Impaginato 67 Adv. Hort. Sci., 2023 37(1): 67­73 DOI: 10.36253/ahsc­13838 CO2 modified atmosphere packaging: stress condition or treatment to pre­ serve fruit and vegetable quality? M. Cefola 1, I. Capotorto 1, V. Lippolis 2, S. Cervellieri 2, A. Damascelli 2, R. Cozzolino 3, B. De Giulio 3, B. Pace 1 (*) 1 Institute of Sciences of Food Production, National Research Council (CNR) c/o CS‐DAT, Via M. Protano, 71121 Foggia, Italy. 2 Institute of Sciences of Food Production, National Research Council (CNR), Via G. Amendola, 122/O, 70126 Bari, Italy. 3 Institute of Food Science, National Research Council (CNR), Via Roma, 64, 83100 Avellino, Italy. Key words: Carbon dioxide, fermentative metabolites, modified atmosphere packaging, respiration rate, short­term treatment. Abstract: In addition to the adoption of proper temperature and relative humidity, the selection of an atmosphere surrounding packaged fresh produce with reduced O2 and/or increased CO2 is one of the most widely used and use­ ful tools to prolong the shelf­life of horticultural crops. However, as O2 and/or CO2 values that might cause injury are strictly related to the commodity, they should be optimized for each product. Here three study cases are reported about the application of modified atmospheres (MA), with different CO2 con­ centrations (0­40 kPa), to table grapes (cv. Italia) and sweet cherries (cv. Ferrovia) and, as a short­term treatment (48 h at 0°C), to fresh­cut artichokes (cv. Violet de Provence). In each trial, the effect of high CO2 treatment on quali­ ty parameters was observed during cold storage. Concerning table grape ‘Italia’, our results show that low CO2 (up to 10 kPa) MA preserved the quality and sensory parameters of the fruit, whereas high CO2 (> 20 kPa) caused a fer­ mentative metabolism. As for sweet cherries ‘Ferrovia’, 20 kPa CO2 MA helped to maintain the quality traits during storage. On the other hand, this fruit proved to be sensitive to CO2 accumulation (over 20 kPa) in hypoxic conditions, since it caused an increase in respiration rate and the biosynthesis of volatile fermentative metabolites. Finally, for fresh­cut artichokes, a short­term CO2 treatment, up to 10kPa, reduced respiration rate and browning index, preserv­ ing the volatile profile, while high CO2 (40 kPa) may have caused fermentative metabolism. In conclusion, the application of a MA enriched in CO2 has been shown to have different effects on the quality parameters of the three prod­ ucts, in agreement with the fact that CO2 sensibility depends on each specific fruit or vegetable under study. 1. Introduction Fruits and vegetables are perishable products, and extending the keeping quality during their postharvest life represents one of the main (*) Corresponding author: bernardo.pace@ispa.cnr.it Citation: CEFOLA M., CAPOTORTO I., LIPPOLIS V., CERVELLIERI S., DAMASCELLI A., COZZOLINO R., DE GIULIO B., PACE B., 2023 ­ CO2 modified atmo‐ sphere packaging: stress condition or treatment to preserve fruit and vegetable quality? ­ Adv. Hort. Sci., 37(1): 67­73. Copyright: © 2023 Cefola M., Capotorto I., Lippolis V., Cervellieri S., Damascelli A., Cozzolino R., De Giulio B., Pace B. This is an open access, peer reviewed article published by Firenze University Press (http://www.fupress.net/index.php/ahs/) and distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Competing Interests: The authors declare no competing interests. Received for publication 4 October 2022 Accepted for publication 26 January 2023 AHS Advances in Horticultural Science https://doi.org/10.36253/ahsc-13838 http://www.fupress.net/index.php/ahs/ http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ Adv. Hort. Sci., 2023 37(1): 67­73 68 goals of researchers in this