary and secondary fermentation of the apple lasted 28 days. Aliquot samples were removed and used daily from the fermentation tank for analysis of alcohol content, specific gravity, pH, titratable acidity, and reducing sugar using standard ...
The flavour and the volatilome of apple wines made from the Austrian heritage variety Ilzer Rose was in the scope of this study. The apple wines were produced by adopting oenological practises that are not commonly used in fruit wine production. Different fermentation strategies including the addition of enzymes with β-glucosidase activity, addition of a fining agent, maceration of the mash ...
of different nitrogen concen trations in apple wine fermentation. The a verage total nitrogen content in 51 d ifferent. apples juices was 155.81 mg/L, with 86 .28 % of the values above 100 mg/L ...
The study revealed a process for apple wine preparation using an indigenous yeast and also optimized and compared malolactic and non-malolactic fermented ciders. The present study was conducted to optimize fermentation parameters for apple wine production using Golden Delicious apples. Physicochemical analysis of the cultivar revealed a °Brix-acid ratio of 24.61 with ample amount of total and ...
1. Introduction. Apple wine and cider are traditional alcoholic beverages with an alcohol content lower than 8.25%. The European Cider and Fruit Wine Association (AICV) states that within the European Union, cider and fruits wines have some of the fastest growth rates of all alcoholic beverages [].This increase in popularity is also reflected by the number of scientific papers that were ...
A biocatalyst was prepared by immobilization of Saccharomyces cerevisiae strain AXAZ-1 on apple pieces. It was examined by electron microscope and studied during the fermentation of grape must for batch wine-making. The immobilized yeast showed an important operational stability without any decrease of its activity even at low temperatures (1−12 °C).
The engineered wine yeast strains described in this paper show the potential of novel yeast strain development to improve wine quality. But molecular biologists face a major obstacle to this progress: near world-wide refusal to permit the use of GMOs in the production of foods and beverages, at least in 'developed' countries ( Gross, 2009 ...
The selection of apple fruit for making wine depends upon several factors such as market demand, availability of raw material, production facilities, and sound economic reasons. ... Influence of juice contents on quality of apple wine prepared from apple juice concentrate. Research and Industry 39 (4), 250. 4.3.6. Inoculation With Yeast Culture.
Introduction. The world area under vines and the volume of wine production in 2017 have not changed significantly over the last 15 years since 2002, however, the value of wine exports in US$ has more than doubled (Anderson and Pinilla 2017).Wine production faces new challenges such as global warming (van Leeuwen and Darriet 2016) and increasing competition from the emergence of new markets and ...
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This work has shown that the pH ranges of the pineapple, watermelon, and mixed fruit juice used for the production of the wine for this research were 4.22 ± 0.01, 5.07 ± 0.01 and 4.47 ± 0.01 respectively, while there was no significant difference in the values of the reducing sugars amongst the three samples.
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Production of Wine and Vinegar from Cashew (Anacardium occidentale ) "Apple" Samuel Lowor 1*, Daniel Yabani 1, Kumi Winifred 1 and C. K. Agyente-Badu 1 1Cocoa Research Institute of Ghana, P.O.Box 8, Akim-Tafo, Ghana. Authors' contributions The present work was result of the efforts of all authors. The lead author SL designed the
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