Stewart Postharvest Review

Stewart Postharvest Review An international journal for reviews in postharvest biology and technology

Biochemical description of fresh produce quality factors JK Fellman,1, 2* TJ Michailides3 and GA Manganaris2, * 1

Department of Horticulture, Washington State University, Pullman, USA Department of Agricultural Sciences, Biotechnology and Food Science, Cyprus University of Technology, Cyprus 3 Department of Plant Pathology, Kearney Agricultural Research and Extension Center, University of California at Davis, Parlier, CA, USA 2

Abstract Purpose of review: Consumer appreciation of nutritional value and putative disease prevention roles has fostered worldwide increases in fresh fruit consumption. Preservation of fresh fruit quality remains a postharvest challenge for the perishables industry. Many biochemical factors influence the consumer’s perception of quality. Using examples from widely studied fruits, this review focuses on recent developments in general areas associated with quality assessment, and quality changes in the postharvest environment. Recent findings: The principal biochemical components that contribute to the consumer perception of quality can be separated into three major classes: (1) those associated with “mouth feel”, ie, firmness and texture; (2) those associated with taste, eg, sweetness, acidity, aroma/flavor, and astringency; and (3) those components that contribute to appearance, notably color and surface finish. Objective measurement of texture is possible using a variety of destructive instrumentation, with progress in development of non-destructive technologies with possible on-line applications. Our understanding of cell wall architecture and biochemical components therein has advanced, establishing the relationship between cell wall modifying enzymes and textural softening. Sensory correlations between several types of objective measurements are still being investigated. Advanced sweetness and acidity measurement technologies are welldeveloped, with many studies regarding postharvest changes and the influence on sensory quality. Volatile aroma production remains an active area of investigation, both in the analytical and sensory disciplines. Postharvest storage and handling influence volatile development. Phenolic substance measurement has enjoyed renewed popularity due to the putative neutraceutical benefits, with more emphasis on radical scavenging capability. Exploitation of genomic and biotechnological tools (gene isolation, cloning and expression studies) has resulted in initial quality trait heritability studies. Limitations: Challenges still remain. Fruit eating quality factors are very complex traits that are influenced by the interaction of genome, growing conditions, and harvest maturity, as well as postharvest handling and storage. Fundamental mechanisms responsible for changes in quality are not completely understood, as most biochemical pathways that determine quality traits are still being identified. Directions for future research: Consumer perception of fruit quality by consumer sensory analysis, combined with instrumental analysis should further define the relationship of individual components responsible for texture, taste and aroma to the total “quality experience”. This includes the role of changes in cell wall components, turgor, sugar and acid transformations, and volatile aroma compound changes in relation to instrumental and sensory testing. Through application of biochemical, genomic, proteomic and microscopic methods to determine fundamental metabolism and its control, the true nature of "ripeness", "eating quality" and "freshness" of fruit products will be revealed, facilitating employment of modern storage and handling technologies for preservation of same. Keywords: cell wall; firmness; texture; color; taste; astringency; aroma; perishable; phenolics; phytochemicals; antioxidants

*Correspondence to: JK Fellman, Department of Horticulture, Washington State University, Pullman, WA 99164-6414, United States; Email: [email protected]; GA Manganaris, Cyprus University of Technology, Department of Agricultural Sciences, Biotechnology and Food Science, 3603 Lemesos, Cyprus. Email: [email protected] © 2013 Stewart Postharvest Solutions (UK) Ltd. Online ISSN:1945-9656 www.stewartpostharvest.com

Stewart Postharvest Review 2013, 3:2 Published online October 2013 doi: 10.2212/spr.2013.3.2

Fellman et al. / Stewart Postharvest Review 2013, 3:2

Abbreviations 1-Methycyclopropene 1-MCP Aminoethoxyvinylglycine AVG Controlled Atmosphere CA Proanthocyanidin PA Polyphenol Oxidase PPO Rhamnogalacturonan RG Ultra Low Oxygen ULO

