GOLDENBERRY (PHYSALIS PERUVIANA) JUICE RICH IN HEALTH-BENEFICIAL COMPOUNDS SUPPRESSES...

GOLDENBERRY (PHYSALIS PERUVIANA) JUICE RICH INHEALTH-BENEFICIAL COMPOUNDS SUPPRESSESHIGH-CHOLESTEROL DIET-INDUCED HYPERCHOLESTEROLEMIAIN RATSMOHAMED FAWZY RAMADAN1,2,4, NESMA ALI HASSAN1, RAFAAT M. ELSANHOTY3* andMAHMOUD Z. SITOHY1

1Agricultural Biochemistry Department, Faculty of Agriculture, Zagazig University, Zagazig 44519, Egypt2Department of Nutrition and Food Science, University of Maryland, College Park, MD 207423Department of Industrial Biotechnology, Branch of Food and Dairy Biotechnology, Institute of Genetic Engineering and Biotechnology, MenoufiaUniversity, Zagazig, Egypt

4Corresponding author. TEL: 2-055-2320282or 2-0129782424; FAX: 2-055-2287567 or2-055-2345452; EMAIL:[email protected];[email protected]

*Present address: Department of FoodScience and Human Nutrition, Faculty ofAgriculture and Veterinary Medicine, QassimUniversity, Kingdom of Saudi Arabia.

Received for Publication December 16, 2011Accepted for Publication May 24, 2012

doi:10.1111/j.1745-4514.2012.00669.x

ABSTRACTGoldenberries (Physalis peruviana) are a promising exotic fruit that could be asubject of many novel foods. No reports are available on the effect of administra-tion of goldenberries on different aspects of blood profile in experimentalanimals. The objective of this study was to investigate the effect of feeding golden-berry juice on hypercholesterolemia by analyzing the changes in the blood profileof high-cholesterol diet (HCD)-fed rats. The chemical composition and antiradi-cal properties of juice were determined. Generally, rats fed with goldenberry juiceshowed lower levels of total cholesterol, total triacylglycerol and total low-densitylipoprotein cholesterol, as well as higher levels of high-density lipoprotein choles-terol in comparison with animals fed with HCD and cholesterol-free diet. Juiceadministration induced a decrease in the activity of glutamic pyruvic transami-nase compared with the positive control group after 2 months of administration.There was a remarkable decrease in total serum protein, albumin and globulin forgroups treated with goldenberry juice. Histological examination of the liver andkidney were also conducted. The results demonstrated that consumption of gold-enberry juice may provide beneficial effects on reversing HCD-associated detri-mental changes.

PRACTICAL APPLICATIONSThe administration of goldenberry juice has a profound influence on the metabo-lism of lipids and positively affects the blood profile of rats fed with a high-cholesterol diet (HCD). The results suggest that goldenberry juice has significanthypocholesterolemic activities. In addition, goldenberry juice seems to protect theliver in response to oxidative stress (probably via the elevation of antioxidantenzymes levels) as well as alleviate the magnitude of fatty liver development inresponse to HCD. Therefore, goldenberry juice with high antioxidant potentialcould be helpful for patients suffering from coronary atherosclerosis.

INTRODUCTION

Berries have been shown to provide significant health ben-efits because of their high antioxidants, vitamins, mineralsand fiber content (Zhao 2007). Goldenberries or capegooseberries (Physalis peruviana Linn., Solanaceae) are

short-lived perennials. The fruit with an approximateweight of 4–5 g is covered by a brilliant yellow peel(Mayorga et al. 2001). It is somewhat tomato-like in flavorand appearance, although the taste (sweet and sour) ismuch richer with a hint of tropical luxuriance. Goldenber-ries have been grown in Egypt, South Africa, India, New

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Journal of Food Biochemistry ISSN 1745-4514

708 Journal of Food Biochemistry 37 (2013) 708–722 © 2012 Wiley Periodicals, Inc.

Zealand, Australia and Great Britain (Morton 1987; McCain1993; Ramadan and Mörsel 2003, 2004). Internationalmarkets exist for many exotic fruits, and recently, the pro-cessing of tropical fruits started in many countries(Ramadan and Mörsel 2007). In 2005, there were more than1.8 million acres of berry crops worldwide, including966 acres of gooseberries (Strik 2007). The single plant mayyield 300 fruits and carefully tended plants can provide20–33 tons/ha. Fruits are long-lasting, can be stored forseveral months when well frozen. The fruit has been used asa good source of provitamin A, minerals, vitamin C andvitamin B-complex. Goldenberry juice yield is about 70% ofthe berry weight (Ramadan and Mörsel 2007). Sugarcontent in the juice is 4.9 g/100 g and the main compoundsare sucrose and fructose. Ascorbic acid level in goldenberry(46 mg/100 g) turns out to be higher than in most fruitssuch as pear peach (7 mg/100 g), and somewhat comparablewith orange (50 mg/100 g). In goldenberry, quercetin wasthe main phenolic compound, followed by myricetin andkaempferol (Häkkinen et al. 1999). Goldenberry juice is richin water and fat-soluble bioactive compounds and could bea novel source of functional drinks (Ramadan 2011).

