Effects of the incorporation of cantaloupe pulp in
yogurt: Physicochemical, phytochemical and
rheological properties
F Kermiche
1, L Boulekbache –Makhlouf
1, M Fe
´lix
2,
L Harkat-Madouri
1,3, H Remini
1,4, K Madani
1and A Romero
2Abstract
The therapeutic effects of cantaloupe are of great interest for the development of functional foods such as yogurt. In this study a new dairy product has been formulated by enriching natural yogurt with fruit cantaloupe (yogurt with cantaloupe puree, yogurt with dry cantaloupe and yogurt with dry cantaloupe and cantaloupe puree). Thus, composition (moisture, ash, lipids, proteins), including amino acid contents, lactic flora as well as rheological (viscoelasticity, viscosity) property of cantaloupe yogurt and natural yogurt is assessed. In addition, pH value, water holding capacity and antioxidant activity (reducing power) are measured over refrigerated storage time. There are significant differences between natural yogurt and cantaloupe yogurt in almost all parameters. The results show that the pH decreases during the storage period and the antioxidant activity as well as the water holding capacity are more remarkable in the yogurt with dry cantaloupe at the 14th and the 28th day of storage, respectively. The addition of cantaloupe in natural yogurt ameliorates the load of lactic flora and modifies the rheological property of the new products. The results of the current study show that the addition of cantaloupe to yogurt significantly improved its quality.
Keywords
Yogurt, physical properties, phytochemicals, rheology, microstructure Date received: 2 February 2018; accepted: 10 April 2018
INTRODUCTION
Yogurt is a fermented fresh food which is one of the most popular dairy products available and widely con-sumed over the world. A very wide range of yogurt (reduced fat yogurt, pro biotic yogurt, yogurt mousses, yogurt ice cream, liquid yogurt drinks) is available in the market, with surprising diversification in terms of quality and price. Currently, the food market forces the industries concerned to formulate new products that meet the requirements of the consumer, from the func-tional properties, nutrifunc-tional and therapeutic point of view. Yogurt is produced by acid coagulation (fermen-tation of lactose) of milk by action of microorganisms
such as Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophiles (Fiorda et al., 2016), with the contribution of other lactic acid bacteria, which shows very interesting gastrointestinal health benefits such as lactose intolerance, constipation, diarrheal
1
Laboratoire de Biomathe´matiques, Biophysique, Biochimie, et Scientome´trie (L3BS), Faculte´ des Sciences de la Nature et de la Vie, Universite´ de Bejaia, Bejaia, Alge´rie
2Departamento de Ingenierı´a Quı´mica, Facultad de Fı´sica, Universidad de Sevilla, Sevilla, Spain
3Faculte´ des Sciences Biologiques, Universite´ des Sciences et de la Technologie Houari Boumediene, Alger, Alge´rie
4De´partement de Biologie, Faculte´ des Sciences de la Nature et de la Vie et des Sciences de la Terre, Universite´ de Bouira, Bouira, Alge´rie
Corresponding author:
A Romero, Departamento de Ingenierı´a Quı´mica, Facultad de Quı´mica, Universidad de Sevilla, Sevilla 41012, Spain.
Email: alromero@us.es
Food Science and Technology International 24(7) 585–597 !The Author(s) 2018 Article reuse guidelines:
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diseases, colon cancer, inflammatory bowel disease and Helicobacter pyloriinfection (Bernat et al., 2015).
Indeed, the lactic acid bacteria contribute to different functional properties of food systems through the diver-sity of their biopolymers (Muro Urista et al., 2011). Yogurt is a good source of essential nutrients as protein, carbohydrate, vitamins and minerals (Papastoyiannidis et al., 2006). In addition, it is a dairy product which can be consumed by people with lactose intolerance, due to its good digestibility compared to that of milk. This good digestibility leads to the improvement of bowel function in human (Bernat et al., 2015).