Introduction All people associated with production, handling, and consumption of perishable horticultural crops have an idea of what quality should be, yet it is difficult to arrive at a “one size fits all” definition. This is largely due to the perception and criteria developed by the needs of those interested in a particular aspect of production; a grower may consider yield and size the most important aspects of high quality, while the handler/packer may indicate harvest and transit durability as a major quality aspect. That being said, quality in the eyes of the consumer remains the economic driver of the entire postharvest effort. Quality of perishables represents the unique blend of texture (mouth feel), appearance (eye appeal) and taste characteristic to the particular perishable commodity. High-quality items have the exact blend of these desirable characteristics, and quite often command premium prices in the marketplace. Biochemical factors that contribute to this perception of highquality are manifold and can be influenced by elements encountered in the postharvest environment. There are three major biochemical classes that can influence consumer perception of quality of fresh horticultural products: those associated with “mouth feel”, ie, firmness and texture, those associated with taste: sweetness, acidity, aroma/flavor, and astringency. The third class of biochemical components contributes to appearance, notably color and surface finish.

Firmness and texture The relationship between textural changes as measured by physical methods and changes in specific components known to exist within cell walls of fleshy fruits remains obscure. In fact, physical measurement methods usually measure firmness via resistance to compression or puncture force which can also account for tensile strength [1]. Firmness is a gross measurement that has elements of crispness, mealiness, and juiciness which all contribute to quantitation of firmness [2, 3]. On the tissue morphology level, it is known that histological characteristics impact mechanical characteristics of apple flesh [4–6] and texture perceptions [7]. A recent study of

texture in phenotypes from an apple breeding program revealed a complementarity between texture measured by compression versus penetrometry tests owing to the different mechanical characteristics (shear resistance and or failure mechanisms) of the cuticle and flesh. Although compression correlated better with sensory characteristics than penetrometry, overall correlation with sensory texture descriptors was still low. Interestingly, the relative cell size distribution in the outer parenchyma was shown to be related to flesh mechanical properties and sensory juiciness perception [8]. In an excellent treatise, Ruiz-May and Rose describe it best: “…such parameters likely represent different underlying structures and interacting molecular forces.” [9]. In the same reference, the authors describe state-of-the-art knowledge regarding cell wall molecular architecture. Our fundamental understanding, therefore, represents the accumulated knowledge from biochemical changes associated with firmness loss related to cell wall “disassembly”, a contrived term that represents biochemical events related to metabolism of cell wall components. Apparently, textural softening has been attributed to various forms of cell wall disassembly in a variety of horticultural commodities. In a landmark study, cell wall material from nine fruit species with different firmness characteristics was examined [10]. In vitro examination of extracted material revealed a pronounced degree of cell wall swelling in fruit that had a melting characteristic when ripe, while fruit that retained a firm texture when ripe showed no swelling whatsoever. It was further determined that pectin solubilization and dissociation from the cellulosic matrix was a major contributing factor to these responses. Changes in cell wall structure and composition are the presumed cause of this softening [11], largely due to the fact that many studies correlate softening however measured [1], to the action of an array of cell wall-modifying enzymes involved in this complex biochemical process [11, 12]. During ripening, water-soluble polyuronides increase while insoluble and covalently bound pectin decreases. The loss of firmness during ripening is associated with the activity of several cell wall-modifying enzymes [13]. Firmness loss during fruit development is usually associated with cell wall polysaccharide turnover [11]. Depolymerization of polyuronides from the pectin network, which may help pectin solubilization, is driven by the coordinated action of a large number of enzymes able to degrade or modify cross-links between cell wall polysaccharides. Differences in gene expression pattern and activity of these putative cell wall-modifying enzymes have been reported among different fruit species and even among cultivars of a given species. In addition to pectinolytic enzymes, apple cell wall proteins involved in loss of cell–cell adhesion and cell wall disassembly are xyloglucan transglucosylases/hydrolase, glucanase, and expansin, all acting to deconstruct the hemicellulosecellulose interaction. Arabinofuranosidase and galactosidase 2