Cholesterol is always an issue because blood total choles-terol (TC) and low-density lipoprotein (LDL) correlatestrongly with coronary heart disease (CHD). Cholesterolhomeostasis is maintained by a complex mechanism ofsterol absorption, anabolism, catabolism and excretion(Chen et al. 2011). Current research directions in nutritionindicate that fruits, vegetables, grains and oilseeds arereceiving increasing attention. The contribution of bioactivecompounds (phenolic compounds, vitamins, polyunsatu-rated fatty acids [PUFAs] and fat-soluble bioactives) inmany biological systems and many degenerative and CHDhas been studied. Hypercholesterolemia is a major riskfactor for the development and progression of atherosclero-sis and related cardiovascular diseases (Deepa and Varalak-shmi 2005). A high-cholesterol diet (HCD) is a majorcontributor to an unbalanced lipoprotein metabolism. It isassociated with an increased prevalence of atherosclerosis,which is the major source of morbidity and mortality in thedeveloped world, and it claims more lives than all types ofcancer (Stocker and Keaney 2004). Previous research hasindicated a positive correlation between blood cholesterollevel and the risk of cardiovascular diseases (Leys et al.2002). Despite the fact that there are drugs available clini-cally for treating hypercholesterolemia, the consumption offunctional foods in controlling blood cholesterol levels andrisk of CHD has gained enormous global acceptance overthe years. The concentration of blood cholesterol can beregulated by cholesterol biosynthesis, removal of cholesterolfrom the circulation, absorption of dietary cholesterol andexcretion of cholesterol via bile and feces (Vijaimohan et al.2006). In this study, we tested the hypothesis that consump-

tion of goldenberry juice provides an overall improvementto alleviate the detrimental outcomes associated with HCDof the liver and the cardiovascular systems. The goal was tostudy the impact of feeding goldenberry juice on the bloodprofile of rats upon feeding HCD, with the objective of pro-moting their use in functional foods and nutraceuticals.

MATERIALS AND METHODS

Materials

Ripe P. peruviana fruits were obtained from local growers inZagazig (Sharkia, Egypt). Intact fruits were carefully selectedaccording to the degree of ripeness measured by fruit color(brilliant orange), pH value of the pulp (3.86) and totaltitratable acidity (0.92%). 1,1-Diphenyl-2-picrylhydrazyl(DPPH, approximately 90%) was from Sigma Chemical Co.(St. Louis, MO). Caffeic acid was from Fluka AG (Buchs,Switzerland). Standards used for sterol (ST) characteriza-tion were purchased from Supelco (Bellefonte, PA). Stan-dards used for vitamin E (a-, b-, g- and d-tocopherol) werepurchased from Merck (Darmstadt, Germany). All solventsand reagents from various suppliers were of the highestpurity needed for each application.

Methods

Preparation of Berry Juice. Whole berries were blendedin a Waring blender (Moulinex Ovatio 3, Ecully Cedex,France) for 5 min and pasteurized at 80C for 10 min toinactivate the endogenous enzymes. After heat treatment,the pulp blends were cooled to room temperature. Toremove the seeds and skin residues (fruit pomace), the juicewas filtered through cheesecloth. Small aliquots (25 mL) ofeach juice (no food preservative was added) were stored at-20C. Samples of 25 mL were defrosted immediately beforethe experiments.

Chemical Composition of the Juice. Moisture, ash,protein, reducing sugars and nonreducing sugars weredetermined according to AOAC (1995). Ascorbic acid wasdetermined volumetrically with the 2,6-dichlorophenolindophenol reagent (AOAC 1995). Analytical and prepara-tive thin layer chromatography (TLC) separation of themain sugars in the juice was conducted on silica gelF254 plates (thickness = 0.25 mm; Merck), which activatedat 120C for 2 h immediately before use. Samples wereeluted using dichloromethane/acetic acid/methanol/water(50:25:15:10, v/v/v/v). Plates were air-dried and stained bymethanolic a-naphthol (5%), followed by 40% sulfuricacid. Identification of the bands was made, comparing theband of the references (Sigma Chemical Co.) on the sameTLC plate.

M.F. RAMADAN ET AL. HYPOCHOLESTERMIC PROPERTIES OF GOLDENBERRY JUICE

709Journal of Food Biochemistry 37 (2013) 708–722 © 2012 Wiley Periodicals, Inc.

Total Phenolic Compounds in Fruit Juice. The phenolcontent was measured by Folin–Ciocalteu reagent usingcaffeic acid as standard. One milliliter of juice was mixedwith 5 mL of Folin–Ciocalteu reagent (previously diluted30-fold with distilled water) and a 15 mL of sodium bicar-bonate (20 g/100 mL) and then the mixture was diluted to100 mL with distilled water. The solution was kept in thedark at room temperature for 2 h and then the absorbancewas measured at 760 nm using a Shimadzu UV-260 spectro-photometer (Kyoto, Japan). The mean value of total phe-nolic content was obtained from triplicate experiments.

Analysis of Bioactive Lipids in Juice. Juice samples(25 g) were lyophilized (Alpha 1–5; Martin Christ, Osterodeam Harz, Germany) to 10–25% of the original weight,ground (Analysenmühle A10; Janke and Kunkel GmbH,Staufen Br., Germany), and then the lipids were isolatedusing a chloroform/methanol extraction procedure. Thesamples were homogenized and blended in methanol(50 mL) for 1 min in a blender, chloroform (100 mL) wasadded and blending was contained for 2 more min. Themixture was filtered and the solid residue resuspended inchloroform/methanol (2:1, v/v, 150 mL) and blended for3 min. The mixture was filtered again and washed withfresh solvent (2:1, v/v, 150 mL). The combined filtrates werecleaned with a repeat addition of 0.2 volumes of 0.75%aqueous sodium chloride solution. The whole solution(combined filtrates and aqueous sodium chloride) wasthoroughly mixed without shaking, the layers were allowedto separate and the chloroform layer was recovered. Thepurified lipids was collected in a flask and subsequentlytreated with sodium sulfate to remove traces of water;after filtration, the extract was taken to dryness on arotary evaporator at 40C. Total lipids recovered wereweighed and stored in chloroform at -20C until analysis.Fatty acids, sterols, b-carotene and tocopherols were deter-mined in the lipid from the juice according to Ramadanet al. (2010).

