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Health-PromotingCompoundsinCape

gooseberry(PhysalisPeruvianaL.):Review

fromasupplychainperspective

ArticleinTrendsinFoodScience&Technology·September2016

DOI:10.1016/j.tifs.2016.09.009

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Review

Health-promoting compounds in cape gooseberry (Physalis peruvianaL.): Review from a supply chain perspective

Mary-Luz Olivares-Tenorio a, b, *, Matthijs Dekker a, Ruud Verkerk a,Martinus A.J.S. van Boekel aa Wageningen University, Food Quality and Design Group, The Netherlandsb Fundaci!on Universitaria Agraria de Colombia, UNIAGRARIA, Colombia

a r t i c l e i n f o

Article history:Received 20 July 2016Received in revised form5 September 2016Accepted 19 September 2016Available online 21 September 2016

Keywords:Antioxidant activityb-caroteneFlavonoidsPhenolic compoundsPhytochemicalsSupply chainVitamin C

a b s t r a c t

Background: The fruit of Physalis peruviana L., known as Cape Gooseberry (CG) is a source of a variety ofcompounds with potential health benefits. Therefore, CG has been subject of scientific and commercialinterest.Scope and approach: This review paper evaluates changes of such health-promoting compounds andantioxidant activity in CG, based on published literature and from a supply chain perspective, consideringpre-harvest, post-harvest, processing (thermal and not thermal) and storage steps to give an insight ofcontents at consumption stage.Key findings and conclusions: CG has vitamin C (20 and 35 mg 100 g!1 FW), b-carotene (up to2.0 mg.100 g!1 FW), total phenolic compounds TPC (50e250 gallic acid equivalents.100 g!1 FW),phenolic acids (caffeic, gallic, chlorogenic, ferulic and p-cumaric acids), flavonoids (quercetin, rutin,myricetin, kaempferol, catechin and epicatechin) and antioxidant activity. There is not yet evidence ofpresence of physalins and withanolides in CG as previous review papers have stated. The ripeness stageof CG is a relevant factor affecting the content of many phytochemicals. Vitamin C and b-carotenecontents are directly proportional to ripeness stage. The reported data in literature showed a largevariation, likely caused by different raw material properties (origin, ripeness stage, growing conditionsetc.) and differences in the employed analytical methods. Thermal and non-thermal processing have aneffect on the extractability of the phytochemicals but also on the decrease of compounds and antioxidantactivity. Relative stability to certain phytochemicals to processing suggest an opportunity to add value tosupply chain with processed food containing health-promoting compounds.

© 2016 Elsevier Ltd. All rights reserved.

1. Introduction

Cape gooseberry (CG), also known as goldenberry, is the fruit ofthe plant Physalis peruviana L. that belongs to Solanaceae familyand genus Physalis. This plant is native from the Andean Region andis cultivated currently in South American countries, especiallyColombia, Peru and Ecuador. CG is a fruit with approximately1.25e2.50 cm of diameter, 4e10 g of weight, orange yellow skin andjuicy pulp containing numerous small yellowish seeds (Fischer,1995).

Consumption of fruits and vegetables is inversely associated tothe risk of cardiovascular (CVD), respiratory and digestive diseasesand certain cancers (Hjartåker, Knudsen, Tretli, & Weiderpass,2015; Leenders et al., 2014). Although, other studies did not findthese associations (Norat, Aune, Chan, & Romaguera, 2014), theincrease of fruit and vegetable consumption is advisable (Terry,Terry, & Wolk, 2001). Anti-tumour, anti-diabetic, anti-inflammatory, anti-hypertension activities and cardio-protectiveeffects have been associated with the consumption of berry fruitssuch as strawberries, blueberries, blackberries, raspberries andcranberries (Hjartåker et al., 2015; Mursu, Virtanen, Tuomainen,Nurmi, & Voutilainen, 2014) and have also been related to theplant Physalis peruviana (leaf and stems) and CG (Abdel Moneimet al., 2014; Areiza-Mazo, Maldonado, & Rojano, 2013; Da SilvaPinto et al., 2009; Osman, AL-seeni, Alkhatib, & Al-shreef, 2013;

* Corresponding author. Wageningen University, Food Quality and Design Group,Bornse Weilanden 9, 6708WG, Wageningen, The Netherlands; UNIAGRARIA, Pro-grama Ingeniería de Alimentos Calle 170 No. 54A - 10 Bogot!a, Colombia.

E-mail addresses: maryluz.olivarestenorio@wur.nl, maryluzolivares@hotmail.com (M.-L. Olivares-Tenorio).

Contents lists available at ScienceDirect

Trends in Food Science & Technologyjournal homepage: http: / /www.journals .e lsevier .com/trends- in- food-science-

and-technology

http://dx.doi.org/10.1016/j.tifs.2016.09.0090924-2244/© 2016 Elsevier Ltd. All rights reserved.

Trends in Food Science & Technology 57 (2016) 83e92

Rodríguez & Rodríguez, 2007; Yen et al., 2010). The associations tohealth benefits are related to the content of phytochemicals such asvitamins, minerals, phenolic compounds, withanolides and phys-alins. Nevertheless, knowledge about health protective mecha-nisms is limited.

This review gives an overview of the state of art of changes ofhealth-promoting compounds of CG in a supply chain perspective,evaluating pre-harvest, post-harvest, processing and storage steps,giving an insight of compounds content at consumption stage(fresh and processed) and identifying knowledge gaps. Theobserved high variation in the reported data will be discussed,including the discrepancies and uncertainties in analytical methodsthat were used for the determination of the compounds.

2. Cape gooseberry supply chain

CG is the most exported tropical fruit in Colombia, after banana(Agronet, 2016), while the main CG market is the European Union,especially the Netherlands, followed by Belgium and Germany(Agronet, 2016). Although most of the fruit is exported as freshfruit, the physical and chemical characteristics of CG make it asuitable raw material for numerous products such as juices, jam,pulp, desserts, dried fruit, etc (MADR, UNAL, & CORPOICA, 2009;Rabie, Soliman, Diaconeasa, & Constantin, 2015; Ramadan &Moersel, 2007). which are currently available in the domestic andinternational markets. The Colombian CG supply chain essentiallyinvolves 4 main stages: production, processing, distribution/mar-keting and consumption (Olivares-Tenorio, Linnemann, Pascucci,Verkerk, & van Boekel, 2014).

A supply chain approach in food quality is important to guar-antee safety and quality from farm to table (consumption). Nowa-days, consumers are increasingly interested about what they eat interms of nutritional and health promoting properties. Actors inagri-food supply chains should not make unsubstantiated healthclaims that can mislead consumers, but provide accurate infor-mation about the nutritional and health-promoting compounds inproducts (Ponte & Gibbon, 2005). A report from the Colombiangovernment has stated the need to have information about health-promoting compounds in CG, not only in the fruit after harvesting,but also at consumption stage (fresh or processed) (MADR et al.,2009). For the purpose of this review and what is reported inliterature, the CG supply chain evaluation has been focused on pre-harvest, post-harvest, processing and storage. In the CG supplychain, like in any other agri-food supply chain, several factors affectthe content of health-promoting compounds, such as the varietiesof fruits, cultivation conditions, harvest time, storage, processingand consumer processing (Dekker, Verkerk, & Jongen, 2000). Ananalysis of these factors on compounds in CG will be discussedbased on published data.

3. Pre- harvest and post-harvest

3.1. Vitamin C

Vitamin C is the most abundant water-soluble antioxidant in thebody. This nutrient is associated to the protection against cancerand CVC diseases, and to the beneficial effects on immune functions(Grosso et al., 2013). The theoretical mechanisms related to thosebenefits are essentially, the scavenging activity against free radicalsand reactive oxygen species, the role in promoting collagen for-mation in the body, the inhibition of formation of N-nitroso com-pounds (carcinogenic nitrosamines), the participation ascosubstrate in catecholamine and carnitine biosynthesis and theprotection of low density lipoprotein (LDL) cholesterol againstoxidation (Grosso et al., 2013).

Comparing various studies, a very high variation of data isobserved, which is illustrated in Fig. 1 amounting up to 50-folddifferences, ranging from of 18e929 mg 100 g!1 FW (freshweight) of vitamin C.

The variation of vitamin C content can be caused by the usedanalytical methods. Titration method and HPLC are frequently usedmethods in reported studies. Titration is known to lack sensitivityand can lead to an overestimation of vitamin C content (Brause,Woollard, & Indyk, 2003; Odriozola-Serrano, Hern!andez-Jover, &Martín-Belloso, 2007). Besides, differences in extraction proceduresmight cause variability in both, titration and HPLC methods(Hern!andez, Lobo, & Gonz!alez, 2006). Barcia, Jacques, Pertuzatti,and Zambiazi (2010) probably overestimated the content ofvitamin C with an amount of 929 mg 100 g!1 FW. Overestimationcan be caused by a failure to separate interferences from theascorbic acid peak in HPLC (Tarrago-Trani, Phillips, & Cotty, 2012).