hydrolyze pectic, arabinan, and galactan side chains during apple ripening, but unlike other fleshy fruits, pectin methyl esterase and endopolygalacturonase enzymes appear to play a minor role in spite of the increased pectin solubility during softening [13, 14]. In contrast, pectin depolymerization studies in cherries showed that soft ‘Bigarreau Burlat’ cherries had more polymer degradation than firm fruit [15]. However, in other cases, softening occurs without extensive endopolygalacturonase action and pectin degradation [16]. In ripening of melting-flesh peaches and nectarines, the solubility increase of cell wall materials during the melting phase of fruit softening suggests a large part of the solubilized polysaccharides remain ionically linked to the cell wall [11]. In summary, pectin solubilization, removal of rhamnogalacturonan I (RG-I) side chains [17], increase of cell walldegrading enzymes (ie, hemicellulases, cellulases, polygalacturonase, and β-galactosidase ) all play a role, but the individual contribution of each activity to overall softening remains poorly understood [18]. Although general assumptions can be made, apparently certain phenomena related to cell wall metabolism are species-specific. On the other hand, loss of fruit firmness, an important quality factor for all perishables, is not solely dependent on cell wall metabolism and there may be other factors such as water status (turgor pressure) and cuticle structure that also contribute to postharvest life [19]. With regard to cellular water status, fruit softening is related to changes in turgor pressure [20– 23]. Studies with blueberries have conclusively linked decreased firmness with moisture loss [24], yet the true biological mechanism responsible for this relationship remains obscure. A comparison of melting- and non-melting flesh peach tissues showed a marked difference in cell-cell adhesion upon the advance of ripening, where the melting flesh peach cells came apart due to endo-polygalacturaonase action on the middle lamella, and the non-melting flesh peach tissues stayed together, yet firmness change was attributed to the mechanisms of cellular water status (turgor) change connected with cell wall disassembly [25]. Nevertheless, a reduction in cell turgor may contribute to firmness decrease during storage but it is unlikely that this process alone causes textural softening and changes in fruit. Future studies will probably involve assessment of epidermal resistance and changes in cell morphology coupled with direct turgor measurements.

Taste: sweetness Perceived flavor quality, especially in fleshy fruits, represents a delicate interplay between texture, mixed with the proper concentrations of free sugars, organic acids and volatile compounds. Principal sugars responsible for perception of sweetness are sucrose, fructose, glucose and sometimes a sugar alcohol sorbitol (species dependent). In the majority of recent quality-related studies, individual sugars were rarely quantified, rather a simple refractive index measurement of soluble solids content is reported. Relative concentration of soluble sugars is species and cultivar dependent, with most fruits of

commerce within the range of 0.5 and 15% of the total fresh weight. In harvested products, the metabolic origins of monosaccharides are sometimes linked to the hydrolysis of starch reserves, previously deposited during growth and development, again species-dependent. As climacteric fruit ripen, free sugar content increases as starch is hydrolyzed, thus providing the characteristic sweetness [26–29]. Glucose, the direct product of starch degradation, generally increases during storage along with associated monosaccharides and sorbitol. There is very little additional change during storage after starch content is completely converted to soluble sugars. While having the same general monosaccharide profiles, non -climacteric fruits like mandarin and pineapple undergo no appreciable sugar decrease during storage [30–31].

Taste: acidity Major organic acid components are also species-dependent, with the majority of the edible fruits of commerce falling into categories based on the principal organic acid present, ie, malic or citric acid except for grapes, where the major acid is tartaric [32, 33]. These acids occur in amounts far beyond those necessary as intermediary metabolites, often as 70– 90% of the total amounts of acids in the tissue. As is the case with sugar content, individual acid species are rarely measured, and are quantified by titration methods with results reported as the relative amount of the most abundant acid species within the fruit. Acidity tends to decrease correspondent to a lengthening storage period, regardless of the fruit under study. In citrus, for example, the temperature of the storage environment affected the rate of acidity loss, with a notable exception in the case of malic acid content, which increased when fruit were held at 30°C [31]. In apples, a survey of seven cultivars demonstrated an average malate decline of 36% after 4–5 months refrigerated storage [34]. Organic acids, being respiratory substrates, are always metabolized in stored crops as a function of maturity at harvest. Immature fruit have a relative abundance of acids, which slowly declines during the ripening period [35, 36]. It follows that any postharvest condition that delays the rate of ripening also preserves the acid content, especially in climacteric fruits.