Gas chromatography (GC) Analysis of Fatty AcidMethyl Esters (FAME). Fatty acids were transesteri-fied into FAME using N-trimethylsulfoniumhydroxide(Macherey-Nagel, Düren, Germany). FAME were identifiedon a Shimadzu GC-14A equipped with flame ionizationdetector (FID) and C-R4AX chromatopac integrator. Theflow rate of the carrier gas helium was 0.6 mL/min and thesplit value with a ratio of 1:40. A sample of 1 mL wasinjected on a 30 m ¥ 0.25 mm ¥ 0.2 mm film thicknessSupelco SP-2380 capillary column. The injector and FIDtemperature was set at 250C. The initial column tempera-ture was 100C programmed by 5C/min until 175C and keptfor 10 min at 175C, then 8C/min until 220C and kept for

10 min at 220C. A comparison between the retention timesof the samples with those of authentic standard mixture(Sigma; 99% purity specific for gas–liquid chromatography[GLC]), run on the same column under the same condi-tions, was made to facilitate identification.

GC Analysis of Sterols (ST). Separation of ST was per-formed after saponification of the oil sample withoutderivatization. Oil samples (250 mg) were refluxed with5 mL of ethanolic potassium hydroxide solution (6% w/v)and a few anti-bumping granules for 60 min. The unsaponi-fiables were first extracted three times with 10 mL of petro-leum ether, the extracts were combined and washed threetimes with 10 mL of neutral ethanol/water (1:1, v/v) andthen dried overnight with anhydrous sodium sulfate. Theextract was evaporated in a rotary evaporator at 25C underreduced pressure, and then ether was completely evaporatedunder nitrogen. GLC analyses of unsaponifiable residueswere carried out using a Mega Series (HRGC 5160; CarloErba Strumentazione, Milan, Italy) equipped with FID. Thefollowing conditions were carried out: DB 5 column (J&WScientific, Folsom, CA) packed with 5% phenyl methylpol-ysiloxane, 30 m in length, 0.25-mm inside diameter (i.d.),1.0-mm film thickness; carrier gas (helium) flow rate is38 mL/min (split-splitless injection was used). The detectorand injector were set at 280C. The oven temperature waskept constant at 310C and the injected volume was 2 mL.The repeatability of the analytical procedure was testedand the relative standard deviation of three repeated analy-ses of a single sample was <5%. Quantitative analyseswere performed with a Shimadzu (C-R6A chromatopac)integrator.

Normal Phase High-performance Liquid Chromato-graphy (NP-HPLC) Separation, Identification andQuantification of Tocopherols

Procedure. NP-HPLC was selected to avoid extra sampletreatment (e.g., saponification). Analysis was performedwith a solvent delivery LC-9A HPLC (Shimadzu). The chro-matographic system included a model 87.00 variable wave-length detector and a 250 ¥ 4 mm i.d. LiChrospher-Si 60,5 mm, column (Knauer, Berlin, Germany). Separation oftocopherol isomers was based on isocratic elution when thesolvent flow rate was maintained at 1 mL/min at a columnbackpressure of about 65–70 bar. The solvent systemselected for elution was isooctane/ethyl acetate (96:4, v/v)with detection at 295 nm. Twenty microliters of the dilutedsolution of total lipids in the mobile phase was directlyinjected into the HPLC column. Tocopherol isomers wereidentified by comparing their retention times with those ofauthentic standards.

HYPOCHOLESTERMIC PROPERTIES OF GOLDENBERRY JUICE M.F. RAMADAN ET AL.


Preparation of Standard Curves. Standard solutions wereprepared by serial dilution to a concentration of approxi-mately 5 mg/mL of each tocopherol isomer. Standard solu-tions were prepared from a stock solution, which was storedin the dark at -20C. Twenty microliters was injected andpeak areas were determined to generate standard curve data.

Quantification. All quantitation was by peak area usingShimadzu C-R6A chromatopac integrator. Standard curves(concentration versus peak area) were calculated from sixconcentration levels by linear regression. Based on theestablished chromatographic conditions, repeated injectionsof different concentrations of the standard tocopherols weremade three times onto the HPLC system. Injections in trip-licate were made at each concentration for both standardsand samples. All work was carried out under subdued lightconditions.

Radical-Scavenging Activity of Juice (DPPHTest). The radical-scavenging activity of P. peruviana juicewas tested as bleaching of the stable DPPH radicals. Thereaction mixture contained 390 mL of ethanolic 10-4 MDPPH and 100 mL of the juice sample. The mixture wasvortexed for 20 s at ambient temperature. Against a blank ofpure ethanol without DPPH, the decrease in absorption at515 nm was measured in 1-cm quartz cells after 1, 30 and60 min of mixing using UV-260 visible recording spectro-photometer (Shimadzu). Radical-scavenging activity towardDPPH radicals was estimated from the differences in absor-bance of methanolic DPPH solution with or withoutsample (control), and the inhibition percent was calculatedfrom the following equation according to Ramadan andMörsel (2003):

% inhibition = [(absorbance of control - absorbance oftest sample)/absorbance of control] ¥ 100.

All results presented are mean values of at least threeexperiments, wherein no statistically significant difference(P > 0.05) was found among the experiments.

Animal Experiment. Fruit juice was incorporated intothe experimental diets and the full composition of experi-mental diets is detailed in Table 1. The basal diet includedwheat starch, casein, cellulose, and mineral and vitaminmixtures. Table 2 presents the composition of minerals andvitamins in the diet used in this study. The work was carriedout at the Agricultural Biochemistry Department, Faculty ofAgriculture, Zagazig University. To study the effect of twoconcentrations of goldenberry juice (5 and 15%) on thelipid profile of albino rats, 20 male albino rats (weighingbetween 120 and 140 g) were used for this investigation.The experiment lasted for 60 days and the animals weredivided into four groups, each contained five rats. Animalgroup numbers 3 and 4 represent control groups, whereingroup 4 fed basal diet as negative (-) control, while controlgroup 3 received HCD until the end of the experiment toserve as the positive (+) control. Groups 1 and 2 wereallowed to feed hypercholesterolemic diet (1% choles-terol + 0.25% colic acid) supplemented with goldenberry

TABLE 1. CHEMICAL COMPOSITION (g/kg) AND CALCULATED ANALYSIS OF EXPERIMENTAL DIETS

HCD HCD (positive control) CFD (negative control)

Group 1 (5% juice) Group 2 (15% juice) Group 3 Group 4

Casein 150 150 150 150Starch 687.5 578.5 727.5 747.5Goldenberry juice 50 150 – –Salt mixture 40 40 40 40Vitamin mixture 10 10 10 10Cellulose 50 50 50 50Colic acid 2.5 2.5 2.5 2.5Cholesterol 10 10 10 –Sheep tail fat – – 10 –

HCD, high-cholesterol diet.