Another cause of variation of vitamin C content can be thedifferent varieties/cultivars/ecotypes used in cultivation. Due to thefact that information on cultivars is often missing in literature, theeffect of them on vitamin C remains unclear. Differences in vitaminC content where found in cultivars from South Africa, Giant, Inkaand Golden Berry (Rop, Mlcek, Jurikova, & Valsikova, 2012), but forthree ecotypes Colombia, Kenya and South Africa there were nosignificant differences (Fischer, Ebert, & Ludders, 2000). Reportedstudies on vitamin C in CG from Ecuador, Peru and Argentina arenot comparable due to difference in experimental conditions orlack of reported information (Novoa, Bojac!a, Galvis, & Fischer,2006; Rop et al., 2012; Valdenegro, 2013; Valdenegro, Fuentes,Herrera, & Moya-Le!on, 2012). Location of cultivation might meanother cause of variation in results. Nevertheless, studies on CGfrom different countries (South American countries, Egypt, Ger-many and Czech Republic) were not comparable because of the lackof detailed information about cultivation conditions. The altitude ofcultivation did not have a significant effect on vitamin C content inCG (Fischer et al., 2000). During post-harvest, presence of the calyxallowed the vitamin C stability (Valdenegro et al., 2012).

An estimation of ripening stages was attempted to be able tocompare results, using standard NTC 4580 (ICONTEC., 1999). Thisstandard classifies ripeness stage, according to colour, measuredvisually; "Brix, measured by refractometry and acidity, reported as% acid citric and measured by titration with a scale from 0 to 6,where 6 is the highest ripeness stage (ICONTEC., 1999). In Fig. 2,normalized data of vitamin C contents have been plotted as afunction of ripeness stage. Only studies evaluating vitamin C invarious ripeness stages were included.

Some studies indicated a directly proportional association ofvitamin C to ripeness stage (Gutierrez, Trinchero, Cerri, Vilella, &Sozzi, 2008; Repo de Carrasco & Encina, 2008; Valdenegro et al.,2012). Normalized data showed significant differences betweenmeans of vitamin C at the 6 stages (P < 0.05). Ascorbic acid canincrease because of biochemical synthesis during the ripeningprocess (Repo de Carrasco & Encina, 2008) as has been reported fortomatoes, peppers and guava (Gomez & Lajolo, 2008; Navarro,Flores, Garrido, & Martinez, 2006; Raffo et al., 2002).

CG at the edible ripening stages (4e6) contains between 20 and50 mg 100 g!1 FW of vitamin C. Therefore, CG is a good source ofvitamin C compared with other common sources, such as mango(15e36mg 100 g!1 FW), comparable to orange (50mg 100 g!1 FW),but less than guava (120e228 mg 100 g!1 FW) or marula(120 mg 100 g!1 FW) (Gomez & Lajolo, 2008; Hiwilepo-van Hal,Bosschaart, van Twisk, Verkerk, & Dekker, 2012; Sogi, Siddiq, Roi-doung, & Dolan, 2012; USDA., 2014). Following internationalnutritional recommendations, the daily intake of vitamin C shouldbe between 15 and 90 mg per day (depending on gender and age),thus, to comply this consumptionwith only CG as vitamin C source,

M.-L. Olivares-Tenorio et al. / Trends in Food Science & Technology 57 (2016) 83e9284

approximately 200 g (approx. 20e50 berries) should be eaten (CEC.,1993; Johnston, 2012; USDA & HSS, 2010).

3.2. Total phenolic compounds

Phenolic compounds form a group of secondary metaboliteswidely occurring in plants. These compounds may play a role in theinhibition carcinogenesis by affecting the molecular events in theinitiation, promotion, and progression stages, especially, thanks totheir antioxidant capacity. However, precision of the mechanisminvolved are still unclear (Vald!es et al., 2015). There are four maingroups of phenolic compounds: phenolic acids, flavonoids, stil-benes, and lignans (Balasundram, Sundram, & Samman, 2006).

Total Phenolic Compounds (TPC) contents in CG and similarspecies have been reported showing a wide range of2.5e934.9 mg 100 g!1 FW, usually expressed as gallic acid equiv-alents. This large variation is illustrated in Fig. 3.

The large variation of TPC contents might be caused by thedifferent use of varieties/cultivars/ecotypes (K. Bravo, Sepulveda-Ortega, Lara-Guzman, Navas-Arboleda, & Osorio, 2015; Rop et al.,2012). Maturity stages show higher phenolic compound contentswhen the fruit was still in the plant (Bravo et al., 2015; Mier& C!aez,

2011; Narv!aez-Cuenca, Mateus-G!omez, & Restrepo-S!anchez, 2014;Severo et al., 2010; Valdenegro et al., 2012). So far, there is not morepublished information about TPC content of CG during pre-harvestand post-harvest. Variation of TPC content also can be due tomethod of analysis. Folin ciocalteau is themost widely usedmethod.Nevertheless, there are variations in type of extraction solvent,extraction conditions, reaction time, standards used and wave-length. Studies reported low contents of TPC when no extractionwas performed (Ramadan & Moersel, 2007; Valdenegro et al.,2012). TPC can also be underestimated when they are in boundforms because usually they are excluded from analysis(Balasundram et al., 2006). From data reported for CG, gallic acid isthe most common standard used to quantify phenolic compoundsand differences can arise when the standard used is caffeic acid (orother). Gallic acid can be less reactive to folin ciocalteau than caffeicacid, giving lower absorbance and affecting final results (Stratil,Klejdus, & Kub!an, 2006).

In Fig. 4, TPC contents have been plotted in relation to ripenessstages of the fruit according to NTC 4580 (ICONTEC., 1999), usingthe same criteria as in Section 3.1.

In Fig. 4, there are discrepancies in the trend of TPC duringripening and changes of normalized data are not significant(P > 0.05). Contradictory results in Figs. 3 and 4, do not allowidentifying the trend of TPC during maturity and ripening in CG.

TPC contents of CG at edible ripening stage (50e250 gallic acidequivalents.100 g!1 FW) are higher than what is reported formango (56e193 gallic acid equivalents.100 g!1 FW) pineapple (94.3gallic acid equivalents.100 g!1 FW) and banana (11.8e90.4 gallicacid equivalents.100 g!1 FW); similar to other fruits such asstrawberry (160 gallic acid equivalents.100 g!1 FW), raspberry(114e178 gallic acid equivalents.100 g!1 FW), plums (174e375gallic acid equivalents.100 g!1 FW) and cherry (105.4 ± 27.0 gallicacid equivalents.100 g!1 FW) (Balasundram et al., 2006); but lowerthan what is reported in blackberry (417e555 gallic acidequivalents.100 g!1 FW) (Balasundram et al., 2006; Ma et al., 2011;Vasco, Ruales, & Kamal-Eldin, 2008).

3.2.1. Phenolic acids and flavonoidsPhenolic acids are believed to participate in the inhibition of

tumour promotion and progression, therefore, they might be effi-cient preventing cancer in humans rather than helping in carcin-ogen treatment. However, mechanisms are still unclear.

Flavonoids are well-known to be able to scavenge a wide range

Fig. 1. Histogram of Vitamin C values reported in literature for CG (Physalis peruviana L).

Fig. 2. Normalized data of vitamin C and b-carotene contents in CG (Physalis peruvianaL) for ripeness stages (according to NTC 4580, 1999). Verticals bars represent standarddeviations of estimated means (n ¼ 3e4). Data sources: Bravo et al., 2015; Fischer &Martínez, 1999; Gutierrez et al., 2008; Mier & C!aez, 2011; Repo de Carrasco &Encina, 2008; Severo et al., 2010; Valdenegro et al., 2012.

M.-L. Olivares-Tenorio et al. / Trends in Food Science & Technology 57 (2016) 83e92 85

of reactive oxygen, nitrogen, and chlorine species, such as super-oxide, hydroxyl radical, peroxyl radicals, hypochlorous acid, andperoxynitrous acid. They can also chelate metal ions, oftendecreasing metal ion prooxidant activity, contributing with theprevention of major age-related diseases (Del Rio et al., 2013).