field. It is widely known that, together with the proper temperature and rela­ tive humidity management, the gas composition sur­ rounding the product during storage, is one of the main factors that affect the quality of horticultural crops (Kader, 2003). In general, the decrease in oxy­ gen, the increase in CO2, or the association of both conditions are useful to preserve the physiological state of fruits and vegetables, reducing the rate of respiration, oxidative processes, and decay, thus pro­ longing their shelf­life. In contrast, inappropriate gas concentrations outside safe limits can cause stress conditions that lead to physiological disorders, devel­ o p m e n t o f o ff ­ o d o u r s d u e t o f e r m e n t a ti v e metabolism, or increases in susceptibility to decay (Mangaraj and Goswami, 2009). Although low O2 and high CO2 have similar effects, under modified atmo­ sphere packaging (MAP) conditions, elevated CO2 is a major factor influencing the quality of fruits and veg­ etables (Watkins, 2000). In addition, the sensitivity to elevated high CO2 and/or low O2 levels depends on the commodity (Toivonen and DeEll, 2002). It is influ­ enced by pre and postharvest factors, such as culti­ vars or stage of maturity, and by processing, since the oxygen consumption and the consequent CO2 accumulation in fresh­cut produce is faster than in corresponding intact produce (Francis et al., 2012). To obtain the beneficial effect of MAP, gas conditions should be optimized for each product. Starting from these considerations, the aim of the present work was to compare the effect of different CO2 concen­ trations in MAP on the quality of table grapes, sweet cherries and fresh­cut artichokes as case studies. 2. Materials and Methods Table grapes (Vitis vinifera L., cv. Italia), sweet cherries (Prunus avium L., cv. Ferrovia), and artichokes (Cynara cardunculus (L.) subsp. scolymus Hayek, cv. Violet de Provence) were provided by local farms located in Noicattaro and Foggia (Italy) and processed at the Postharvest Laboratory of CNR­ISPA the day of harvest. Selected bunches of table grapes (about 1 kg each) were placed in polyethylene terephthalate (PET) trays (model CL1/135 Carton Pack, Rutigliano, Italy). They were sealed with a vacuum sealer (model Boxer 50 Lavezzini Vacuum Packaging System, Fiorenzuola d’Arda, Italy) in 30 x 40 cm polyamide/polyethylene (PA/PE) bags (Orved S.p.A., Musile di Piave, Italy) applying two modified atmosphere (MA) mixtures with different initial CO2 concentrations plus 1 kPa of O2: 1.0/0.03 O2/CO2 kPa (1 kPa­O2), and 1.0/20.0 O2/CO2 kPa (1 kPa­O2 + 20 kPa­CO2). Unsealed bags were used as control (Air). All samples (4 replicates per treatment) were analyzed at harvest and after 20 days of storage at 5°C for respiration rate (RR), rachis browning (rB), ethanol, and acetaldehyde contents. For sweet cherries, about 200 g of fruits, without defects or diseases, were placed in PET trays and sealed in 30 x 40 cm PA/PE bags with three MA mix­ tures: 1.0/0.03 O2/CO2 kPa (1 kPa­O2), 16.0/20.0 O2/CO2 kPa (16 kPa­O2 + 20 kPa­CO2), and 1.0/20.0 O2/CO2 kPa (1 kPa­O2 + 20 kPa­CO2). Samples stored in unsealed bags (Air) were used as controls. All sam­ ples (3 replicates per treatment) were analyzed at harvest and after 21 days of storage at 5°C for RR, relative water content of peduncles (RWC), and volatile organic compounds (VOCs). As for artichokes, the heads were trimmed, elimi­ nating the external bracts and cutting the stem. The obtained artichoke hearts were then cut into quar­ ters and dipped for 5 min in a solution of 1% ascorbic acid + 0.2% citric acid (w:v), drained, and randomly selected for different treatments. In particular, three replicates of 16 artichoke quarters