TABLE 2. COMPOSITION OF VITAMINS AND MINERAL MIXTURE INDIET*

Vitamin Quantity Mineral Quantity

Vitamin A 2,000 IU NaCl 0.5%Vitamin D 200 IU KI 0.013%Vitamin E 75 IU K2HPO4 1.62%Vitamin K 0.5 mg MgSO4 0.325%Inositol 10 mg CaCO3 1.5%Niacin 4.0 mg CaHPO4 0.30%Ca pantothenate 4.0 mg FeSO4 0.125%Riboflavin 0.8 mg CuSO4 0.0015%Thiamin HCL 0.5 mg MnSO4 0.011%Pyridoxine 0.5 mg ZnSO4 0.00916%Folic acid 0.2 mgBiotin 0.04 mgVitamin B12 0.003 mgCholine chloride 200 mgPara amino benzoic acid 10 mg

* Starch was added to make 1,000 mg.



juice (5%, group 1; 15%, group 2), as mentioned in Table 1.The rats were housed in cages with screen bottom in a con-trolled room with 12-h light and 12-h dark cycles. Diets andwater were available over the 60-day period and rats wereweighed every week. All groups were fed the basal diet for10 days as adaptation period.

Blood Sampling and Analysis. Blood samples were col-lected by sacrificing all groups after overnight fasting andblood samples were collected into anticoagulant tubes andthen centrifuged at 3,000 rpm for 15 min to obtain theplasma, which was kept frozen until analysis. TC was ana-lyzed according to Richmond (1973). Total lipids weredetermined by the reaction of total lipids with sulfophos-phovanillic mixture according to Coudon and Bouige(1973). According to Demacker et al. (1984), LDL-cholesterol was determined as the difference between TCand the high-density lipoprotein (HDL)-cholesterol contentof the supernatant after precipitation of the LDL fraction bythe polyvinyl sulfate in the presence of polyethylene glycolmonomethyl ether. Triacylglycerols (TAGs) were analyzedaccording to Fossati and Prencipe (1982).

Liver and Kidney Functions Tests. Serum glutamicpyruvate transaminase (SGPT), serum glutamic oxaloacetictransaminase (SGOT), total serum protein, serum albuminand serum globulins were determined according to Reitmanand Frankel (1957), Henry (1964), Doumas et al. (1971)and Reinhold (1953). Kidney functions, including serumuric acid and urea, were determined according to Pattonand Crouch (1977).

Histopathological Examinations. Randomly selectedthree male rats from each treated group were anesthetizedunder ether and sacrificed by cervical dislocation at the endof the experimental period. For histopathological examina-tion, vital organs such as kidney and liver tissues were dis-sected out and examined grossly. Subsequently, the tissuespecimens were taken and fixed in 15% formalin saline forthe histopathological alternations. The fixed tissues wereprocessed by dehydration in a series of graded ethanol con-centrations, cleared with xylol and embedded in paraffinblocks. Sections of 4-mm thick were obtained and stained byhematoxylin and eosin method for further analysis in a lightmicroscope for histopathological changes, as described pre-viously (Ratcliffe 1982).

Statistical Analysis. Results are presented as mean �

standard deviation of the means. One-way analysis of vari-ance was used to ascertain if the dietary treatments were asource of variance related to the various lipid parameters

measured. If a significant F-test was noted, means wereseparated using critical difference. A level of P < 0.05 wasconsidered significant.

RESULTS

Chemical Composition and BioactiveCompounds in Juice

The chemical composition of P. peruviana juice is presentedin Table 3. The yield of juice produced from P. peruvianawas 71.8% of the total berry weight. The results indicatedthat the chemical constituents analyzed were within therange of values reported previously (Popenoe et al. 1990).Total reducing and nonreducing sugars of the goldenberryjuice are presented in Table 3. Total sugar content was4.90 g/100 g. TLC analysis showed that the preponderantcarbohydrates of the goldenberry cell wall are, in decreasingorder: sucrose (35 g/100 g total sugar), fructose (29 g/100 gtotal sugar) and glucose (25 g/100 g total sugar). It is worthyto mention that the approximate sugar content in othercommon fruit juices was reported to be in pear (9.8%),orange (7.0%), apple (11.1%), peach (8.5%), strawberry(5.7%), pineapple (12.3%), raspberry (4.5%), plum (7.8%)and apricot (6.1%) (Gurrieri et al. 2000). The resultsobtained from the determination of ascorbic acid (vitaminC) and total phenols in goldenberry juice are reported inTable 3. Interestingly, vitamin C is present in high amounts(46 mg/100 g). The ascorbic acid content in goldenberry, onaverage, turns out to be higher than in most common fruitssuch as pear (4 mg/100 g), apple (6 mg/100 g), peach (7 mg/100 g), pineapple (25 mg/100 g), plum (3 mg/100 g) andapricot (9 mg/100 g), and only slightly lower than otherfruits such as orange (50 mg/100 g) or strawberry (60 mg/100 g) (Belitz and Grosch 1999; Gurrieri et al. 2000). Thestudy of the phenols in fruits is of great interest, owing tothe qualitative and quantitative differences appearing as afunction of the species, cultivar, degree of ripening and