The addition of fruits to yogurt is a common applica-tion which enhances its funcapplica-tionality, taste and thera-peutic properties (Papastoyiannidis et al., 2006). Cucumis melo, Cucurbitaceae plant, cultivated in all trop-ical regions of the world (Nattaporn, 2011), is among the plants of great economic importance (Solval et al., 2012). In Algeria, about 1,495,081 t of cantaloupe fruit are pro-duced in 2012. It is widely consumed in the world because of its sweet aromatic flavour and nutritional quality, tex-ture and flavour/aroma (Nattaporn, 2011; Solval et al., 2012). Cantaloupe fragrance is used in an industrial scale to improve the flavour of snacks and desserts. It is known for its high nutritional value, and it is a good source of vitamin C, polyphenols, carotenoids, fibres and potas-sium, with potent antioxidant and anti-inflammatory properties (Nattaporn, 2011; Solval et al., 2012).
So, for its abundance, low cost, sweet flavour, nutri-tional and pharmacological values, it would be interest-ing to incorporate cantaloupe fruit in the product milk such as yogurt. That’s why, we use the pulp of canta-loupe instead of its extracts, in order to improve the overall nutrients of the yogurt and to save the time, the energy and the organic solvents which are involved in the extraction of the bioactive substances. This alter-native is more favourable from an economic point of view. On the other hand, in addition to the fresh pulp, we used the dried fruit because the cantaloupe is a sea-sonal plant, so its drying is an alternative solution that allows the extending of its shelf life.
Therefore, in this study we propose the development of a new product ‘Novel food’ by the formulation of yogurt with cantaloupe fruit. Thus, our main objectives are (1) the valorization of the varieties of C. melo Cantaloupe, local fruit, which is widely distributed in Algeria; (2) the development of a new product by the formulation of cantaloupe-based yogurt (fresh pulp, dried pulp and dried and fresh pulp mixture).
MATERIALS AND METHODS
Materials
Cantaloupe samples. Fresh cantaloupe (C. melon) was obtained from the local market (Bejaia, Algeria).
These latter were cut, peeled and diced into smaller pieces. The cantaloupe puree (CP) was extracted using a blender (Rhinos Electronics HB950S, 55W, China) and stored at 18C, the dry cantaloupe (DC) was
obtained by drying pieces (with 2 cm of diameter and 3–4 mm of thickness) in the oven at 40C until the
weight level was constant.
Milk and lactic ferments. The milk used is a dehy-drated powdered milk brand LOYA (Blida, Algeria). The lactic ferments used are Streptococcus thermophilus and L. bulgaricus at a freeze–dried state (CHR HANSEN, France).
Yogurt making. The preparation of yogurt (natural yogurt (NY)), yogurt with dry cantaloupe (CDY), yogurt with cantaloupe puree (CPY) and yogurt with mixture (yogurt with cantaloupe puree and dry canta-loupe (CPDY)) was made in the laboratory scale respecting the diagram for making standard yogurt. The incorporation was made before the heat treatment. The adapted recipe was that proposed by Amellal-Chibane and Benamara (2011) (Table 1).
Methods
Physicochemical evaluation of yogurt and cantaloupe samples. Moisture, ash and lipid contents were deter-mined in quadruplicate using A.O.A.C. method (2000). The protein content was determined in quadruplicate as % N x 6.38using a LECO CHNS-932 nitrogen micro-analyser (Leco Corporation, St Joseph, USA) (Isanga and Zhang, 2009; Sodini et al., 2005).
Analysis of proteins by sodium dodecyl sulphate polyacrylamide gel electrophoresis (SDS-PAGE) electrophoresis. Electrophoresis tests were performed using polyacrylamide gels (10%) in presence of SDS-PAGE according to Laemmli (1970) methodology.
Table 1. Recipe of standard natural yogurt (NY) and yogurt with cantaloupe (yogurt with cantaloupe puree (CPY), yogurt with dry cantaloupe (CDY) and yogurt with cantaloupe puree and dry cantaloupe (CPDY)) for 1l of milk
Samples Milk powder (g) DC (%) CP (%)
Lactic ferment (%) NY 20 0 0 0.03 CPY 20 0 5 0.03 CDY 20 4 0 0.03 CPDY 20 3 7 0.03 DC: dry cantaloupe.