Main phenolic acids identified in CG are caffeic, chlorogenic,ferulic, p-coumaric and gallic acids (Mier, 2012; Mu~noz-J!auregui,Ramos-Escudero, & Fernando, 2007; Namiesnik et al., 2014; Rock-enbach et al., 2009; Vega-G!alvez, L!opez et al., 2014; Vega-G!alvez,Puente-Díaz et al., 2014). However, there is not agreement in con-tents, probably due to differences in method of analysis. Main fla-vonoids identified and quantified in CG are quercetin(0.1e10.9 mg Kg!1), rutin (1.7e6.7 mg Kg!1), myricetin(1.1e1.3 mg Kg!1), epicatechin (0.2e0.6 mg Kg!1), and catechin(3.8e6.7 mg Kg!1). Morine was not detected (Licodiedoff, Andr!e,Koslowski, & Ribani, 2013; Licodiedoff, Koslowski, & Ribani, 2013;Mier, 2012; Mu~noz-J!auregui et al., 2007; Namiesnik et al., 2014;Pillai & Sathyadevi, 2015). In hydrolysed CG extracts, rutin(78.64 mg L!1), myricetin (4.67 mg L!1) and kaempferol(2.38 mg L!1) were found (Licodiedoff, Andr!e et al., 2013;

Licodiedoff, Koslowski et al.,2013). Rutin is unexpected becausethis is a glycoside of quercetin, thus it should be gone after hy-drolysis. Contents of quercetin hereby reported are lower than inother berries and myricetin and kaempferol are present in CG,while they were not detected in other berries (H€akkinen,K€arenlampi, Heinonen, Mykk€anen, & T€orr€onen, 1999). The totalflavonoid content assessed with a colorimetric assay was of 487 mgcatechin equivalent.100 g!1 DW (dried weight) of extract (Areiza-Mazo et al., 2013) and 241 mg g!1 DW of fruit (Pillai &Sathyadevi, 2015). Differences in analytical procedures and sam-ples conditions give variation in reported results. Thus, there is aremaining knowledge gap about what are the most importantphenolic acids and flavonoids in CG. Several studies reported fla-vonoids in Physalis peruviana L. leaves; however, they do not belongto the scope of this review.

3.3. Carotenoids

Carotenoids are convertible to vitamin A (approx. 10%) byenzymatic cleavage in the body. Thus carotenoids are believed to

Fig. 3. Histogram of Total Phenolic Compounds TPC values reported in literature for CG (Physalis peruviana L).

Fig. 4. Total phenolic compounds TPC in CG (Physalis peruviana L) for ripeness stages (according to NTC 4580, 1999).

M.-L. Olivares-Tenorio et al. / Trends in Food Science & Technology 57 (2016) 83e9286

participate in cancer prevention because of their provitamin A ac-tivity, since this is essential for the normal maintenance epithelialcellular differentiation (Fiedor & Burda, 2014). b-carotene is aquencher of singlet oxygen and also can inhibit lipid peroxidation.However, beta-carotene is a relatively weak antioxidant. (Fiedor &Burda, 2014).

The most important carotenoid in CG is b-carotene beingresponsible of the yellow orange colour (Fischer et al., 2000). Largevariation is observed in reported data ranging from 0.2 to1074.7 mg b-carotene.100 g!1 FW, which is illustrated in Fig. 5.

The variation causes are different varieties/cultivars/ecotypes,cultivation conditions, and ripeness stage as explained for previouscompounds. b-carotene content can vary depending on chosenmethods for extraction and analysis (Machmudah & Goto, 2013).Unfortunately, sometimes authors use incorrect extinction co-efficients in their calculation of carotenoids contents. Besides, ca-rotenoids are sensitive to light, heat, air (oxygen), and activesurfaces (with biological activity) (Scott, 2001), thus apart of takingprecautions during extraction and analysis; the standard used needsto be checked to evaluate actual purity and avoid miscalculation ofcontents. Nevertheless, references evaluated in this review do notprovide information about this evaluation. Fig. 2 represents thenormalize data of contents of carotenoids or b-carotene in differentripeness stages according to NTC 4580, as explained in Section 3.1.

There is an increase of b-carotene content with ripeness in somestudies (K. Bravo et al., 2015; Mier& C!aez, 2011; Severo et al., 2010).Normalized data showed significant differences of b-carotene be-tween ripeness stages (P < 0.05). The increase is expected inaccordancewith the development of the colour with ripening (fromgreen to orange), which is found with NTC 4580 and in otherstudies (Fischer & Martínez, 1999; Fischer, 1995; ICONTEC., 1999).Methods of analyses did not have significant differences (P > 0.05).

From the results evaluated in this review, the concentration of b-carotene in fresh and ripen (stage 5e6) CG is $ 2.0 mg.100 g!1 FW,despite the substantial variation of data previously mentioned.USDA database reports as the most important sources of b-caro-tene, the sweet potato and carrot with 8.3e8.5 mg 100 g!1 FW.Within fruits group, the highest contents of b-carotene are in rawmelonwith 2.0 mg 100 g!1 FWand apricot with 1.1 mg 100 g!1 FW(USDA., 2014). CG is not included in the USDA database, however,

Briones-Labarca, Giovagnoli-Vicu~na, Figueroa-Alvarez, Quispe-Fuentes, and P!erez-Won (2013) reported a content of1075 mg 100 g!1 FW b-carotene, thus this value could be anoverestimation or misreport. There is no specific recommendedintake for b-carotene but there is for the REA (retinol activityequivalents) which is 400e950 mg/day (USDA & HSS, 2010). Theratio of conversion of the b-carotene obtained from a foodmatrix tovitamin A in oil is 12:1 (Lindshield, 2012). Therefore, a diet with5e10 mg (depending on age and gender) of b-carotene would berecommended per day. That means that a portion of 50 g of CG(10e15 berries) could provide 10e20% of the recommended dailyintake of vitamin A.

3.4. Vitamins E and B3 and B6

As carotenoids, vitamin E (tocopherol) is a fat-soluble com-pound. The mechanisms involved in the health promotion are, asvitamin C, the inhibition of the formation of N-nitroso compoundsin the stomach, the protection of selenium against reduction andpolyunsaturated fatty acids in lipid membranes from oxidativedamage. Vitamin E is thought to be the most important antioxidantfound within lipid membranes in the body (Mocchegiani et al.,2014).

In CG, there is not consensus about tocopherol content. Totaltocopherol of 1.5 mg g!1 of fruit was reported (Barcia et al., 2010)and considering that 2% of the fruit is the lipid part (Ramadan &M€orsel, 2003). This amount is equivalent to 7.5 mg 100 g!1 lipidpart. However, total tocopherols (including aþbþgþd) was re-ported to be 32.7 g Kg!1 lipid part, corresponding to3270 mg 100 g!1 lipid part, being extremely higher (Ramadan &M€orsel, 2003). Restrepo, Cort!es, and M!arquez (2009) consideredthe content of vitamin E in CG as negligible, while Vega-G!alvez et al.(2016) reported an amount of 10.70 ± 0.28 g kg!1

(1070mg 100 g!1) of a-tocopherol in the lipid portion of CG fruit. d-tocopherol was not detected in CG (Vega-G!alvez et al., 2016). b-tocopherol and g-tocopherol were the major components in wholeberry and seed oils, whereas detocopherol and a-tocopherol werethe main constituents in pulp and skin oil. The amounts of to-copherols in pulp oil found were (g kg!1): a-tocopherol 28.3 ± 0.45,b-tocopherol 15.2 ± 0.85, g -tocopherol 45.5 ± 2.35, d -tocopherol

Fig. 5. Histogram of b-carotene values reported in literature for CG (Physalis peruviana L).

M.-L. Olivares-Tenorio et al. / Trends in Food Science & Technology 57 (2016) 83e92 87

1.50 ± 0.05 (Ramadan & Moersel, 2007), corresponding to a totaltocopherol of 90.5 g kg!1 (9050 mg.100 g!1). These values are sohigh in comparison to what is reported by USDA database,where the source with highest amount of vitamin E (a-tocopherol)is wheat germ oil with 149.4 mg 100 g!1 (USDA., 2015). Thesediscrepancies do not allow to draw conclusions about vitamin E inCG.

Vitamin B6 (pyridoxine) and B3 (niacin) help the body convertcarbohydrates to produce energy, help in the metabolism offats and proteins and also help to regulate the nervous system.Contents of vitamins B3 and B6 reported for CG pulp are26.6 ± 0.9 mg 100 g!1 DW and 24.8 ± 0.2 mg 100 g!1 DW,respectively (Vega-G!alvez et al., 2016).

3.5. Minerals

Reported results on the mineral content of CG are shown inTable 1. CG has high content of potassium and phosphoruscompared to other fruits (Florez, Fischer,& Sora, 2000; Rodríguez&Rodríguez, 2007; USDA., 2015). K is predominantly an intracellularcation, participating in the cellular uptake of molecules againstelectrochemical and concentration gradients, to the electro-physiology of nerves and muscle, and to acid-base regulation. P isused in a large variety of phosphorylated compounds which areneeded for metabolic energy transfer and storage processes,enzyme activation and control (Gupta & Gupta, 2014).