were kept for the initial determinations, while the remaining quarters were closed in 50 x 50 polypropylene (PP) bags (Carton Pack® Rutigliano, Italy), about 600 g per bag, applying 4 MA mixtures with different initial CO2 con­ centrations plus 10 kPa of O2: 10.0/10.0 O2/CO2 kPa (CO2­10kPa), 10.0/20.0 O2/CO2 kPa (CO2­20kPa), 10.0/30.0 O2/CO2 kPa (CO2­30 kPa), 10.0/40.0 O2/CO2 kPa (CO2­40 kPa). Unsealed bags were used as con­ trol (Air). After 48 h of storage at 0°C, all bags were opened, artichoke quarters were placed in open poly­ ethylene bags and analyzed after 48 h at 0°C plus 7 days of storage at 5°C for RR, browning index (BI) and VOCs profile. The headspace gas composition (O2 and CO2) within each MA package was monitored daily using a gas analyzer (CheckPoint, PBI Dansensor, Ringsted, Denmark). RR was measured initially (Fresh) and at the end of the storage for each prod­ uct using a closed system, as reported by Kader (2002 a). Samples were put into 6 L sealed plastic jars, allowing the accumulation of CO2 up to 0.1 kPa. For CO2 analysis, 1 mL of gas sample was collected from the headspace of each jar and injected into a gas chromatograph (p200 micro GC, Agilent, Santa Clara, CA, USA) equipped with dual columns and a thermal conductivity detector. Carbon dioxide was analysed Cefola et al. ‐ Response of fruit and vegetable to different CO2 levels in MAP 69 with a retention time of 16 s and a total run time of 120 s on a 10 m porous polymer (PPU) column (Agilent, Santa Clara, CA, USA) at a constant tempera­ ture of 70°C. RR was expressed as mL CO2 kg ­1 h­1. In table grapes, rB was scored on a rating scale from 1 to 5 (1= absence, 2= light; 3= moderate; 4= severe; 5= extreme) as reported by Lichter et al. (2011), whereas for acetaldehyde and ethanol analysis, the procedure reported by Cefola et al. (2018) was used. In sweet cherries, the RWC of peduncles was cal­ culated in percentage, as reported by Cefola et al. (2018), while the VOCs analysis was carried out, as reported by Cozzolino et al. (2019). In fresh­cut artichokes, BI and VOCs were evalua­ ted, as reported by Capotorto et al. (2020). 3. Results and Discussion Starting from the gas composition inside MA pack­ ages described above for each product, during stor­ age the concentrations of O2 and CO2 changed due to the respiration of the products and gas permeation through packaging material, and the final gases com­ position were reported in Table 1. As for table grapes, O2 concentrations decreased from 1 kPa to about 0.2 kPa or 0.3 kPa, in 1k Pa­O2 and in 1 kPa­O2 + 20 kPa­CO2 respectively, while CO2 concentrations increased from 0.03 kPa to roughly 10 kPa in 1 kPa­O2 packages, and from 20 kPa to about 30 kPa in 1k Pa­O2 + 20 kPa­CO2 MA. For sweet cherries, in 16 kPa­O2 + 20 kPa­CO2 bags, the O2 concentration gradually decreased, reaching the mean value of about 1 kPa after 21 days of storage. In 1 kPa­O2 and 1 kPa­O2 + 20 kPa­CO2 samples, the initial O 2 concentration remained unchanged during the storage. On the other hand, the amount of CO2 increased during conservation, reaching the final mean values of 25.7 kPa, 45.3 kPa and 42.4 kPa in 1 kPa­O2, 16 kPa­O2 + 20 kPa­CO2 and 1 kPa­O2 + 20 kPa­CO2 packages, respectively. Finally, as for fresh­cut artichokes, no significant changes in gas composition inside bags were observed. Results on table grapes are reported in Table 2. In the Fresh samples the RR measured was equal to 4.2 (± 0.4) mL CO2 kg ­1 h­1; after 20 days of the storage, a reduction in RR was measured in air samples (3.0 ± 0.2 mL CO2 kg ­1 h­1), while it remained almost con­ stant in table grapes samples treated with 1 KPa O2 (4.7 ± 0.6 mL CO2 kg ­1 h­1). On the contrary the use of high CO2 concentrations (>20 