Continuous and stacking gels of 10 and 3.5% of acryl-amide, respectively, were prepared. A buffer containing 2 M Tris–base, 0.15% SDS, pH 8.8 was used for the separating gels. A running buffer consisted of 0.027 M Tris–base, 0.38 M glycine, pH 8.3 with the addition of 0.15% SDS was utilized. Molecular weights of extracted protein fractions were determined by using SDS-PAGE gels, considering the relationship between the logarithm of protein molecular weight and electro-phoretic mobility, as analytical standard ‘Protein Plus Protein Standards’ (Bio-Rad, Richmond, CA, USA), and Coomassie Brilliant Blue was used for staining. Analysis of amino acids by high performance liquid chromatography (HPLC). Cantaloupe and yogurt pro-tein concentrates were prepared using Weiss et al. (1998) procedure, and HPLC analysis was performed by the methodology of Lindroth and Mopper (1979). Glycine/arginine and methionine/tryptophan were determined together, as their peaks merged. The ana-lysis was performed once on each sample. By this pro-cedure, it is possible to detect the following amino acids: alanine (Ala), aspartic acid (Asp), glutamic acid (Glu), histidine (His), serine (Ser), glycine (Gly), argin-ine (Arg), threonargin-ine (Thr), tyrosargin-ine (Tyr), methionargin-ine (Met), valine (Val), phenylalanine (Phe), isoleucine (Ile), leucine (Leu) and lysine (Lys). The other amino acids were not included in the results because they are completely destroyed by acid hydrolysis or cannot be directly determined from acid hydrolysed samples (Fountoulakis and Lahm, 1998).
Determination of total phenolics
Extraction of phenolics from yogurt samples (YSs). In order to quantify the total polyphenols of the prepared YSs, we proceeded to their extraction. Ten grams of yogurt was mixed with 2.5 ml of distilled water; then the pH was adjusted to 4.0 using 1 M HCl. The preparation was then incubated at 45C for 10 min
and then centrifuged (10,000 r/min, 20 min, 4C). The
supernatant was harvested and the pH was adjusted to 7.0 using NaOH solution. The neutralized supernatant was then centrifuged (10,000 r/min, 20 min, 4C)
(Zainoldin and Baba, 2009). The obtained extracts were stored at low temperature for further analysis (quantification of phenolics and their reducing power activity).
Preparation of raw extracts (REs) from cantaloupe. Similarly, to quantify the total polyphe-nols from cantaloupe samples, we proceeded to their extraction. Purees or juices (10–20 g) were homogenized with the aqueous acetone (acetone/water, 7/3, v/v) for 30 min (George´ et al., 2005). The supernatants
recovered by filtration (REs) were stored at 20C,
for further analysis (quantification of cantaloupe poly-phenols and their reducing power capacity).
The total phenolic content (TPC), in both yogurt and cantaloupe extracts, was determined by the meth-odology of Zainoldin and Baba (2009). Therefore, 1 ml of the homogenized extracts was transferred into a test tube and mixed with 1 ml of 95% ethanol and 5 ml of distilled water (Zainoldin and Baba, 2009). A volume of 250 ml of extract (diluted yogurt extract with distilled water and REs from cantaloupe) was added to 1.25 ml of 10-fold diluted Folin–Ciocalteu reagent. The solution was mixed and incubated at room tem-perature for 2 min. After that, 1 ml of 7.5% sodium carbonate (Na2CO3) (v/v) was added. Then the mixture
was incubated at 50C for 15 min and the absorbance
was measured at 760 nm against a blank (solution con-taining all reagents without samples) by using a UV– VIS Spectrophotometer (SpectroScan 50, Nicosia, Cyprus). The assay was performed in triplicate. For quantification, a calibration curve was generated with the standard solution of gallic acid (R2¼0.998). The TPCs were expressed as mg of gallic acid equivalent (GAE) per 100 g of dry weight for cantaloupe sample and mg of GAE per 100 g of YS, for all prepared yog-urts (George´ et al., 2005).
Total carotenoid contents. Total carotenoids extrac-tion was carried out according to Tadmor et al. (2010). To 0.5 g of the sample were added 8 ml of hex-ane:acetone:ethanol (50:25:25 v/v/v), followed by the addition of 1 ml KOH in water (80% w/v), vortexing and shaking for 5 min, followed by the addition of 1 ml of NaCl in water (25% w/v), vortexing and shak-ing for an additional 5 min. Subsequently, 8 ml of water was added, the samples were vortexed and incu-bated for 10 min in darkness until phase separation was achieved. Finally, the upper phase was collected, and the lower phase was re-extracted with an add-itional volume of hexane (2 ml), and the absorbance of the combined extract was read at 450 nm (Scott, 2001), using a Varian spectrophotometer (SpectroScan 50, Biotech Engineering Management Company Limited, UK).