TABLE 3. COMPOSITION OF PHYSALIS PERUVIANA JUICE

Moisture (g/100 g juice) 92.7 � 2.35Ash (g/100 g juice) 1.01 � 0.07Protein (g/100 g juice) 0.44 � 0.01Carbohydratea (g/100 g juice) 5.65 � 0.22Lipids (g/100 g juice) 0.20 � 0.02Total sugar (g/100 g juice) 4.90 � 0.16Total reducing sugars (g/100 g juice) 3.09 � 0.13Total nonreducing sugars (g/100 g juice) 1.81 � 0.09Vitamin C (mg/100 g juice) 46 � 1.22Total phenolics (mg/100 g juice) 6.30 � 0.36

Values given are the mean of three replicates � standard deviation.a % carbohydrate = 100 - (% protein + % lipids + % moisture + %ash).



environmental conditions of growing, ripening as well asstorage. Good amount of phenolics was estimated in gold-enberry juice (Table 3), wherein the level of total phenols, asdetermined by Folin–Ciocalteu method, was 6.30 mg/100 gjuice as caffeic acid equivalents.

Lipid Content and Composition ofFruit Juice

In the present study on goldenberry, it was found that thejuice contains ca. 0.2% oil (on fresh weight basis). Analysisof FAME gave the proportion of linoleic, oleic, palmitic,g-linolenic (GLA) and palmitoleic esters as the majorFAME. According to the results shown in Table 4, 15 fattyacids were identified. Linoleic and oleic were the main fattyacids, wherein the ratio of linoleic acid to oleic acid wasabout 1:1. Palmitic acid (ca. 19.3%) followed by stearic acid(ca. 1.87%) were the major saturated fatty acids. The juicewas characterized by a relatively high amount of saturatedfatty acids, which comprised more than 22.7% of the totalFAME. Five minor fatty acids, namely gadoleic, dihomo-g-linolenic (DHGLA), erucic, lignoceric and nervonic acids,were also identified. The juice could be a good source ofPUFAs. The total content of trienes was about 22.7% andthe oil was characterized by extremely high level of GLA(18.8% of the total FAME), while w-3 fatty acid (a-linolenicacid) and DHGLA were estimated to be in lower levels.

Interest in the PUFA as health-promoting nutrients hasexpanded dramatically in recent years, with rapidly growingliterature illustrating their benefits (Riemersma 2001).The fatty acid composition and the high amounts ofPUFA make P. peruviana a special fruit for nutritionalapplications.

Phytosterols represent a group of the most importantbioactive compounds. They are of interest because of theirantioxidant activity and their impact on health. The contentand composition of sterols determined in goldenberry juiceare shown in Table 4. The major sterols detected were,in order of decreasing prevalence, D5-avenasterol >campesterol > ergosterol > lanosterol > stigmasterol > b-sit-osterol > D7-avenasterol. D5-Avenasterol and campesterolwere detected at equal levels and comprised together about44% of the total sterols. Furthermore, ergosterol was pre-sented in a relatively higher amount (ca. 16.6% of totalsterols). Data about the qualitative and quantitative compo-sition of vitamin E are summarized in Table 4. Vitamin Elevel was extremely high, wherein g- and a-tocopherolswere the main constituents. a-Tocopherol is the most effi-cient antioxidant of these compounds. b-Tocopherol has25–50% of the antioxidative activity of a- and g-tocopherol,10–35%. Goldenberry juice could be a novel source of func-tional drinks without a need of fortification with fat-solublebioactives.

Antiradical Action of Goldenberry Juice

The antioxidant activity of the juice was assessed by meansof DPPH test and the resulting values were correlated witheach one of these classes of antioxidant compounds. Gold-enberry juice showed an evident antioxidant effect (Fig. 1).The juice produced a 78% decrease versus the absorbance of

TABLE 4. LEVELS OF FATTY ACIDS (%), STEROLS AND TOCOPHEROLSIN PHYSALIS PERUVIANA JUICE

Fatty acid Compoundb

C12:0 0.25 � 0.03 Ergosterol 9.23 � 0.23C14:0 1.09 � 0.07 Campesterol 12.2 � 0.69C16:0 19.3 � 0.12 Stigmasterol 6.23 � 0.55C16:1n-7 7.52 � 0.09 Lanosterol 6.55 � 0.36C18:0 1.87 � 0.05 b-Sitosterol 5.23 � 0.56C18:1n-9 22.2 � 0.13 D5-Avenasterol 12.5 � 0.73C18:2n-6 22.7 � 0.08 D7-Avenasterol 3.71 � 0.32C18:3n-6 18.8 � 0.09 Total sterols 55.6 � 3.52C20:0 0.21 � 0.02C18:3n-3 0.63 � 0.02 a-Tocopherol 28.3 � 0.45C20:1n-9 0.15 � 0.01 b-Tocopherol 15.2 � 0.85C20:3n-6 2.31 � 0.04 g-Tocopherol 45.5 � 2.35C22:1n-9 0.91 � 0.06 d-Tocopherol 1.50 � 0.05C24:0 0.65 � 0.04 Total vitamin E 90.5 � 2.98C24:1n-9 1.12 � 0.03Total saturates 22.7 � 0.12Total monoenes 31.9 � 0.09Total dienes 22.7 � 0.08Total trienes 21.7 � 0.10S/U ratio (%)a 29.4

Values are given as mean of three replicates � standard deviation.a Ratio of saturated fatty acids to unsaturated fatty acids.b Grams per kilogram of total lipids.