Taste: astringency/bitterness Plant phenolics are one of the most abundant natural chemical groups and are of particular interest with regard to significant roles in defining a wide range of organoleptic characteristics in fruit, such as color, bitterness and astringency. In ripe fruits, concentrations range from trace amounts up to 8.5% dry weight [37, 38]. An increasing body of evidence strives to implicate fruit phenolic substances as a “neutraceutical” quality factor as well, undoubtedly attributable to their antioxidant properties [39, 40], as well as their relative abundance. The health benefits of phenolic compounds have been extensively examined [41], and remain under continuous investigation. 3


A majority of phenolics, especially those associated with fruit colors (discussed in another section) have no taste properties, yet some members of this chemical group can profoundly influence the perception of bitter and astringent flavors. Phenolic acids can impart a sour character and some citrus flavonoids (naringin) impart a bitter taste [42]. In fresh persimmon, this phenomenon is well documented, as most persimmon fruits accumulate proanthocyanidins (PAs) in their flesh during development, which causes the sensation of astringency due to coagulation of oral proteins, a property of all tannin substances [43, 44]. Therefore, these fruits are rendered inedible if they are not artificially treated to eliminate astringency and the commercial quality is compromised by PA accumulation. Treatment after the harvest usually involves methods to induce anaerobic metabolism in order to cause a transient increase in ethanol levels, where the acetaldehyde metabolite reacts with water-soluble astringent PA molecules, causing them to polymerize. After polymerization, the procyanidins (tannins) are no longer astringent as they are unable to react with taste receptors. Browning is due to the oxidation of phenolics. Data suggest that various factors such as total phenolic content, its compounds composition and polyphenol oxidase (PPO) activity all have roles in the browning response [40, 45, 46]. As PPO is localized on the thylakoid membrane of chloroplasts and polyphenols are in the vacuole, a cellular loss of compartmentation is also needed to make PPO oxidize its substrates [47]. Browning therefore, results upon tissue disruption during bruising from mishandling [48] atmospheric damage [49] and the processing of fruits into high-value products [50]. Due to discrepancy between cultivars and species, additional knowledge is required to clarify any links between these factors and tissue browning. The mechanism for browning involves the reaction of phenolics with PPO in the presence of oxygen; PPO catalyzes two reactions: (1) hydroxylation of monophenols to diphenols and (2) oxidation of diphenols to quinones. The hydroxylation reaction is relatively slow and results in colorless products, while the oxidation reaction is relatively rapid and the resultant quinones are dark-colored. Subsequent reactions (polymerization) of quinones lead to melanin accumulation, which is the brown or black pigment associated with “browning” in plant tissues. Specific reactions resulting in brown or black-colored products depend on the specific structures of the polyphenolic substrate [51]. Control of enzymatic browning will eventually require genetic manipulation of PPO activity, either via traditional breeding and selection [52], or introduction of antisense elements to deactivate native enzymes [53].

Taste: aroma/flavor Flavor in terms of volatile aroma compounds is determined primarily by genetic factors and it can be affected by preharvest conditions, postharvest handling, packing operations and storage. Odor-active volatile compounds represent a major

quality parameter for fresh produce. This represents a complex mixture of a large number of volatile compounds, whose composition is species-specific, sometimes even to the level of varietal differences and often to the variety of fruit. As a result, enhancing the concentration of volatiles within and emanating from fruit has remained an important challenge. A survey of available information reveals interesting phenomena as noted here. Characterization of the nature and occurrence of important aroma contents has been described in many fruits of commerce, with new information frequently becoming available [54–57]. In addition, many sensory studies using human subjects are available [58, 59]. Generally, climacteric fruits, those sensitive to the ethylene ripening signal, do not manufacture appreciable amounts of volatiles associated with quality until ripening commences [60]. Therefore, fruits harvested before ripening have a reduced ability to produce aromas, no doubt related to the ethylene insensitivity of unripe fruit. Any postharvest treatment that inhibits the action of ethylene, such as 1-methylcyclopropene (1-MCP) will also inhibit flavor and aroma development [61,62]. Volatile biosynthesis is significantly reduced in apple fruit subjected to ultra low oxygen (ULO) storage, and also after treatments with aminoethoxyvinyl glycine (AVG) and 1-MCP; the reduction became severe after an extended storage period [63]. In oranges, sensory quality as measured by likeability was maintained throughout a 6 week storage period when fruit were kept at 5°C, but rapidly declined upon moving fruit to 20°C. Flavor loss increased as the duration of cold storage prior to the warm temperature holding period was lengthened. The beneficial effect of maintaining mandarins in cold storage was also observed in three of the five other varieties where there was flavor quality loss during storage at a warmer temperature [64]. Genomic studies have confirmed the ethylene-sensitivity to aroma generation in climacteric fruit, as well as identified the genes and gene products responsible for aroma generation [65]. Other work has identified quantitative trait loci for apple aroma for use in efforts to enhance the properties of apple varieties with regard to aroma and flavor [66].