kPa) in the MA mixture (1 kPa­O2 + 20 kPa­CO2) increased the value of RR resulting more than a 2­fold higher than Fresh sam­ ple. Significant differences were observed, for sample stored in air and 1 kPa­O2 + 20 kPa­CO2 (Table 2). As shown in Table 1, browning of the table grapes rachis was found in all treatments after 20 days of storage. However, higher browning was observed in air and in 1 kPa­O2 + 20 kPa­CO2 samples, whereas the use of 1 kPa­O2 was able to keep a light to moderate brown­ ing of the rachis (mean value of 2.5). After storage ethanol and acetaldehyde concentrations did not change from their initial values (4.2 and 0.6 mg L­1, respectively) in the Air samples, whereas they signifi­ cantly increased in table grapes exposed to low (<10 kPa) or high CO2 (>20 kPa) concentrations (Table 2). Moreover, samples exposed to 1 kPa­O2 + 20 kPa­CO2 s h o w e d h i g h e r a c c u m u l a ti o n s o f e t h a n o l a n d acetaldehyde than table grapes packed in 1 kPa­O2. Treatment Initial kPa Final kPa O2 CO2 O2 CO2 1 kPa­O2 1.0 0.04 0.2 10.0 1 kPa­O2 + 20 kPa­CO2 1.0 20.0 0.3 30.0 Air 20.0 0.03 20.0 0.03 Table 1 ­ Initial and final concentration of O2 and CO2 for each treatment on table grape Treatment Respiration rate (mL CO2 kg ­1 h­1) Rachis browning (1­5) Ethanol (mg L­1) Acetaldhyde Fresh 4.2 b 1.0 c 4.2 c 0.6 c 1 kPa­O2 4.7 b 2.5 b 2142 b 8.9 b 1 kPa­O2 + 20kPa­CO2 9.0 a 3.6 a 3606 a 17.6 a Air 3.0 c 4.4 a 5.8 c 0.6 c Table 2 ­ Effect of CO2 treatments on respiration rate, rachis browning, ethanol and acetaldehyde contents of table grapes (Vitis vinifera cv. Italia) after 20 days of storage at 5°C Mean values followed by different uppercase and lowercase letters indicate significant differences between fresh and treated sample, and within treatments at day 20, respectively, according to LSD test (P≤0.05). Adv. Hort. Sci., 2023 37(1): 67­73 70 Sweet cherries (Table 3) showed an initial respira­ tion rate of 8.2 (± 0.3) mL CO2 kg ­1 h­1 which increased 1.5 fold in air and more than 5 times in the other MA treatments. The highest RR was observed in 1 kPa­O2 + 20 kPa­CO2 (48.9 ± 0.7 mL CO2 kg ­1 h­1) followed by 16 kPa­O2 + 20 kPa­CO2 (44.4 ± 0.6 mL CO2 kg ­1 h­1) and 1 kPa­O2 (43.2 ± 0.1 mL CO2 kg ­1 h­1). The RWC % of peduncle increased in all MA treat­ ments, maybe due to the high relative humidity inside the packages. The highest RWC % values were observed in low O2 treatments, probably thanks to the lower respiration rate of these samples. Among VOCs analysed, 1­pentanol, marker of sen­ sory alteration, was closely associated with negative aroma intensity which resulted directly described as pungent, and fermented flavour. Whereas the reduc­ tion of hexenal and 2­hexenal were indicators of lost in freshness (Cozzolino et al., 2019). As reported in Table 2, 1­pentanol was not detect­ ed in Fresh and Air samples, while a significant increase of this alcohol was observed in the other MA treatments. Samples treated with 1 kPa­O2 + 20 kPa­CO2 had the highest value of 1­pentanol, while 1 kPa­O2 and 16 kPa­O2 + 20kPa­CO2 MA treatments had similar values (Table 2). As for hexanal, (Table 3) statistical analysis did not show significant changes after 21 days at 5°C excepted for the treatment, 1 kPa­O2 + 20 kPA­CO2 which showed a reduction with respect to the fresh sample. In contrast, 2­hexenal decreased significantly during storage, but no differ­ ences in its concentration were observed when com­ paring MA treatments (Table 3). Results of fresh­cut artichokes are reported in Table 4. RR of the fresh sample was 120.8 (± 0.2) mL CO2 kg ­1 h­1. After the short­term CO2 treatments (48 h, 0°C) and 7 days of storage at 5°C, RR decreased significantly in all samples, except in artichokes