Contents of Ca, Fe, Mn, Mg and Zn are low, in contrast with whathas been claimed by some authors (Restrepo et al., 2009). Contentsof Mn, Zn, Cu, Se, Co, Ni, Cr, Na, Al, Ba, Sr, Rb were very low in thefruit (Leterme, Buldgen, Estrada, & Londo~no, 2006; Rodrigues et al.,2009; Torres-Ossand!on et al., 2015), and Se was not detected(Leterme et al., 2006).

3.6. Withanolides

Withanolides form a group of naturally steroids usually found inplants of the Solanaceae family and have received increasingattention from researchers because of its complex structural char-acteristics, potential bioactivity and large variety of health prop-erties (Mirjalili, Moyano, Bonfill, Cusido,& Palaz!on, 2009; Yen et al.,2010). Research on the isolation and identification of these com-pounds is still ongoing and a number of withanolides have beenobtained and characterized from Physalis peruviana L plant parts(Fang, Li, & Liu, 2009; Fang, Liu, & Li, 2012). Nevertheless, there isno evidence of withanolides presence in CG fruit (Fang et al., 2012),therefore, presumptive health benefits from these compoundscannot be claimed from CG consumption as suggested in literature(Ramadan, 2011).

3.7. Physalins

Physalins are pseudo-steroids that have been isolated fromplant of the genus Physalis sp. (M. B. P. Soares et al., 2006). Thesecompounds have been associated to anti-tumour, antibacterial andimmunosuppressive activities (He et al., 2013; Li et al., 2012; M. B.Soares, Bellintani, Ribeiro, Tomassini, & dos Santos, 2003; M. B. P.;Soares et al., 2006; Wu et al., 2012). The studies, however, as withwithanolides, have not been conducted on the fruit but on the plantPhysalis. So, there is no information on physalin content in CG, norevidence of mechanisms of beneficial activities of oral consumptionof physalin compounds.

3.8. Antioxidant activity

Antioxidant activity is a property discussed widely in literaturebecause oxidation has been related to several diseases likecancer, among others (Gülçin, 2012; Max Leenders et al., 2014). CGwas reported to have less antioxidant activity than blueberriesand cranberries (Namiesnik et al., 2013). Antioxidant activitiesdetermined by four methods, being DPPH assay the most usedmethod. Reported data for antioxidant activity also have largevariation in numbers, unit expressions and assays. These variationcome from previous aspects discussed for antioxidant compounds.In Fig. 6, antioxidant activity has been plotted according to ripenessstage of the CG, as explained in Section 3.1.

However, this information is not enough evidence to make as-sociations of specific health-promoting compound with antioxi-dant activity.

4. Processing and storage

Nowadays, CG is available as dried fruit and in juices and jam. Inthis section, storage effect on health-promoting compounds isassessed as well as the effect of processing such as drying,pasteurization, enzymatic treatment and high pressure, accordingto availability of data.

4.1. Storage

In CG packed in expanded polystyrene covered to vinyl filmduring 8 days of storage at 20 "C, carotenoids increased from 124 to170 mg g!1, and at 4 "C, the increase was from 124 to 142 mg g!1.Similar effect was observed for phenolic compounds contentswhich at 20 "C increased from 210 to 360 mg GAE 100 g!1, while at4 "C, the increase reached an amount of 300 mg GAE 100 g!1

(Severo et al., 2010). Antioxidant activity, however, remained stableat 20 "C and decreased at 4 "C from 1.55 to 1.3 mmol TE g!1, assessedby 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) ABTSassay (Severo et al., 2010). These results suggested that coolingtemperatures do not favour health-promoting compounds con-tents. Unfortunately, it is not mentioned whether the fruitswere contained in the calyx or not. Vitamin C (from 28.58 to 31.65to 13.05e13.24 mg 100 g!1), phenolic compounds (from 6.12 to6.02 mg GAE 100 g!1) and antioxidant activity decreased(0.31e0.26 mM TE.Kg!1) during 14 days of storage at 20 "C withoutcalyx (Valdenegro et al., 2012). These results, in addition tostudies on ripening, previously discussed, suggest that calyx playsan important role in protecting the health-promoting compoundsof the fruit. Preservation of antioxidant activity (0.31e0.32 -mM TE.Kg!1) assessed by ABTS assay was obtained with the use of1-methylcyclopropene as inhibitor of ethylene biosynthesis on thefruit during post-harvest (Valdenegro et al., 2012).

Storage of pasteurized CG juice lead to a reduction of caroten-oids (from 70.1 to 68.66 mg ml!1), antioxidant activity (from 416.9

Table 1Content of minerals in cape gooseberry (Physalis peruviana L.).

Mineral Content (mg 100 g!1 FW)

Iron (Fe) 0.1e3.9Magnesium (Mg) 34.7e120.1Calcium (Ca) 7.0e37.7Potassium (K) 55.3e501.9Phosphorous (P) 34.0e54.9Sodium (Na) 52.7Zinc (Zn) 1.5Copper (Cu) 0.7Manganese (Mn) 0.7

Data sources: (Capus, Tenezaca,& Redrobn, Leterme et al., 2006; Ramadan&Moersel, 2007; Repo de Carrasco & Encina, 2008; Rodrigues et al., 2009;Torres-Ossand!on et al., 2015).

M.-L. Olivares-Tenorio et al. / Trends in Food Science & Technology 57 (2016) 83e9288

to 298 mM TE.100 g!1) assessed by DPPH assay, TPC (from 0.65 to0.66 mg GAE.100 g!1) and vitamin C (from 38.9 to 30.2 mg.100 g!1)after 21 days of storage at 4 "C (Rabie et al., 2015). However, pre-sented data are not consistent with carotenoids, TPC and antioxi-dant activity (DPPH) values reported in other researches as shownin Sections 3.2, 3.3 and 3.8. Vitamin C content in the CG powderobtained by spray drying was affected by storage temperature andvacuum conditions. At 30 "C, vitamin C reduced (from 36.68 to10.34 mg.100 g!1) after six months under non-vacuum conditions.This reduction was lower reaching values of 25.64 and21.78 mg.100 g!1 at 4 and 20 "C, respectively. The used of vacuum,under the same conditions, reduced the losses of vitamin C from 0.7to 12%, having more effect at 30 "C rather than at 4 "C (Hern!andez-Sandoval, Cort!es-Rodríguez, & Ciro-Vel!asquez, 2014).

Total carotenoids (up to 6 mg.100 g!1) and total phenolic com-pound (up to 90 mg GAE.100 g!1) were stable in alginate coatedfruits after 21 days of storage at 2 "C. Antioxidant activity (assaywith ABTS), however decreased (from 120 to 80 mg TE 100 g!1)after one week. Authors did not find significant differences withcontrol samples (Carvalho, Villa~no, Moreno, Serrano, & Valero,2015).

Effect of storage after high hydrostatic pressure processing willbe discussed further on, at evaluation of non-thermal processing inCG.

Scattered data on storage of fresh and processed CG does notallow having a clear insight of health-promoting compounds dur-ing this stage.

4.2. Thermal processing

Thermal processing is the most common method to process CG.Literature is mainly focused on drying (convection, drum, andfreeze drying). Traditional pasteurization (low temperature, longtime) and jam production has been studied as well (Rutz, Voss,Pertuzatti, Barcia, & Zambiazi, 2012).

TPC of dried CG processed with microwave and convectivemethods showed a drastic decrease of these compounds (from 863to 237 mg GAE.100 g!1 DW). There were not significant differencesin the degradation of TPC, probably because polyphenol oxidasesand peroxidases are not immediately inactivated duringmicrowavedrying, therefore they can speed up the degradation of TPC in thesame way heat treatment does (_Izli, Yıldız, Ünal, Isık, & Uylaser,

2014). Antioxidant activity evaluated by DPPH assay alsodecreased (from 47.2 to 11.5 mmol TE g!1 DW), probably as aconsequence of TPC decrease.

b-carotene content increased in convection drying whenincreasing temperature (L!opez et al., 2013), probably for a betterextractability caused by heat treatment (van het Hof, West,Weststrate, & Hautvast, 2000). In contrast, studies of convectiondrying reported degradations of 30e55% (Narv!aez-Cuenca et al.,2014). Carotenoids increased in a combined osmodryingeheattreatment processing, because of the temperature rather thanbecause of concentration of osmotic solutions (Luchese, Gurak, &Marczak, 2015). Discrepancies in results of b-carotene do notallow understanding the effect of heat treatment on b-carotene northe content of this compound in thermal processed food.