Surface characteristics Appearance, perhaps the most important quality determinant, is influenced by physical factors such as size, shape, presence of defects (ie, blemishes, bruises, spots), finish or gloss. Size and shape may be influenced by cultivar, maturity, production inputs, and the growing environment. For successful commercial marketing, it is important for fruits and vegetables to have uniform size and characteristic shape [67]. Presence of defects will be affected by exposure to disease and insects during the growing period, harvest, and postharvest handling operations. Some mechanically harvested fruits and vegetables are usually subjected to more bruises and cracks than those harvested by hand. Fruit and vegetable luster (shininess) is related to the ability of a surface to reflect light; 4


freshly harvested products are often more glossy [68]. Luster is affected by surface wax deposition [69], which is influenced by postharvest handling and storage practices. Like most aerial parts of plants, fruits are covered with a continuous extracellular cuticle, composed of a cutin layer and a surface, or epicuticular wax layer. The wax is secreted from the cutin matrix to form the surface between the environment and the plant. Most of our knowledge of fruit waxes comes from the study of apple and citrus. Generally, the amount, composition and structure of epicuticular wax varies among cultivars, and changes with fruit development, maturation, age [70], and environmental conditions. Indicatively, in French prune, environmental conditions (ie, rain during full bloom) play a significant role in the amount of cuticle formation and epicuticular wax accumulation [71]. Wax characteristics influence water loss as well as cuticular gas transport, and protection from insects and microorganisms [72]. In French prune for instance, surfaces having thinner cuticle and lacking epicuticular wax are prone to infection by the brown rot fungus Monilinia fructicola more so than sites of fruit having thicker cuticle and epicuticular wax. When epicuticular wax was removed by scraping or wiping, or removed with the use of chloroform, or ethanol significantly more fruit were infected than the fruit where the epicuticular wax left intact [73]. The chemical characteristics of epicuticular wax have been thoroughly examined in apple and orange; fruit waxes are composed of long-chain hydrocarbons, primary alcohols, fatty acids (mostly palmitic acid) and aldehydes in varying proportions of the total extract depending on the species considered [74]. As turgor pressure determined by water potential is an important component of firmness quality, limiting water loss during storage is of manifest importance for overall quality maintenance. Changes in epicuticular wax characteristics during storage have been reported. In citrus, ethylene has been shown to increase epicuticular wax content while inducing structural changes in the surface wax, possibly related to ongoing wax biosynthesis after harvest. In this case, formation of new waxes during storage helps to cover areas lacking wax and probably improves physical barriers to fungal pathogen penetration as well as protect against peel pitting [70]. Apples with different surface characteristics also have waxes with different chemical composition. Controlledatmosphere (CA) storage of apples caused changes in the chemical composition, especially during a 7 day holding period after removal from storage [72]. An interesting phenomenon seen in apple, peel ‘greasiness’, is a function of continued wax and wax constituent deposition in storage. Greasiness develops during apple ripening and storage and has been linked to wax compositional changes. Greasiness has been associated with changes in surface wax composition [75] and is associated with advanced-maturity fruit and extended storage periods [76]. Treatment with 1-MCP, an inhibitor of ethylene action that delays ripening and senescence in a diverse range of fruits and vegetables [76, 77], reduces the incidence of greasiness in ‘Granny Smith’, ‘Royal Gala’, ‘Fuji’ and

‘Honeycrisp’ apples [75, 78]. Apparently, wax component biosynthesis continues throughout cold storage and is suppressed by inhibitors of ethylene action as well as controlled atmosphere (CA) storage [79]. A recent report described the analysis of apple genomic sequences that identified candidate genes potentially involved in these processes. Expression studies of the genes in fruit skin tissues showed them to be active, with transcript profiles putatively identified as participants in fruit cuticle formation [80]. As some of the gene activity was correlated with the products known to be incorporated into apple wax, future investigations have the potential to identify fruit-finish markers for cultivar quality improvement.