Monitoring of pH, reducing power and water holding capacity (WHC). The pH value of the NY as well as cantaloupe-based yogurts (CPY, CDY and CPDY) was measured during 28 days of storage at 4C according to
the method used by Nguyen et al. (2014). The reducing power of sample extract from cantaloupe and YSs was determined by the method of Oyaizu (1986). Values are expressed as micrograms of GAE per 100 g of powder (mg GAE/100 g powder) (y ¼ 13.52 x 0.081; r ¼ 0.99). WHC was determined according to Mao et al. (2001)
method. All analysis were carried out in triplicate at the first, seventh, 14th, 21st and 28th days of storage (4C).
Rheological measurements of yogurts
Dynamic viscoelastic properties. YSs were charac-terized by small amplitude oscillatory shear measure-ments, using a controlled-stress rheometer (AR2000, TA Instruments, USA) at 10C. A parallel plates geometry
(dia: 60 mm) with a rough surface was used, in order to avoid slipping effects, and a gap between plates of 1 mm was selected. Low viscosity Dow Corning 200 fluid was used as sealant to avoid sample drying. Strain sweep tests between 0.002 and 2.0% at constant frequency (1 Hz) were also performed in order to establish the linear visco-elasticity range (LVR) as well as critical strain (gc).
Subsequently, frequency sweep tests (0.1–100 rad/s) were carried out within the LVR.
The elastic (G0) and the viscous (G00) moduli were
measured across the frequency range. Besides, the elas-tic modulus and loss tangent at 5 rad/s (G0
5and tan d5)
were selected in order to perform a suitable comparison for systems.
Steady-state shear properties. Steady-state shear flow tests were carried out using the same rheometer (AR2000, TA Instruments, USA) at 10C. The
meas-urements were performed at 10C from 103
to 10 Hz and the geometry used was a plate and plate geometry (dia: 60 mm) with a rough surface, avoiding sample slide, and a gap between plates of 1 mm. The results were adjusted to the Ostwald de Waele or Power law model, which is one of the methods known for explain-ing the behaviour of fluids. The model applies the fol-lowing expression
¼ K _
n1ð1Þ
where is the apparent viscosity; _is the shear rate and K and n are the consistency and flow index, respect-ively. The apparent viscosity () at intermediate shear rate ( _ ¼0.01 s1) and flow index (n) were the param-eters selected for comparison. The flow index (n) is selected because it determines how the flow precisely develops, if n < 1 the fluids called pseudo-plastic, these fluids flow more easily by increasing shear rate (shear thinning). On the other hand, when n > 1, the flow resistance increases with increased shear rate, and it is called a dilatant fluid (shear thickening). Microstructural characterization: Confocal laser scan-ning microscopy (CLSM). CLSM allows the three-dimensional observation of yogurt and CP (Hassan et al., 2003), avoiding the structural changes. The micros-copy used was a ZEISS LSM7 DUO (Germany) with an
Argon laser at 488 nm and detection between 493 and 619 nm. The microstructure images were analysed using image analysis software (ZEN2012SP1).
Determination of the lactic flora. The analysis of the microbial enumerations was performed using the pour plate technique. L. bulgaricus and S. thermophilus counts were determined using Reps et al. (2009) and Williams (1949) procedures, respectively. The counts are expressed as the log10CFU ml
1
of yogurt.
Statistical analysis
The analysis of variance was performed using XLSTAT Release 10 (Addinsoft, France). Tukey’s multiple range test (HSD) was used to compare means of the estimated parameters. Evaluations were based on the p < 0.05 sig-nificance level.