Retention of antioxidant activity (DPPH method) for jam andjuice was higher at 90 "C after approx. 30 min (about9.7 mmol TE.g!1) (Rabie et al., 2015; Ramadan & Moersel, 2007;Rutz et al., 2012). For drying processes, lowest retention of anti-oxidant activity (approx. 25%) was reported for microwave, con-vection and combined dryingmethod (not plotted) (_Izli et al., 2014).Highest retention was reported for pasteurization, which has to dowith shorter times of heat exposure (Rabie et al., 2015; Ramadan &Moersel, 2007; Rutz et al., 2012). Participation of b-carotene in theantioxidant activity is apparently low because even with the in-crease of b-carotene content, antioxidant activity is stable. Thegathered information does not allow associating antioxidant ac-tivity and health-promoting compounds.

In addition to thermal processing, the use of enzymes such aspectinase-arabanase, polygalacturonase, pectinase, hemicellulaseand cellulose, has been tested to improve the yield in juiceextraction. No significant decrease of TPC, ascorbic acid and anti-oxidant activity resulted of enzymes addition, but related topasteurization treatment (80 "C and 10 min) (Ramadan & Moersel,2007).

In summary, there is dispersed information on the effect ofthermal processing on the health-promoting compounds in CGwith high discrepancies in results, thus behaviour of compoundsduring thermal process are still unclear.

4.3. Non-thermal processing

While research on thermal processing of CG is still in

Fig. 6. Antioxidant activity of CG (Physalis peruviana L) assayed with ABTS method (8A) and DPPH method (8B) for ripeness stages (according NTC 4580, 1999) and reported data. In8A, units are Trolox Equivalents. Kg!1 FW (Valdenegro et al., 2012) and mmol Trolox. g!1 FW (Licodiedoff, Andr!e et al., 2013; Severo et al., 2010). In 8B, units are g Trolox Equivalents.g!1 FW (Repo de Carrasco & Encina, 2008); % inhibition DPPH (Mier & C!aez, 2011) and IC50 g L!1 (Bravo et al., 2015).

M.-L. Olivares-Tenorio et al. / Trends in Food Science & Technology 57 (2016) 83e92 89

development, research about non-thermal processing is justemerging. The effect high hydrostatic pressure HHP for threepressures (control, 300 Mpa, 400 Mpa and 500 Mpa) and threeprocessing times (1 min, 3 min and 5 min) on total phenoliccompounds TPC, phenolic acids, antioxidant activity (ORAC, FRAP,DPPH), tocopherols, fibres, and vitamin B3 and B6 andminerals; andthree pressures (control, 300, 400 and 500 Mpa) and 5 min ofprocessing time on vitamin C, b-carotene and antioxidant activity(ORAC and DPPH) have been reported for CG pulp (Torres-Ossand!on et al., 2015; Vega-G!alvez et al., 2016; Vega-G!alvezL!opez et al., 2014; Vega-G!alvez, Puente-Díaz et al., 2014). In sum-mary, after HHP treatment, the pulps had contents of about 17.5 mgof vitamin C 100 g!1 FW, 194.92e232.5 of b-carotene mg g!1 FW,antioxidant activity values of 116.7e210.2 mg TE g!1 and TPC of164.68e268.7 mg GAE 100 g!1. Comparing to initial values, vitaminC and b-carotene were stable to HHP treatment which is differentfromwhat is reported for tomato (400Mpa/15 min/25 "C) where b-carotene increased remarkably (80%) given improvement ofextractability and bioavailability (S!anchez-Moreno, Plaza, de Ancos,& Cano, 2006). Antioxidant activity increased and TPC decreased.

Effect on storage after HHP process was also evaluated at 4 "C for30 and 60 days. Content of TPC in CG pulp had contradictory results.After HHP treatment, an experiment showed an increase of TPC anda decrease after 60 day of storage at 4 "C (Vega-G!alvez et al., 2016).However, same authors reported another experiment where is notclear behaviour of TPC after HHP and storage (Vega-G!alvez L!opezet al., 2014; Vega-G!alvez, Puente-Díaz et al., 2014). Neither wayno significant differences were found in TPC contents betweenpressures and between process times after HHP processing andstorage (P > 0.05).

Antioxidant activity decreased during 30 and 60 days of storageat 4 "C (with some samples exceptions) (Torres-Ossand!on et al.,2015; Vega-G!alvez et al., 2016; Vega-G!alvez L!opez et al., 2014;Vega-G!alvez, Puente-Díaz et al., 2014). No significant differenceswere found in changes of antioxidant activity between pressuresand times of processing, after processing and during storage(P > 0.05).

Vitamin C decreased approx. 81% after 30 days of storage at 4 "C.(Torres-Ossand!on et al., 2015). No significant differences werefound in changes of vitamin C between pressures, after processingand during storage (P > 0.05).

b-carotene decreased after 30 days of storage (Torres-Ossand!onet al., 2015). HHP treatment has an effect on the content of a-tocopherol but not on (bþg)-tocopherol. Higher pressure used,higher reduction of a-tocopherol during storage time (Vega-G!alvezet al., 2016). There were significant differences of a-tocopherol atday 30 between pressures (P < 0.05), but not between processingtimes (P > 0.05).

B3 and B6 were reported to increase after HHP treatment (Vega-G!alvez et al., 2016). Significant differences between pressures afterHHP treatment were found only for B6, and after 30 days of storageat 4 "C for B3 and B6 (P < 0.05). No significant differences withprocessing time were found (P > 0.05).

There was no clear pattern for insoluble dietary fibre, solubledietary fibre and total dietary fibre after HHP (Vega-G!alvez et al.,2016). Therefore, effect of HHP on fibres is unknown.

In summary, HHP processing has shown to improve extract-ability of health-promoting compounds in CG (Briones-Labarcaet al., 2013), especially, vitamins B3 and B6 and antioxidant activ-ity (Vega-G!alvez et al., 2016; Vega-G!alvez L!opez et al., 2014; Vega-G!alvez, Puente-Díaz et al., 2014). HHP might disrupt cell walls,increasing permeability and allowing solvent penetration andtherefore, improve extractability and bioavailability of some com-pounds (Prasad, Yang, Yi, Zhao, & Jiang, 2009). This effect could bepositive when it relates to the bioavailability of the compounds at

consumption. However, more information is required to make aproper assessment about behaviour of health-promoting com-pounds of CG during HHP processing.

5. Conclusions

Health-promoting compounds of CG have been reviewed froma supply-chain perspective, involving pre-harvest, post-harvest,processing and storage, in order to get an understanding of thepresence of compounds at consumption stage. According to re-ported data, CG is a source of vitamin C (20 and 35 mg.100 g!1

FW), b-carotene (up to 2.0 mg 100 g!1 FW), total phenolic com-pounds TPC (50e250 gallic acid equivalents.100 g!1 FW), phenolicacids (caffeic, gallic, chlorogenic, ferulic and p-cumaric acids),flavonoids (quercetin, rutin, myricetin, kaempferol, catechin andepicatechin) and antioxidant activity. Presence of tocopherols, vi-tamins B3 and B6, minerals and fibre have been also reported.Contents of health-promoting compounds in CG are relevantcompared to other fruit sources for every type of compound.Consumption of fresh CG provides a diversity of compounds,especially when the fruit fully ripened, as reported in this review.Contents of withanolides and physalins in CG are not well studiedyet, therefore it is not possible to make assumptions about thepresence of those compounds in CG, let alone whether there arehealth benefits.

Large variability of data has been found especially due to dif-ferences in methods of extraction and analysis, making a compar-ison of reported data an uneasy task. Moreover, varieties/cultivars/ecotypes and location of cultivation can have an effect of health-promoting compounds. In post-harvest, there are discrepancies inreported data. The effect of storage and calyx presence on health-promoting compounds and antioxidant activity remains unclear.Therefore, the contents of those compounds of fresh and processedCG after storage are unknown.

Vitamin C is reported to be the most sensitive compound tothermal and non-thermal treatment. b-carotene did not show aclear pattern in processing, decreasing or increasing, probablybecause enhance of extractability or oxidations reactions. TPCand antioxidant activity were stable in thermal processing(90 "C) and antioxidant activity increased in non-thermal treat-ment. HHP seems to improve the extractability of compounds.However, there is no systematic information yet to infer the ef-fect of these processing on health-promoting compounds;therefore, more research into the content and bioavailability ofthese compounds at the consumption stage of processed CG isneeded.

6. Suggestion for future research

Because of the variety of health-promoting compounds in CGand the large list of factors affecting their contents from cultivationto consumption, more research on this fruit is relevant. It isimportant to identify the effects of varieties/cultivars/ecotypes,cultivation and harvest conditions on phytochemicals and nutrientsof CG. The understanding of post-harvest physiology of the CG isneeded to know the role of calyx in health-promoting compoundspreservation or degradation. Because processing is part of thesupply chain, there is a big field of work for scientific research.Behaviour of phytochemicals and nutrients in CG during storage,thermal and non-thermal processes requires more research. Lastbut not least, bioavailability of health-promoting compounds andthe relationwith antioxidant activity need to be researched in orderto evaluate potential health benefits when CG is consumed, soconsumers can have the right information.