Color The natural pigments in fruits impart color characteristics to fresh produce. Peel color changes, hence pigment qualities change during development and ripening. Pigment species responsible for color intensity include the fat-soluble chlorophylls (green) and carotenoids (yellow, orange, and red) and the water-soluble flavonoids and anthocyanins (yellow, red, blue). In addition, enzymatic browning reactions may result in the formation of water soluble brown colored pigments. The enzymes involved in browning reactions include polyphenol oxidase, which catalyzes the oxidation of polyphenolic compounds, and phenylalanine ammonia lyase, which catalyzes the synthesis of precursors to phenolic substrates. Pigments can be analyzed by destructive methods usually via extraction with specific solvents, filtration, and quantitative measurements by spectrophotometric methods before or after chromatographic separation of individual pigment moieties. Alternately, tristimulus color measurements using nondestructive technology are widely used to measure surface color characteristics of harvested perishables. Surface measurements are usually described in terms of their L, a, and b values [68]. Chlorophyll content is usually measured as green color appearance, rather than extraction and subsequent spectrophotometric measurement. Chlorophyll is known to degrade upon fruit ripening with a concomitant increase in final color [81, 82]. Many studies have examined the ethylene-induced degreening of citrus [83, 84], yet regulation of chlorophyll breakdown is poorly understood, with only one oxygenase gene linked to senescence [85]. Another study with pear has established a relationship between non-destructive chlorophyll fluorescence measurements and postharvest behavior in storage [86]. Apparently the use of commercially-available fluorescence monitoring devices is becoming more prevalent for determining the physiological state of perishables in storage [86, 87]. Development of carotenoid-associated red and orange colors during ripening and preservation of same during postharvest storage has been well studied [88]. As is the case with chlorophyll measurement, use of tristimulus color readings to meas5


ure degree of coloring and carotenoid content by association is frequently used in postharvest studies [84, 88], sometimes combined with extractive chemical measurements [89]. Carotenoid contents can change in fruits subjected to different storage treatments. Storage temperature conditions [81, 84] and treatment of stored fruit with ozone, a known oxidant used for residue-free postharvest sanitation [89, 90] cause an increase in carotenoid content during storage. Due to the rapid advance in high-throughput gene sequencing and genomic technologies, much effort is devoted to identification of genes involved in carotenoid accumulation [83, 91], and identification of chromosome locations associated with increased carotenoid content in fruits [92, 93]. Advances in this area will ultimately translate to practical quality improvement.

Foundation, sponsored by the United States Department of State, Bureau of Educational and Cultural Affairs, for support from a Fulbright scholar grant awarded to J.K. Fellman.

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Anthocyanin (red-purple) pigment accumulation has been well studied in major fruits of commerce [35, 94]. In apple, a representative Rosaceous species, it is well known that red color, hence anthocyanin, biosynthesis is well-regulated and subject to environmental influences such as light, temperature and stress [95]. Once deposited in skin cell vacuoles, very little change occurs after the harvest. Use of modern genomics has increased prospects for quality improvement, as structural genes for red pigment biosynthesis in fruits have been well characterized. There is a distinct relationship between the anthocyanin-related genes of phenylpropanoid and flavonoid biosynthesis pathways, differential transcriptional factors, and accumulation of fruit-specific anthocyanins. However, gene regulation appears to involve a series of asyet-unknown complex events, where future studies are concentrated [96, 97]. It is expected that such studies will attempt to elucidate metabolic and genetic elements that are responsive to postharvest storage conditions.

Conclusions Fruits provide an important source of primary nutrition, health-related substances, plus minerals and vitamins, and the quality of a fruit is influenced by variety, nutritional status, and environmental conditions during plant growth and fruit development. Ripening is considered to be the ultimate stage in fruit development, and most fruit quality studies have been focused on this process which involves sensory, physicochemical, biochemical, and molecular analysis. With the development of genomic tools such as high-throughput sequencing and development of molecular markers for plant improvement, the strategies for studying fruit ripening and storage life, which can be considered an extension of the ripening process, have changed. This leads us to new and different methods of studying the complex and variable, sometimes elusive, quality changes associated with the postharvest environment.

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Acknowledgements The authors wish to acknowledge the J. William Fulbright

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