RESULTS AND DISCUSSION
Physicochemical evaluation of yogurt and cantaloupe
Physicochemical properties of all samples are shown in Table 2. The pH of yogurts and food is important with respect to public safety (Jayasinghe et al., 2015). The variation in pH was statistically significant (p < 0.05) due to the effects of the different forms of cantaloupe (puree (CP) or dry (DC) incorporated into the formu-lated yogurts (Table 2)). The addition of cantaloupe fruit increases the pH of the samples, the lowest (4.39 0.01) and the highest (4.54 0.01) values are recorded in NY and CDY, respectively. Indeed, yogurts prepared with cantaloupe are less acid compared to NY, because the cantaloupe pH is close to neutrality: CP and DC are 5.99 0.02 and 6.57 0.03, respectively.
Significant variation (p < 0.05) in moisture percent-ages is observed in cantaloupe yogurts (CYs) compared to the natural one. The moisture percentage in CYs increases with the increase of the fresh fruit but not in the presence of the dried sample. The highest (78.62 0.05%) and the lowest (76.05 0.04%) mois-ture percentages in yogurts are found in CPY and CDY samples, respectively, showing CPDY and control sample (NY) intermediate values (ca. 77%). The mois-ture content in CDY and CPDY decreased with the increase of DC because of its low moisture percentage (17.95 1.41%) compared to the CP (90.74 0.65%). With regards to CPDY, the moisture content of this preparation is the average of those CPY and CDY sam-ples (78.62 0.05 and 76.05 0.04%, respectively). It should be noted that the increase of the moisture content of fruit yogurt was due to the high moisture of the fruit pulp. This result was in agreement with the finding of Kumar Dutta Roy (2015).
Concerning the ash content, a significant difference (p < 0.05) has been observed between the NY and the formulated samples with cantaloupe fruit (Table 2). The addition of cantaloupe (CP and DC) exhibits more prominent effects on their ash content. Indeed, the ash amount of the NY is about 0.37% significantly lower (p < 0.05) than those of CDY (0.68 0.02%) and CPDY (0.57 0.04%). Indeed, DC ash content is about 5.29 0.06% and that of CP 0.35 0.14% (Table 2). Similar results were reported by Kumar Dutta Roy (2015) for the yogurt-based watermelon, but they are not in agreement with those reported by Arslan and Bayrakci (2016). These researchers have obtained a decrease in the ash content of the fortified yogurts by persimmon marmalade and puree. Another study conducted on the physicochemical composition of plain yogurt and different types of fruit (Papaya: Carica Papaya and Cactus Pear: Opuntia ficus indica) flavoured yogurt has not reported any significant dif-ferences between the NY and the flavoured one (Amal et al., 2016).
For protein determination, significant difference (p < 0.05) in protein content was observed between the NY sample and the new formulated products (Table 2). The change in protein content in YSs is greatly influenced by the incorporation of fruit (cantaloupe) (Table 2). Similar result was reported by Andronoiu et al. (2011) and his colleagues about their work on yogurt with added walnuts and strawberries jam, but in disagreement with that reported on the study carried out on the yogurt flavoured with Guddaim fruit (Grewia tenax) (Mohamed et al., 2015). Indeed, the protein content in YSs increases with the increase of DC (3.37 0.05%); the highest (2.78 0.11%) and the lowest (2.15 0.12%) contents are found in CDY and NY samples, respectively. Low protein content (0.57 0.01) in fruit pulp (CP) is the major cause of the low protein content of fruit pulp incorporated in yogurt preparation.
Lipid content is one of the most important quality factors of food and the minimum intake of fat should
be 15% of an adult’s energy intake (Dari, 2013). Fat content in yogurt or fruit yogurt depends on milk qual-ity, fruit pulp amount, fruit variety and other treatments. Addition of fruit has significant effects (p < 0.05) on lipid content of the formulated yogurt (Table 2). Indeed, the content of the new formulated products is significantly lower (p < 0.05) than that of the NY. The highest (2.57 0.03%) and the lowest (1.98 0.01%) lipid con-tents were found in NY and CPY, respectively. CDY and CPDY present 2.34 0.02 and 2.10 0.01% lipid percentages. Therefore, lipid content in yogurt decreased gradually with the increase of CP because of the very low amount of lipid amount in cantaloupe compared to milk. So, yogurt enriched by cantaloupe fruit can be described as a healthy product based on its low fat con-tent. The obtained result is in agreement with that reported by Dari (2013) about his research on butternut squash yogurt. In the other hand, Amal et al. (2016) have reported a slight decrease in the fat content of the yogurt contained Papaya and Cactus Pear fruits.