M.-L. Olivares-Tenorio et al. / Trends in Food Science & Technology 57 (2016) 83e9290

Acknowledgments

This work was supported by NUFFIC Netherlands UniversitiesFoundation for International Cooperation (NFD-PhD.11/830).

References

Abdel Moneim, A. E., Bauomy, A. A., Diab, M. M. S., Shata, M. T. M., Al-Olayan, E. M.,& El-Khadragy, M. F. (2014). The protective effect of Physalis peruviana L. againstcadmium-induced neurotoxicity in rats. Biological Trace Element Researchs, 160,392e399.

Agronet. (2016). Estadisticas sector agropecuario (Vol. 2016). Ministerio de Agri-cultura y Desarrollo Rural. http://www.agronet.gov.co/Paginas/estadisticas.aspx. Red de Informaci!on y Comunicaci!on del Sector Agropecuario. Colombia.Assessed April 2016.

Areiza-Mazo, N., Maldonado, M. E., & Rojano, B. (2013). Extracto acuoso de uchuva(Physalis peruviana): Actividades antiproliferativa, apopt!otica y antioxidante.Perspectivas en Nutrici!on Humana, 15, 41.

Balasundram, N., Sundram, K., & Samman, S. (2006). Phenolic compounds in plantsand agri-industrial by-products: Antioxidant activity, occurrence, and potentialuses. Food Chemistry, 99, 191e203.

Barcia, M. T., Jacques, A. C., Pertuzatti, P. B., & Zambiazi, R. C. (2010). Determinationby HPLC of ascorbic acid and tocopherols in fruits. Semina.Ciencias Agr!arias, 31,381e390.

Brause, A. R., Woollard, D. C., & Indyk, H. E. (2003). Determination of total vitamin Cin fruit juices and related products by liquid chromatography: Interlaboratorystudy. The Journal of AOAC International, 86, 367e374.

Bravo, K., Sepulveda-Ortega, S., Lara-Guzman, O., Navas-Arboleda, A. A., & Osorio, E.(2015). Influence of cultivar and ripening time on bioactive compounds andantioxidant properties in Cape gooseberry (Physalis peruviana L.). Journal of theScience of Food and Agriculture, 95, 1562e1569.

Briones-Labarca, V., Giovagnoli-Vicu~na, C., Figueroa-Alvarez, P., Quispe-Fuentes, I., &P!erez-Won, M. (2013). Extraction of b-carotene, vitamin C and antioxidantcompounds from Physalis peruviana (Cape Gooseberry) assisted by high hy-drostatic pressure. Food and Nutrition Sciences, 2013, 109e118.

Capus, C. P., Tenezaca, E. R. J., & Redrob!an, O. P. L.. Evaluaci!on nutricional de la uvilla(Physalis peruviana L.) deshidratada, a tres temperaturas mediante un deshi-dratador de bandejas. Revista Perfiles, 15.

Carvalho, C. P., Villa~no, D., Moreno, D. A., Serrano, M., & Valero, D. (2015). Alginateedible coating and cold storage for improving the physicochemical quality ofcape gooseberry (Physalis peruviana L.). Journal of Food Science and Nutrition, 1.

CEC.. (1993). Food science and techniques. In Reports of the scientific committe forfood: Commission of the european communities.

Da Silva Pinto, M., Ranilla, L. G., Apostolidis, E., Lajolo, F. M., Genovese, M. I., &Shetty, K. (2009). Evaluation of antihyperglycemia and antihypertension po-tential of native Peruvian fruits using in vitro models. Journal of Medicinal Food,12, 278e291.

Dekker, M., Verkerk, R., & Jongen, W. M. F. (2000). Predictive modelling of healthaspects in the food production chain: A case study on glucosinolates in cabbage.Trends in Food Science & Technology, 11, 174e181.

Del Rio, D., Rodriguez-Mateos, A., Spencer, J. P., Tognolini, M., Borges, G., &Crozier, A. (2013). Dietary (poly) phenolics in human health: Structures,bioavailability, and evidence of protective effects against chronic diseases. An-tioxidants & redox signaling, 18, 1818e1892.

Fang, S. T., Li, B., & Liu, J.-K. (2009). Two new withanolides from Physalis peruviana.Helvetica Chimica Acta, 92, 1304e1308.

Fang, S. T., Liu, J. K., & Li, B. (2012). Ten new withanolides from Physalis peruviana.Steroids, 77, 36e44.

Fiedor, J., & Burda, K. (2014). Potential role of carotenoids as antioxidants in humanhealth and disease. Nutrients, 6, 466e488.

Fischer, G. (1995). Effect of root zone temperature and tropical altitude on the growth,development and fruit q Valdenegro, Fuentes, Herrera, & Moya-Le!on, 2012 uality ofcape gooseberry (Physalis peruviana L.). Berlin. Germany: Humboldt-Universit€atzu Berlin.

Fischer, G., Ebert, G., & Ludders, P. (2000). Provitamin A carotenoids, organic acidsand ascorbic acid content of cape gooseberry (Physalis peruviana L.) ecotypesgrown at two tropical altitudes. Acta Horticulturae, 263e268.

Fischer, G., & Martínez, O. (1999). Calidad y madurez de la uchuva (Physalisperuviana L.) en relaci!on con la coloraci!on del fruto. Agronomía Colombiana, 16,35e39.

Florez, V., Fischer, G., & Sora, A. (2000). Producci!on, Poscosecha y Exportaci!on de laUchuva (Physalis peruviana L.). Bogot!a. Colombia. Universidad Nacional deColombia, Secci!on Imprenta.

Gomez, M. L., & Lajolo, F. M. (2008). Ascorbic acid metabolism in fruits: Activity ofenzymes involved in synthesis and degradation during ripening in mango andguava. Journal of the Science of Food and Agriculture, 88, 756e762.

Grosso, G., Bei, R., Mistretta, A., Marventano, S., Calabrese, G., Masuelli, L., et al.(2013). Effects of vitamin C on health: A review of evidence. Frontiers inBioscience, 18, 1017e1029.

Gülçin, _I. (2012). Antioxidant activity of food constituents: An overview. Archives ofToxicology, 86, 345e391.

Gupta, U. C., & Gupta, S. C. (2014). Sources and deficiency diseases of mineral nu-trients in human health and nutrition: A review. Pedosphere, 24, 13e38.

Gutierrez, M. S., Trinchero, G. D., Cerri, A. M., Vilella, F., & Sozzi, G. O. (2008).Different responses of goldenberry fruit treated at four maturity stages with theethylene antagonist 1-methylcyclopropene. Postharvest Biology and Technology,48, 199e205.

H€akkinen, S. H., K€arenlampi, S. O., Heinonen, I. M., Mykk€anen, H. M., &T€orr€onen, A. R. (1999). Content of the flavonols quercetin, myricetin, andkaempferol in 25 edible berries. Journal of Agricultural and Food Chemistry, 47,2274e2279.

Hern!andez-Sandoval, G. R., Cort!es-Rodríguez, M., & Ciro-Vel!asquez, H. J. (2014).Effect of storage conditions on quality of a functional powder of cape goose-berry obtained by spray drying. Revista UDCA Actualidad & Divulgaci!on Cien-tífica, 17, 139e149.

Hern!andez, Y., Lobo, M. G., & Gonz!alez, M. (2006). Determination of vitamin C intropical fruits: A comparative evaluation of methods. Food Chemistry, 96,654e664.

He, H., Zang, L.-H., Feng, Y.-S., Chen, L.-X., Kang, N., Tashiro, S.-i., et al. (2013).Physalin A induces apoptosis via p53-Noxa-mediated ROS generation, andautophagy plays a protective role against apoptosis through p38-NF-kB survivalpathway in A375-S2 cells. Journal of Ethnopharmacology, 148, 544e555.

Hiwilepo-van Hal, P., Bosschaart, C., van Twisk, C., Verkerk, R., & Dekker, M. (2012).Kinetics of thermal degradation of vitamin C in marula fruit (Sclerocarya birreasubsp. caffra) as compared to other selected tropical fruits. LWT- Food Scienceand Technology, 49, 188e191.

Hjartåker, A., Knudsen, M. D., Tretli, S., & Weiderpass, E. (2015). Consumption ofberries, fruits and vegetables and mortality among 10,000 Norwegian menfollowed for four decades. European Journal of Nutrition, 54, 599e608.

van het Hof, K. H., West, C. E., Weststrate, J. A., & Hautvast, J. G. (2000). Dietaryfactors that affect the bioavailability of carotenoids. Jounal of Nutrition, 130,503e506.