treat­ ed with 40 kPa of CO2. The lowest RR was detected in fresh­cut artichokes treated with CO2­10 kPa (44.5 ± 4.3 mL CO2 kg ­1 h­1), followed by CO2­20 kPa and CO2­ 30 kPa, which reported similar values (68.1 ± 1.1 and 63.9 ± 5.2 mL CO2 kg ­1 h­1, respectively), and Air (93.6 Table 3 ­ Effect of CO2 treatments on respiration rate, relative water content (RWC) of peduncles, 1­pentanol, hexanal and 2­hexenal relative peak area (RPA) contents of sweet cherries (Prunus avium cv. Ferrovia) after 21 days of storage at 5°C Mean values followed by different uppercase and lowercase letters indicate significant differences between fresh and treated sample, and within treatments at day 21, respectively, according to LSD test (P≤0.05). Table 4 ­ Effect of short­term CO2 treatments on respiration rate, browning index, ethanol and hexanal relative peak area (RPA) con­ tents of fresh­cut artichokes (Cynara cardunculus cv. Violet de Provence) after 7 days of storage at 5°C Mean values followed by different uppercase and lowercase letters indicate significant differences between fresh and treated sample, and within treatments at day 7, respectively, according to LSD test (P≤0.05). Treatment Respiration rate (mL CO2 kg ­1 h­1) Relative water content of peduncles (%) 1­Pentanol relative peak area (%) Hexanal 2­Hexenal Fresh 8.2 B 53.9 B 0.0 B 112.3 NS 366.6 A 1kPa­O2 43.2 Ac 65.4 Aa 6.0 Ab 47.3 NS a 118.0 B NS 16kPa­O2 + 20kPa­CO2 44.4 Ab 58 Ab 7.6 Ab 26.4 NS ab 99.9 B NS 1kPa­O2 + 20kPa­CO2 48.9 Aa 60.5 Ab 18.6 Aa 14.3 Bb 55.7 B NS Air 12.1 Ad 53.6 NS c 0.0 NS c 40.5 NS ab 125.2 B NS Treatment Respiration rate (mL CO2 kg ­1 h­1) Browning index Ethanol relative peak area (%) Hexanal Fresh 120.8 A 0.0 B 34.5 NS 41.7 NS CO2­10 kPa 44.5 Bd 131 Ad 114.0 NS c 5.4 NS a CO2­20 kPa 68.1 Bc 137 Abc 379.1 Ab 5.0 NS a CO2­30 kPa 63.9 Bc 135 Acd 482.5 Ab 4.3 NS a CO2­40 kPa 121.5 Aa 140 Ab 363.5 Ab 2.1 Bb Air 93.6 Bb 152 Aa 886.3 Aa 3.8 NS a Cefola et al. ‐ Response of fruit and vegetable to different CO2 levels in MAP 71 ± 1.7 mL CO2 kg ­1 h­1), while the highest RR was observed in CO2­40 kPa (121.5 ± 0.2 mL CO2 kg ­1 h­1). As expected, all samples developed browning after 7 days of storage, regardless of treatment. However, d i ff e r e n c e s i n t h e s e v e r i t y o f b r o w n i n g w e r e observed when comparing treatments at the end of the storage: the application of short­term CO2 treat­ ments (from 10 kPa to 40 kPa) significantly reduced the incidence of browning compared to Air samples and, among the CO2 treatments, CO2­10 kPa had the lowest browning index (Table 4). Considering all the VOCs identified by HS ­SPME/GC­MS analysis, ethanol and hexenal were, respectively, the most representative compounds of negative and positive aspects of fresh­cut artichokes (Capotorto et al., 2020). A s s h o w n i n T a b l e 4 , e t h a n o l s i g n i fi c a n t l y increased during storage, except for the CO2­10kPa treatment, where its concentration was similar to that of fresh samples. The highest ethanol concentra­ tion was found in Air samples, followed by treat­ ments added with CO2 at 20, 30, and 40 kPa that showed similar values. As for hexanal, it was signifi­ cantly lower only in fresh­cut artichokes treated with CO2­40 kPa (Table 4). For table grapes, data related to ethanol and acetaldehyde, together with the RR results, indicate that high CO2 concentrations (>20 kPa) on this com­ modity may cause physiological injury and the induc­ tion of anaerobic metabolism. The present results are supported by similar find­ ings on the effect of high CO2 concentrations (>20 kPa) on table grapes by Cefola and Pace (2016). High CO2 concentrations also negatively influence the acceptability of table grapes by consumers: rachis browning, is, in fact, the main issue that limits the acceptability of table grapes by consumers (Cefola et al., 2018). A similar effect of high CO2 concentrations (>20 kPa) on the acceleration of rachis browning was previously observed on table grapes (Crisosto et al., 2002; Deng et al., 2006) and is a consequence of the stress induced by exposure to high CO2 concentra­ tions (Crisosto et al., 2002; Liguori et al., 2015). For sweet cherries, considering that the highest RR was observed when MA with 20kPa CO2 was applied, these results indicate that this CO2 concen­ tration, especially when associated with low oxygen, can cause stress, as confirmed by VOC analysis. Similar behaviour in the production of C5 volatiles, s u c h a s 1 ­ p e n t a n o l , w a s p r e v i o u s l y o b s e r v e d (Contreras et al., 2017; Mastrandrea et al., 2017), and it seems to be favoured under low O2 and high CO2 atmospheres. The present results on the cv. Ferrovia are in contrast with previous results on other sweet cherries cultivars (Kader et al., 1989; Esturk et al., 2012), but those cultivars have better tolerance to high CO2. It has been stated that the physiological suscepti­ bility of commodities to high CO2 can be cultivar­ dependent, and is generally seen with vegetables and other fruit (Watkins, 2000). Results on fresh­cut artichokes indicate that the application of high CO2 concentrations (around 40 kPa) has a negative effect on the shelf­life. Similar results on the detrimental effect of high CO2 were previously observed on fresh­cut arti­ chokes during storage (La Zazzera et al., 2012, 2015). As observed for table grapes, sweet cherries, and fresh­cut artichokes, the exposure to elevated CO2 atmospheres can stimulate respiration and ethylene production rates, indicating a stress response (Kader, 2002 a). These increases in respiration might be related to the inhibition by high CO 2 of several enzymes of the Krebs cycle, including succinate dehydrogenase, which triggers anaerobic respiration or causes the accumulation of succinic acid, which is potentially toxic to cells (Kays, 1991; Varoquaux, 1991; Kader, 2002 b). Furthermore, for fresh­cut arti­ chokes, the intolerance to high CO2 concentration and mechanical wounding enhances a different array of enzymatic pathways, many of which are associat­ ed with volatile accumulation, which lead to devel­ opment of off­flavors (Salunkhe et al., 1976; La Zazzera et al., 2015). 4. Conclusions For table grapes, the storage in high CO2 (>20 kPa) caused a severe increase in respiration rate, ethanol and acetaldehyde accumulation, and a decline in sen­ sory quality due to the rachis browning, all probably consequences of the induction of the anaerobic metabolism. The application of CO2 up to 10kPa was able, instead, to keep the good quality table grapes during storage. Sweet cherry (cv. Ferrovia) is very sensitive to high CO2 when it is applied together with low oxygen in MA, as indicated by responses in respiration rate, rel­ ative water content of the peduncles, and VOC emis­ sions, with some of these responses being considered positive and some negative in relation to quality. 72 Adv. Hort. Sci., 2023 37(1): 67­73 Short­term treatment with high CO2 (around 40 kPa) caused an increase in respiration rate and the induction of fermentative metabolism in fresh­cut artichoke. The application of CO2 concentrations up to 10 kPa reduced respiration rate and tissue brown­ ing during storage in air at 5°C and preserved the fresh VOC profile. Application of short­term CO2 might be a promising postharvest treatment to pre­ serve the quality and the volatile profile of fresh­cut artichokes during storage. 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