FIG. 1. SCAVENGING EFFECT AT DIFFERENT INCUBATION TIMES OFPHYSALIS PERUVIANA JUICE ON 1,1-DIPHENYL-2-PICRYLHYDRAZYL(DPPH) RADICAL AS MEASURED BY CHANGES IN ABSORBANCEVALUES AT 515 NM



DPPH radicals’ control solution at a volume of 10 mL. Theantioxidant activity of goldenberry juice is not a property ofa single compound, but a synergistic effect of different anti-oxidant existing in the juice. Phenolic compounds arereported to be responsible for the antioxidant activity offruit juices (Meyer et al. 1995). On the other hand, there isevidence that ascorbic acid plays a minor role in the totalantioxidant efficiency of juices. Wang et al. (2002) evaluatedthat the contribution of vitamin C to the total antioxidantactivity of a fruit, which was less than 15%. Moreover,Miller and Rice-Evans (1997) underlined the significant roleof phenols to the antioxidant activity of long-life orangejuice, even if vitamin C was the most abundant antioxidant.The presence of a good amount of phenolics in goldenberryjuice could contribute to the high level of antioxidantcapacity determined in this study.

Impact of Feeding Juice on Blood Profile

The obtained results stated that hypercholesterolemic statewas accompanied by an increase in blood glucose, whichrecorded the highest level for the positive control group(125 mg/dL). The increase of glucose might be due toimpaired function of liver, which is reported to play animportant role in the regulation of blood glucose. Alterna-tively, it may be due to the lowered circulating insulin levelcaused by the high level of glucose. Feeding with fruit juiceresulted in significant reduction of glucose levels (82–105 mg/dL). Treated rats exhibited a significant decrease inglucose concentration, which can be explained by the incor-poration of circulating glucose as hepatic glycogen.

TAG

TAG in the blood tends to damage vascular endothelial cells,leading to heart disease. High-fat diet produces an increase

in TAG levels due to lipoprotein lipase TAG hydrolysis, sothe accumulation in the liver becomes more evident (Feoliet al. 2003). In contrast, the effect of PUFA can be attributedto a reduction in the hepatic synthesis of fatty acid, whichdecreases the concentration of TAG in the liver. The data inFig. 2 show the levels of TAG of hyperlipidemic rats fedfruit juice. After 60 days, the data revealed that all groupsshowed a decrease in TAG in comparison with the positivecontrol group. Group 2 (15% juice) possessed the lowestlevel of TAG in comparison with other groups. These effectsmight be due to high plasma lipoprotein lipase activity, anenzyme involved in hydrolysis of the plasma very-low-density lipoprotein TAGs.

TC

The rise in cholesterol in liver and plasma may be due toincreased uptake of exogenous cholesterol and subsequentdeposition and decreased cholesterol catabolism, as evi-denced by a reduction in bile acid production and turnoverof bile acids. The metabolism of free and ester cholesterol isimpaired in liver, spleen and thymus tissue, and the rate ofturnover was specifically decreased in all tissues of hyper-lipidemic rats (Choi et al. 2001; Feoli et al. 2003). After 60days of feeding, the data show that group 4 (CFD) had thelowest TC, followed by group 2 in comparison with theHCD group (Fig. 3). Feeding rats with fruit juice (15%)caused a decrease in TC by 31.6% compared with the posi-tive control group.

HDL-cholesterol

The inverse association between the incidence of CHD andHDL-cholesterol levels has been known. HDL is an impor-

FIG. 2. IMPACT OF FEEDING GOLDENBERRY JUICE ON TOTAL TRIACYLGLYCEROLS (TAGs)Values given are the mean of three replicates, and error bars show the variations of three determinations in terms of standard deviation.



tant scavenger of surplus cholesterol, transporting it fromthe cell membrane to the liver where it is metabolized orconverted into the bile acids. However, the mechanism ofthe increase of HDL-cholesterol is not at all clear. After 60days of feeding experiment, it was generally noted that thelevels of HDL significantly increased in both groups (1 and2) compared with the control groups (Fig. 4). The highestincrease of HDL was measured in group 1 (35 mg/dL) thatwas fed with 5% fruit juice. Supplementation of diet withgoldenberry juice increased the rate of HDL-cholesterol.HDL plays an important role in the transport of cholesterolfrom peripheral cells to the liver, and hence the elevated

HDL-cholesterol levels by dietary goldenberry juice are con-sidered to be favorable as there is a negative correlationbetween HDL-cholesterol levels and CHD risk.

LDL-cholesterol

The oxidation of lipids and proteins in lipoproteins and cellmembranes leads to impairment of lipid transport and tocell injury, and thereby contributes to the development ofvarious diseases. LDL carries cholesterol from the liver tothe peripheral cells and smooth muscle cells of the arteries;a rise in LDL may cause deposition of cholesterol in the

FIG. 3. IMPACT OF FEEDING JUICE AND POMACE ON TOTAL CHOLESTEROLValues given are the mean of three replicates, and error bars show the variations of three determinations in terms of standard deviation.

FIG. 4. IMPACT OF FEEDING GOLDENBERRY JUICE ON THE LEVELS OF HIGH-DENSITY LIPOPROTEIN (HDL)-CHOLESTEROLValues given are the mean of three replicates, and error bars show the variations of three determinations in terms of standard deviation.



arteries and aorta, and hence is bad for health and is a directrisk factor for CHD (Ramadan et al. 2008a,b). Accumula-tion of LDL (bad cholesterol) within the arterial wallappears to play a crucial role in the initiation and progres-sion of atherosclerotic plaque. After 2 months, the datashowed that LDL levels were decreased (Fig. 5) in all treat-ments compared with the control groups. The highestdecrease (ca. 56.6% compared with the HCD group) of LDLwas detected in group 2.

Liver Functions

Figure 6 shows the effect of administrating goldenberryjuice on the liver functions (GPT and GOT) of hypercholes-terolemic rats. Hypercholesterolemia (group 3) was charac-terized by a significant increase in SGPT. The highest levelof GPT was 14.8 U/L in the positive control group, while thelevels 7.0–10.0 U/L in groups feed with juice. The increasein serum GPT activity indicates liver cell necrosis and

FIG. 5. IMPACT OF FEEDING GOLDENBERRY JUICE ON THE LEVELS OF LOW-DENSITY LIPOPROTEIN (LDL)-CHOLESTEROLValues given are the mean of three replicates, and error bars show the variations of three determinations in terms of standard deviation.