ICONTEC.. (1999). NTC 4580. Fresh fruits. Cape Gooseberry. Specifications. Bogota.Colombia: Colombian Standard.

_Izli, N., Yıldız, G., Ünal, H., Isık, E., & Uylaser, V. (2014). Effect of different dryingmethods on drying characteristics, colour, total phenolic content and antioxi-dant capacity of goldenberry (Physalis peruviana L.). International Journal of FoodScience & Technology, 49, 9e17.

Johnston, C. S. (2012). Vitamin C, in present Knowledge in nutrition (10th ed.). Oxford,UK: Wiley-Blackwell.

Leenders, M., Boshuizen, H. C., Ferrari, P., Siersema, P. D., Overvad, K., Tjønneland, A.,et al. (2014). Fruit and vegetable intake and cause-specific mortality in the EPICstudy. European Journal of Epidemiology, 29, 639e652.

Leterme, P., Buldgen, A., Estrada, F., & Londo~no, A. M. (2006). Mineral content oftropical fruits and unconventional foods of the Andes and the rain forest ofColombia. Food Chemistry, 95, 644e652.

Licodiedoff, S., Andr!e, L., Koslowski, D., & Ribani, R. H. (2013). Flavonols and anti-oxidant activity of Physalis peruviana L. fruit at two maturity stages. Acta Sci-entiarum Technology, 35, 393e399.

Licodiedoff, S., Koslowski, L. A. D., & Ribani, R. H. (2013). Flavonol rates of gosseberryfruits Physalis peruviana determined by HPLC through the optimization andvalidation of the analytic method. International Journal of Food Science andNutrition, 3, 1e6.

Lindshield, B. L. (2012). Carotenoids, in present Knowledge in nutrition (10th ed.).Oxford, UK: Wiley-Blackwell.

Li, X., Zhang, C., Wu, D., Tang, L., Cao, X., & Xin, Y. (2012). In vitro effects on intestinalbacterium of physalins from Physalis alkekengi var. Francheti. Fitoterapia, 83,1460e1465.

L!opez, J., Vega-G!alvez, A., Torres, M. J., Lemus-Mondaca, R., Quispe-Fuentes, I., & DiScala, K. (2013). Effect of dehydration temperature on physico-chemical prop-erties and antioxidant capacity of goldenberry (Physalis peruviana L.). ChileanJournal of Agricultural Research, 73, 293e300.

Luchese, C. L., Gurak, P. D., & Marczak, L. D. F. (2015). Osmotic dehydration ofphysalis (Physalis peruviana L.): Evaluation of water loss and sucrose incorpo-ration and the quantification of carotenoids. LWT- Food Science and Technology,63, 1128e1136.

Machmudah, S., & Goto, M. (2013). Methods for extraction and analysis of carot-enoids. In Natural products (pp. 3367e3411). Springer.

MADR, UNAL, CORPOICA. (2009). Agenda prospectiva de investigaci!on y desarrollotecnol!ogico para la cadena productiva de la uchuva en fresco para exportaci!on encolombia. Bogot!a: Universidad Nacional de Colombia. Ministerio de Agriculturay Desarrollo Rural, Corporaci!on Colombiana de Investigaci!on Agropecuaria.Available in http://conectarural.org/sitio/sites/default/files/documentos/AGENDA%20CADENA%20UCHUVA.pdf.

Ma, X., Wu, H., Liu, L., Yao, Q., Wang, S., Zhan, R., et al. (2011). Polyphenolic com-pounds and antioxidant properties in mango fruits. Scientia Horticulturae, 129,102e107.

Mier, H. (2012). Evaluaci!on del contenido de polifenoles y carotenos en extractos defrutos de Physalis peruviana y su potential antioxidante, citot!oxico e inmunomo-dulador in vitro. Colombia: Universidad de la Sabana, Bogot!a.

Mier, H. J., & C!aez, R. G. (2011). Contenido de polifenoles, carotenos y capacidadantioxidante en fruos de uchuva (Physalis peruviana) en relaci!on con su estadode maduraci!on. ReCiTeIA, 11, 103e112.

Mirjalili, M. H., Moyano, E., Bonfill, M., Cusido, R. M., & Palaz!on, J. (2009). Steroidallactones from Withania somnifera, an ancient plant for novel medicine. Mole-cules, 14, 2373e2393.

Mocchegiani, E., Costarelli, L., Giacconi, R., Malavolta, M., Basso, A., Piacenza, F., et al.(2014). Vitamin Eegene interactions in aging and inflammatory age-related

M.-L. Olivares-Tenorio et al. / Trends in Food Science & Technology 57 (2016) 83e92 91

diseases: Implications for treatment. A systematic review. Ageing research re-views, 14, 81e101.

Mu~noz-J!auregui, A. M., Ramos-Escudero, D., & Fernando, A. O. U. (2007). Evaluaci!onde la capacidad antioxidante y contenido de compuestos fen!olicos en recursosvegetales promisorios. Revista de la Sociedad Química del Perú, 73, 142e149.

Mursu, J., Virtanen, J. K., Tuomainen, T.-P., Nurmi, T., & Voutilainen, S. (2014). Intakeof fruit, berries, and vegetables and risk of type 2 diabetes in finnish men: Thekuopio ischaemic heart disease risk factor study. The American Journal of ClinicalNutrition, 99, 328e333.

Namiesnik, J., Vearasilp, K., Kupska, M., Ham, K. S., Kang, S. G., Park, Y. K., et al.(2013). Antioxidant activities and bioactive components in some berries. Eu-ropean Food Research and Technology, 237, 819e829.

Namiesnik, J., Vearasilp, K., Leontowicz, H., Leontowicz, M., Ham, K. S., Kang, S. G.,et al. (2014). Comparative assessment of two extraction procedures for deter-mination of bioactive compounds in some berries used for daily food con-sumption. International Journal of Food Science & Technology, 49, 337e346.

Narv!aez-Cuenca, C., Mateus-G!omez, A., & Restrepo-S!anchez, L. (2014). Antioxidantcapacity and total phenolic content of air-dried cape gooseberry (Physalisperuviana L.) at different ripeness stages. Agronomía Colombiana, 32, 232e237.

Navarro, J. M., Flores, P., Garrido, C., & Martinez, V. (2006). Changes in the contentsof antioxidant compounds in pepper fruits at different ripening stages, asaffected by salinity. Food Chemistry, 96, 66e73.

Norat, T., Aune, D., Chan, D., & Romaguera, D. (2014). Fruits and vegetables:Updating the epidemiologic evidence for the WCRF/AICR lifestyle recommen-dations for cancer prevention. In Advances in nutrition and cancer (pp. 35e50).Springer.

Novoa, R., Bojac!a, M., Galvis, J., & Fischer, G. (2006). La madurez del fruto y el secadodel c!aliz influyen en el comportamiento poscosecha de la uchuva, almacenada a12 C (Physalis peruviana L.). Agronomía Colombiana, 24, 77e86.

Odriozola-Serrano, I., Hern!andez-Jover, T., & Martín-Belloso, O. (2007). Comparativeevaluation of UV-HPLC methods and reducing agents to determine vitamin C infruits. Food Chemistry, 105, 1151e1158.

Olivares-Tenorio, M., Linnemann, A., Pascucci, S., Verkerk, R., & van Boekel, M.(2014). Misaligned preferences and perceptions on quality attributes of capegooseberry (Physalis peruviana L) supply chain actors. In Conference proceedingsPart 4 international food marketing research symposium 2014 (pp. 106e112).

Osman, N. N., AL-seeni, M. N., Alkhatib, M. H., & Al-shreef, H. A. (2013). Modulationof radiation injury by Physalis peruviana. Life Science Journal, 4, 10.

Pillai, S. S., & Sathyadevi, M. (2015). Extraction, isolation and characterization ofbioactive flavonoids from the fruits of Physalis peruviana Linn extract. AsianJournal of Pharmaceutical and Clinical Research, 8.

Ponte, S., & Gibbon, P. (2005). Quality standards, conventions and the governance ofglobal value chains. Economics society, 34, 1e31.

Prasad, K. N., Yang, E., Yi, C., Zhao, M., & Jiang, Y. (2009). Effects of high pressureextraction on the extraction yield, total phenolic content and antioxidant ac-tivity of longan fruit pericarp. Innovative Food Science and Emerging Technolo-gies, 10, 155e159.

Rabie, M., Soliman, A., Diaconeasa, Z., & Constantin, B. (2015). Effect of pasteuri-zation and shelf life on the physicochemical properties of physalis (PhysalisperuvianaL.) juice. Journal of Food Processing and Preservation, 39, 1051e1060.