TPC
It is well known that regular intake of fruits and vege-tables is related to the reduced risk of diseases such as cancer and cardiovascular diseases, because they are rich sources of natural antioxidants. Cantaloupe fruit is reported to be a good source of phenolic compounds (Ismail et al., 2010). The TPCs of cantaloupe extracts are 18.44 0.03 mg GAE/100 g for CP and 264.72 0.86 mg GAE/100 g for DC (Table 3), which explains the variation in the content of phenolic compounds of the various prepared yogurts. In fact, all enriched yog-urts (CPY, CDY and CPDY) show an increase in TPC compared to the NY, which means that cantaloupe fruit may change the phenolic content in yogurt. Besides, there is also a significant difference (p < 0.05) in the phenolic content of CPY, CDY and CPDY. In addition, CDY and CPDY show the highest content (p < 0.05) than the CPY. Indeed, the addition of fruit
Table 2. Composition (moisture, ash, protein and lipid contents) and pH values for different samples of yogurt (NY, yogurt with cantaloupe puree (CPY), yogurt with dry cantaloupe (CDY) and yogurt with cantaloupe puree and dry can-taloupe (CPDY)) as well as cancan-taloupe puree (CP) and dry cancan-taloupe (DC)
Sample pH Moisture (%) Ash (%) Protein (%) Lipid (%) NY 4.39 0.01d 77.92 0.10b 0.37 0.03c 2.15 0.12d 2.57 0.03a CPY 4.42 0.01d 78.62 0.05b 0.55 0.02b 2.49 0.02c 1.98 0.01d CDY 4.54 0.01c 76.05 0.04c 0.68 0.02b 2.78 0.11b 2.34 0.02b CPDY 4.51 0.01c 77.22 0.33bc 0.57 0.04b 2.76 0.11b 2.10 0.01c CP 5.99 0.02b 90.74 0.65a 0.35 0.14c 0.57 0.01e 0.18 0.006f DC 6.57 0.03a 17.95 1.41d 5.29 0.06a 3.37 0.05a 0.40 0.01e
Values are mean 95% confidence interval.
as dry way leads to the enrichment of the formulated yogurt in phenolic compounds (Helal and Tagliazucchi, 2018). The obtained result is in agreement with those reported by Amal et al. (2016) and Halah and Mehanna (2011), in their respective studies about the fortified yogurt with Papaya and Cactus Pear fruits as well as natural plant antioxidant. In the other hand, yogurts enriched with red grape and callus extracts have dis-played high phenolic content (Karaaslan et al., 2011). But all these results are not in agreement with those of Arslan and Bayrakci (2016), where they have reported a decrease of the phenolic contents on the yogurt pre-pared with persimmon. In the other hand, Oliveira et al. (2015) have reported an immediate decrease of the phenolic content after the addition of strawberries preparation in yogurt.
Carotenoids content
Carotenoids are natural pigments with desirable health benefits and nutraceuticals properties. These com-pounds have become increasingly important because they have been used as an alternative to replace syn-thetic red and yellow colorants which are harmful to our health. Indeed, b-carotene is a unique antioxidant that effectively neutralizes reactive oxygen species, improves endothelial cell growth and improves endo-thelial function in the establishment of hypercholester-olemia (Solval et al., 2012). Results from Table 3 show that all YSs contain a quantity of carotenoids that varies significantly (p < 0.05) from one product to another. As we can see in Table 3, the total carotenoids in yogurt enriched CP are much higher than that of NY. On the other hand, it is obvious that the dried sample is the richest one because it is more
concentrated after its loss of water during drying. So, through our study we confirm that cantaloupe (C. melo L.) is a good source of carotenoids (Nattaporn, 2011; Vouldoukis et al., 2004). As a result, the quality of yogurt has improved with these bioactive substances. Indeed, our result supports that obtained by Halah and Mehanna (2011), where they have reported an increase in carotenoids content when they have used natural plant antioxidant in the production of novel yogurt.