FIG. 6. IMPACT OF FEEDING JUICE ON THE TRANSAMINASE ACTIVITIESValues given are the mean of three replicates, and error bars show the variations of three determinations in terms of standard deviation.GOT, glutamic oxaloacetic transaminase; GPT, glutamic pyruvate transaminase.



hepatic injury. Treatment with juice induced a decrease inthe high activity of GPT and the levels were decreased com-pared with the positive control group after 2 months ofadministration. Also, hypercholesterolemia (group 3) wascharacterized by an increase in GOT. The increase of GOTactivity was more specific for cardiac injury. The amountsof GOT were 6.25–10.3 U/L in groups feed juice. Thehighest level of GOT was 13.6 U/L in the positive controlgroup. GOT and GPT were high as shown in Fig. 6 and thedata agreed with those of Daher et al. (2006).

Hypercholesterolemic state was accompanied by a highincrease in total serum protein, albumin and globulin(Fig. 7). There was a remarkable decrease for groups treatedwith juice. Total protein value for group 3 (positive control)was 7.5 gm/dL, wherein the values were lower for groupstreated with juice (5.5 gm/dL). Concerning serum albu-min, groups treated with juice also recorded loweramounts (2.80–2.97 gm/dL), while positive control group

recorded the highest amount (4.8 gm/dL). Globulin levelsreached also the highest levels for the positive controlgroup, while the negative control group recorded the lowestlevel.

The hyperlipidemia was accompanied by an increase inkidney function parameters. Feeding with juice resulted inreduction of uric acid and urea levels at the end of theexperiment. Uric acid (Fig. 8) level was the highest for thepositive control group (4.94 mg/dL). Blood urea is a majornitrogenous component of the urine. An increased urinaryconcentration of urea was observed in the states with pro-nounced catabolism of proteins and other nitrogenouscomponents (starvation, burns, traumatism and atrophy oftissues, etc.). A decreased excretion of urea is observed inaffected liver (urea-producing organ) and in impairedglomerular filtration of blood. According to the obtainedresults presented in Fig. 8, rat groups fed with goldenberryjuice recorded lower urea levels (37.5–47 mg/dL) after 60

FIG. 7. IMPACT OF FEEDING JUICE ON PROTEIN FRACTIONSValues given are the mean of three replicates, and error bars show the variations of three determinations in terms of standard deviation.

FIG. 8. IMPACT OF FEEDING GOLDENBERRY JUICE ON UREA AND URIC ACIDValues given are the mean of three replicates, and error bars show the variations of three determinations in terms of standard deviation.



days of feeding in comparison with the positive controlgroup (51.4 mg/dL), while the negative group reached40.6 mg/dL.

Histological Profile of Liver and Kidney

The gross appearance of the liver from rats fed with normaldiet, HCD and HCD plus goldenberry juice was monitored.The liver of control (negative) rats has a relatively dark-redcolor, whereas the HCD-fed rats have an enlarged liverwith a yellowish color. The weight of liver in normal diet-fed rats was 13.22 � 0.50 g and HCD-fed was 20.39 �

0.74 g, whereas HCD plus goldenberry juice-fed was18.15 � 0.36 g. In rats fed with HCD plus goldenberryjuice, there was not as much enlargement of the liver (with arelatively “lesser yellowish” color) as that observed in HCD-fed rat. Histological examination of the livers of control ratsand HCD with juice-fed rats revealed intact cell architecture(Fig. 9A–D). In contrast, the liver of HCD-fed rats illus-trated poor cellularity, with extensive lipid depositions andenlarged hepatocytes (Fig. 9B). In goldenberry juice-fed rats(Fig. 9C,D), a lesser degree of lipid deposition and hepato-cytes enlargement was observed.

Figure 10A–D showed histological examination of thekidney of control rats and goldenberry juice-fed rats.Kidney tubules of the negative control rats (Fig. 10A)showed mild dilatation in the renal tubules of both cortexand medulla and degenerative changes in the epithelium ofsome tubules. In the positive control group (Fig. 10B),kidney tubules showed mild dilatation in some tubules anddegenerative changes in the epithelium of other tubules. Ingroup fed 5% goldenberry juice (Fig. 10C), tubules showeddilatation in moderate number of the renal tubules in bothcortex and medulla, vacuolation of the epithelium of somerenal tubules and perivascular edema. While in group fed15% goldenberry juice (Fig. 10D), tubules showed moderatetubular dilatation, degenerative changes in the tubular epi-thelium and perivascular edema. All groups were comparedwith the negative control group, in which liver hepatic tissueand kidney tubules were apparently normal.

DISCUSSION

The basic concepts of nutrition are undergoing significantchange. The classical concept of “adequate nutrition,” thatis, a diet that provides nutrients in sufficient quantities tosatisfy particular organic needs, is tending to be replaced bythe concept of “optimal nutrition,” which includes, besidesnutrients, the potential of food to promote health, improvegeneral well-being and reduce the risk of certain illnesses.This is where functional foods, also known as nutraceuti-cals, therapeutic foods, superfoods or medicinal foods, playtheir part (Nagai and Inoue 2004).

Cholesterol can be good or bad, depending on its concen-tration, circulation, accumulation and abnormal depositionwithin the body. On one hand, cholesterol is essential as ithas four major functions in all animal life. First, cholesterolis an important compound in cell membranes as it canregulate the membrane over a range of physiological tem-peratures. Second, cholesterol is a precursor for the synthe-sis of bile acids, which are emulsifiers of dietary fats and fat-soluble vitamins for digestion and absorption in the smallintestine. Third, it is a substrate for the synthesis of all ste-roidal hormones, including sex hormones, glucocorticoidsand mineralocorticoids. Fourth, vitamin D is derived from acholesterol derivative, 7-dehydrocholesterol. On the otherhand, cholesterol is one of “culprits” that has been used an

FIG. 9. HEPATIC CELLS FROM THE LIVER OF (A) NEGATIVE CONTROLRATS; (B) POSITIVE CONTROL RATS; (C) RATS TREATED WITH 5%GOLDENBERRY JUICE; AND (D) RATS TREATED WITH 15%GOLDENBERRY JUICE



an indication of general heart health. Epidemiologicalstudies have demonstrated a strong association betweenblood cholesterol concentration and CHD risk. A stronglink is also seen between a diet rich in cholesterol and theprevalence of CHD (Chen et al. 2011).