Raffo, A., Leonardi, C., Fogliano, V., Ambrosino, P., Salucci, M., Gennaro, L., et al.(2002). Nutritional value of cherry tomatoes (Lycopersicon esculentum cv.Naomi F1) harvested at different ripening stages. Journal of Agricultural andFood Chemistry, 50, 6550e6556.

Ramadan, M. F. (2011). Bioactive phytochemicals, nutritional value, and functionalproperties of cape gooseberry (Physalis peruviana): An overview. Food ResearchInternational, 44, 1830e1836.

Ramadan, M. F., & Moersel, J. T. (2007). Impact of enzymatic treatment on chemicalcomposition, physicochemical properties and radical scavenging activity ofgoldenberry (Physalis peruviana L.) juice. Journal of the Science of Food andAgriculture, 87, 452e460.

Ramadan, M. F., & M€orsel, J.-T. (2003). Oil goldenberry (Physalis peruviana L.).Journal of Agricultural and Food Chemistry, 51, 969e974.

Repo de Carrasco, R., & Encina, C. R. (2008). Determinaci!on de la capacidad anti-oxidante y compuestos bioactivos de frutas nativas peruanas. Revista de laSociedad Química del Perú, 74, 108e124.

Restrepo, A. M., Cort!es, M., & M!arquez, C. J. (2009). Uchuvas (Physalis peruviana L.)mínimamente procesadas fortificadas con vitamina E. Vitae, 16, 19e30.

Rockenbach, I. I., Rodrigues, E., Cataneo, C., Gonzaga, L. V., Lima, A., Mancini-Filho, J.,et al. (2009). !Acidos fen!olicos e atividade antioxidante em fruto de Physalisperuviana l. Alimentos e Nutriç~ao Araraquara, 19, 271e276.

Rodrigues, E., Rockenbach, I. I., Cataneo, C., Gonzaga, L. V., Chaves, E. S., & Fett, R.(2009). Minerals and essential fatty acids of the exotic fruit Physalis peruviana L.Ciencia e Tecnologia de Alimentos, 29, 642e645.

Rodríguez, S., & Rodríguez, E. (2007). Effect of Physalis peruviana (goldenberry) onpostprandial glycemia in young adults. Revista M!edica Vallejiana, 4, 43e52.

Rop, O., Mlcek, J., Jurikova, T., & Valsikova, M. (2012). Bioactive content and anti-oxidant capacity of Cape gooseberry fruit. Central European Journal of Biology, 7,

672e679.Rutz, J. K., Voss, G. B., Pertuzatti, P. B., Barcia, M. T., & Zambiazi, R. C. (2012). Geleia de

Physalis peruviana L. : Caracterizaç~ao bioativa, antioxidante e sensorial. Ali-mentos e Nutriç~ao, 23, 369e375.

S!anchez-Moreno, C., Plaza, L., de Ancos, B., & Cano, M. P. (2006). Impact of high-pressure and traditional thermal processing of tomato pur!ee on carotenoids,vitamin C and antioxidant activity. Journal of the Science of Food and Agriculture,86, 171e179.

Scott, K. J. (2001). Detection and measurement of carotenoids by UV/VIS spectro-photometry. In Current protocols in food analytical chemistry. John Wiley andSons, Inc.

Severo, J., Lima, C. S. M., Coelho, M. T., Rufatto, A. D. R., Rombaldi, C. V., & Silva, J. A.(2010). Atividade antioxidante e fitoquímicos em frutos de Physalis (Physalisperuviana, L.) durante o amadurecimento e o armazenamento. Revista Brasileirade Agrociencias, 16, 77e82.

Soares, M. B., Bellintani, M. C., Ribeiro, I. M., Tomassini, T. C., & dos Santos, R. R.(2003). Inhibition of macrophage activation and lipopolysaccaride-induceddeath by seco-steroids purified from Physalis angulata L. European Journal ofPharmacology, 459, 107e112.

Soares, M. B. P., Brustolim, D., Santos, L., Bellintani, M., Paiva, F., Ribeiro, Y., et al.(2006). Physalins B, F and G, seco-steroids purified from Physalis angulata L.,inhibit lymphocyte function and allogeneic transplant rejection. InternationalImmunopharmacology, 6, 408e414.

Sogi, D. S., Siddiq, M., Roidoung, S., & Dolan, K. D. (2012). Total phenolics, carot-enoids, ascorbic acid, and antioxidant properties of fresh-cut mango (mangiferaindica L., cv. Tommy Atkin) as affected by infrared heat treatment. Journal ofFood Science, 77, 1197e1202.

Stratil, P., Klejdus, B., & Kub!an, V. (2006). Determination of total content of phenoliccompounds and their antioxidant activity in vegetables evaluation of spectro-photometric methods. Journal of Agricultural and Food Chemistry, 54, 607e616.

Tarrago-Trani, M. T., Phillips, K. M., & Cotty, M. (2012). Matrix-specific methodvalidation for quantitative analysis of vitamin C in diverse foods. Journal of FoodComposition and Analysis, 26, 12e25.

Terry, P., Terry, J., & Wolk, A. (2001). Fruit and vegetable consumption in the pre-vention of cancer: An update. Journal of Internal Medicine, 250, 280e290.

Torres-Ossand!on, M. J., L!opez, J., Vega-G!alvez, A., Galotto, M. J., Perez-Won, M., & DiScala, K. (2015). Impact of high hydrostatic pressure on physicochemical char-acteristics, nutritional content and functional properties of cape gooseberrypulp (Physalis peruvianaL.). Journal of Food Processing and Preservation, 39,2844e2855.

USDA, & HSS.. (2010). Dietary guidelines for Americans. USA: US Department ofAgriculture & US Department of Health and Human Services.

USDA.. (2014). National nutrient database for standard reference release 26. Nutrients:Vitamin C, total ascorbic acid (mg). USA: United States Department ofAgriculture.

USDA.. (2015). National nutrient database for standard reference release 27. Nutrients:K (mg) and P (mg). United States Department of Agriculture.

Valdenegro, E. (2013). The effects of drying processes on organoleptic characteris-tics and the health quality of food ingredients obtained from goldenberry fruits(Physalis peruviana). Open Access Scientific Reports, 2.

Valdenegro, M., Fuentes, L., Herrera, R., & Moya-Le!on, M. A. (2012). Changes inantioxidant capacity during development and ripening of goldenberry (Physalisperuviana L.) fruit and in response to 1-methylcyclopropene treatment. Post-harvest Biology and Technology, 67, 110e117.

Vald!es, L., Cuervo, A., Salazar, N., Ruas-Madiedo, P., Gueimonde, M., & Gonz!alez, S.(2015). The relationship between phenolic compounds from diet and micro-biota: Impact on human health. Food & function, 6, 2424e2439.

Vasco, C., Ruales, J., & Kamal-Eldin, A. (2008). Total phenolic compounds andantioxidant capacities of major fruits from Ecuador. Food Chemistry, 111,816e823.

Vega-G!alvez, A., Díaz, R., L!opez, J., Galotto, M. J., Reyes, J. E., Perez-Won, M., et al.(2016). Assessment of quality parameters and microbial characteristics of Capegooseberry pulp (Physalis peruviana L.) subjected to high hydrostatic pressuretreatment. Food and Bioproducts Processing, 97, 30e40.

Vega-G!alvez, A., L!opez, J., Torres-Ossand!on, M. J., Galotto, M. J., Puente-Díaz, L.,Quispe-Fuentes, I., et al. (2014). High hydrostatic pressure effect on chemicalcomposition, color, phenolic acids and antioxidant capacity of Cape gooseberrypulp (Physalis peruviana L.). LWT- Food Science and Technology, 58, 519e526.

Vega-G!alvez, A., Puente-Díaz, L., Lemus-Mondaca, R., Miranda, M., & Torres, M. J.(2014). Mathematical modeling of thin-layer drying kinetics of cape gooseberry(Physalis peruvianaL.). Journal of Food Processing and Preservation, 38, 728e736.

Wu, S.-Y., Leu, Y.-L., Chang, Y.-L., Wu, T.-S., Kuo, P.-C., Liao, Y.-R., et al. (2012).Physalin F induces cell apoptosis in human renal carcinoma cells by targetingNF-kappaB and generating reactive oxygen species. PLoS One, 7, e40727.

Yen, C.-Y., Chiu, C.-C., Chang, F.-R., Chen, J. Y.-F., Hwang, C.-C., Hseu, Y.-C., et al.(2010). 4beta-Hydroxywithanolide E from Physalis peruviana (golden berry)inhibits growth of human lung cancer cells through DNA damage, apoptosis andG2/M arrest. BMC cancer, 10, 46e46.

M.-L. Olivares-Tenorio et al. / Trends in Food Science & Technology 57 (2016) 83e9292

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