Amino acid content
Essential amino acids including arginine, histidine, iso-leucine, iso-leucine, lysine, methionine, phenylalanine, threonine and valine should be in appropriate propor-tion simultaneity are required for protein synthesis, and they just can be obtained from diet (Ye et al., 2013). In both NY and DC, 17 and 16 kinds of amino acids are detected, respectively (Table 4). Although their levels are different, the amino acids detected in the NY (con-trol) analysed in the present study are similar than those reported in the literature. But, it should be pointed out that the predominant ones are the same than those reported in the study conducted by Boycheva et al. (2012). Indeed, the three major amino acids are Glu, Leu and Asp; unlike those reported by German (2014), which are Gly, Lys and Glu. These differences in the quantities of amino acids can be explained by the difference in the composition of milk
Table 4. Amino acids composition (AA%, g amino acid/ 100 g protein) of dry cantaloupe (DC) and natural yogurt (NY)
Amino acids AA % (DC) AA % (NY) Aspartate (Asp) 10.7 9.12 Threonine (Thr) 4.85 5.88 Serine (Ser) 7.23 8.51 Glutamate (Glu) 27.28 23.74 Glycine (Gly) 10.15 4.28 Alanine (Ala) 10.9 6.32 Valine (Val) 5.32 7.19 Cystein (Cys) / 0.24 Methionine (Met) 1.3 2.18 Isoleucine (Ile) 4.1 5.15 Leucine (Leu) 8.67 11.82 Tyrosine (Tyr) 1.25 1.92 Phenylalanine (Phe) 3.62 4.52 Lysine (Lys) 0.8 1.38 Histidine (His) 1.42 1.8 Arginine (Arg) 0.54 0.78 Proline (Pro) 1.85 5.16 Table 3. Polyphenol compounds and carotenoids of
dif-ferent samples of yogurt (natural yogurt (NY), yogurt with cantaloupe puree (CPY), yogurt with dry cantaloupe (CDY) and yogurt with cantaloupe puree and dry cantaloupe (CPDY)) as well as cantaloupe puree (CP) and dry canta-loupe (DC) Sample Polyphenols (mg GAE/100 g) Carotenoids (mg BC/100 g) NY 5.68 0.05e 175.0 2.2f CPY 7.48 0.01d 285.7 3.9e CDY 9.94 0.02c 500.6 2.2c CPDY 9.53 0.02c 397.7 3.9d CP 18.44 0.03b 1460.7 5.9b DC 264.72 0.86a 2214.9 8.0a
BC: b-caroten; GAE: gallic acid equivalent. Values are mean 95% confidence interval.
Values with different letters (a–b–c–d–e–f) were significantly differ-ent (Tukey, p < 0.05) for the four types of yoghurt, CP and DC.
used for the preparation of the yogurt. Indeed, the quality of milk products is reliant on milk composition that varies with stage of lactation, milking methods, environment, season, diet, feeding system, breed and species (Rafiq et al., 2016). By comparing the compos-ition of NY and DC, the content of aspartate, glutam-ate, glycine and alanine in the DC is significantly higher than those in NY (p < 0.05), whereas there is no significant difference (p > 0.05) in the contents of threonine, methionine, isoleucine, tyrosine, phenyl-alanine, lysine, histidine and arginine between the NY and DC (p > 0.05). Thus, in the view of the results obtained, cantaloupe is a good source of amino acids that can improve the nutritional quality of the prepared yogurts and their aroma. Subsequent data highlighted the increased production of volatile compounds after the incubation of cantaloupe fruit cubes withL-phenylalanine,L-methionine,L-isoleucine, L-leucine and L-valine, which are present in the NY (Table 4). So, the addition of the fruit cantaloupe to NY which is rich in these amino acids will necessarily induce the increase of volatile compounds which will contribute to the increase of the flavour of newly produced yogurts (Wyllie et al., 1996).
Proteins composition
The soluble protein composition of yogurts (NY and CPDY) and DC was analysed by SDS-PAGE. Figure 1 shows the principal protein fractions in the analysed samples (NY, DC and CPDY). As may be observed, there are bands at 32, 29, 20, 16–17 and 14 kDa,
and these can be associated with a-casein, b-casein, k-casein, b-lactoglobulin and a-lactalbumin, respect-ively, by comparison with molecular weight standard. After adding cantaloupe to the yogurt and comparing with NY, we noticed a decrease in the intensity of the casein bands and the appearance of a new band with MW ¼ 17 kDa. There is evidence showing that whey proteins or caseins interact with polysaccharides at low pH by forming soluble or caseins soluble or insol-uble complex coacervates, stable nanoparticles or solid precipitates (Babol et al., 2011; Oliveira et al., 2015). The bands in DC sample indicate the presence of pro-teins in cantaloupe fruit. These propro-teins contain prote-ases like cucumisin, which can be implicated in caseins cleavage (Noda et al., 1994; Yamagata et al., 1994).