Hyperlipidemia has been implicated in atherosclerosis,which is the leading cause of death among the world’spopulation. HCD increases blood LDL levels and oxidativestress, which results in increased oxidized LDL levels andthereby increases atherosclerotic plaque formation. It cansignificantly increase the risk of developing CHD, also calledcoronary artery disease or coronary disease. People withCHD develop thickened or hardened arteries in the heartmuscle. Efforts to develop effective and better hypolipi-demic drugs had led to the discovery of natural agents.Therefore, one of the aims of the present study was toevaluate the impact of goldenberry juice as hypolipidemicagents.

The hypocholesterolemic and atheroscleroprotectivepotentials of dietary consumption of goldenberry juice were

investigated by monitoring the blood profiles in rats fedwith either normal diet, HCD or HCD supplemented withgoldenberry juice. In HCD-fed rats, an increased blood TCand LDL-cholesterol with a decreased HDL-cholesterol wasobserved, and consumption of goldenberry markedly sup-pressed the elevated TC and LDL levels plus an increasedHDL-cholesterol level. HDL has been indicated as a positivefactor in determining the development of atherosclerosis(Miller and Miller 1997). In contrast to the adverse effects ofelevation of LDL, the concentration of HDL is inversely cor-related with atherosclerosis development, apart from its rolein reverse cholesterol transport (Penumathsa et al. 2007;Khera and Rader 2010), and as an antioxidant inhibits theoxidative modification of LDL (McPherson et al. 2007). Pre-vious epidemiologic studies suggested that a high intake offruit and vegetables is associated with a reduced risk ofCHD (Bors et al. 1990). The beneficial effect could berelated to minor components, especially flavonoids, whichare proposed to exert their action by inhibiting LDL oxida-tion and platelet aggregation (Cook and Samman 1996).Phenolic compounds have important pharmacologicalproperties and have been associated with a lowered risk ofCHD via their action toward LDL. Phytosterols in fruit juicemay also play an important role in the decrease of plasmaTC and LDL-cholesterol. Numerous studies have noted thatphytosterols induce a decrease in lipoprotein cholesterollevels in total plasma, but the mode of their action is notfully understood. It has been hypothesized that these com-pounds provoke a decrease in cholesterol solubility and itsabsorption across the intestinal barrier, inducing conse-quently low plasma cholesterol levels (Wasan et al. 2001). Ithas been demonstrated that these compounds prevent ordelay the development of atherosclerotic lesions (Jones et al.1999). Other compounds, such as b-carotenes and vitaminE, are present in fruit juice and could prevent the structuralalteration of lipoproteins (Charleux 1996; Kurowska et al.2000; Ramadan and Mörsel 2007, 2009).

Blood TC and LDL-cholesterol correlate directly with therisk of CHD, whereas HDL-cholesterol correlates inverselywith risk. Dietary fatty acids affect plasma cholesterol levellargely mediated by their interaction with two transcrip-tional factors, sterol regulatory element binding protein-2(SREBP-2) and liver X receptor (LXR-a) (Kastelein 2007).SREBP-2 governs the transcription of LDL receptor(LDL-R) and 3-hydroxy-3-methylglutary-CoA (HMG-CoA) reductase (HMGR). LDL-R is responsible for theremoval of LDL-cholesterol from the circulation, whereasHMGR is a key enzyme in cholesterol synthesis in liver. Onthe other hand, LXR-a regulates the transcription ofCYP7A1-encoding cholesterol 7a-hydroxylase, which is arate-limiting enzyme in conversion of cholesterol to bileacids in the liver and is responsible for elimination of exces-sive cholesterol in the bile (Guan et al. 2011).

FIG. 10. KIDNEY TUBULES OF (A) NEGATIVE CONTROL RATS;(B) POSITIVE CONTROL RATS; (C) RATS TREATED WITH 5%GOLDENBERRY JUICE; AND (D) RATS TREATED WITH 15%GOLDENBERRY JUICE



Several possible mechanisms may be proposed to accountfor the improved hypercholesterolemia by goldenberryjuice. First, the fecal excretion pathway may be involvedbased on the observed decrease in lipid digestibility andincrease in fecal cholesterol concentration. The n-3 fattyacids, including ALA, are reported to lower serum TAGlevels (Cunnane et al. 1993; Craig 1999). The data are in linewith the antiradical action and levels of antioxidants in thefruit juice.

CONCLUSIONS

The results of the in vivo experiment indicate that theadministration of goldenberry juice has a profound influ-ence on the metabolism of lipids in rats fed with a HCD.Goldenberry juice positively affects the blood profile of ratsfed with a HCD. The TC, LDL and TAG concentrations inthe goldenberry juice diet groups were significantly lowerthan those in the positive control group. The positive influ-ence on blood lipids was high in the groups of rats fed withgoldenberry juice, which possesses high antioxidant poten-tial. The results suggest that consumption of goldenberryjuice has significant hypocholesterolemic activities in ratsfed with HCD. In addition, goldenberry supplement seemsto protect the liver in response to oxidative stress (probablyvia the elevation of antioxidant enzymes levels) as well asalleviate the magnitude of fatty liver development inresponse to HCD. Therefore, it could be suggested that theuse of goldenberry juice with high antioxidant potential bypatients suffering from CHD would prevent development ofthese diseases.

ACKNOWLEDGMENT

This study was supported by the research fund from ZagazigUniversity (Egypt).

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