Monitoring of pH, reducing power and WHC of prepared yogurts during the storage period Table 5 presents changes in pH, reducing power and WHC of different samples of yogurt during storage period (28 days).
Generally, the pH of all YSs decreases during storage period. The highest value is registered in the first day after preparation (4.3–4.5) and the lowest value is after 28 days (3.9–4.1). In fact, a significant increase (p < 0.05) in acidity was observed for all yogurts prepared during the storage period. This reduction on pH values is prob-ably due to the growth of acid-forming bacteria and pro-duced lactic acid during the storage period (Amal et al., 2016; Jayasinghe et al., 2015). When the sugar sources are finished, microorganisms begin to consume proteins
Standard (kD) NY DM CPDY 150 100 75 50 37 25 20 10 6 5 3 2 1 3 2 1 4 5 6
Band MW. Protein fraction References
(KD) 1 2 3 4 5 6 32 29 20 17 16 14
α-casein Zagorchev and al
(2013) Zagorchev and al (2013) Zagorchev and al (2013) Oliveira and al (2015) Oliveira and al (2015) Oliveira and al (2015) β-casein K-casein β-lactoglobulin β-lactoglobulin α-lactalbumin
Figure 1. SDS-PAGE of proteins extracted from NY, DC and CPY and CPDY. Enclosed is a table with the molecular weight and protein fraction name of each signal.
leading to the production of some products, which will decrease the pH of the sample (Vahedi et al., 2008). In the other hand, the pH values of all formulated yogurts decreased during the storage time period, including that of NY. This result is in agreement with that reported by Jayasinghe et al. (2015) during their study about the pro-duction of a novel fruit yogurt using dragon fruit as well as those obtained by Jayalalitha et al. (2015) about their work on the formulation of value enriched yogurt with soy milk and mango pulp.
Concerning the antioxidant activity of all YSs, the reducing power increased significantly (p < 0.05) from first day to 14th day, and it decreases until it reaches its minimum activity at the 28th day of storage (Table 5). This result is in agreement with that obtained by Felfoul et al. (2017) in their recent study on the effect of ginger addition on fermented bovine milk. Indeed, these researchers have reported an increase on the redu-cing power of all ginger YSs during 21 days of cold storage at 4C. Another study conducted by Sah et al.
(2015) has reported also the increase of the reducing power capacity of yogurt supplemented with pineapple peel during its storage compared with the first day.
As shown in Table 5, the WHC of all YSs has increased significantly (p < 0.05) during the storage period, the lowest value is obtained in the first day, and the highest one is obtained in the last day. This result is in agreement with that obtained for the yogurt enriched by Papaya and Cactus Pear fruits (Amal et al., 2016). In contrary, Vianna et al. (2017) have reported a decrease of this parameter during the storage time of the yogurt obtained by the mixture of cow milk and sheep milk. In their turn, Arslan and O¨zel (2012) have revealed the
decrease of the WHC of the persimmon-supplemented yogurts during their storage. Comparing the WHC of different samples, all enriched yogurt have exhibited an increase of this parameter. The highest value was found in CDY (71.83%), probably due to the higher percentage of total solid of the DC in comparison to the CP, and even the NY. The increase in the percentage of WHC during the storage period, at low temperature, may be related to the development of a network structure between the fruit and yogurt proteins. In other words, the WHC or lower whey separation refers to a weak gel network (Singh and Muthukumarappan, 2008) as well as to the capacity of water absorption of cantaloupe fruit (Spada et al., 2015).
Rheological measurements of yogurt
Dynamic viscoelastic properties. First, strain sweep tests are performed to determinate the LVR of each yogurt. From these tests, critical strains (gc) are
calcu-lated as can be observed in Table 6. The critical strain associated to CDY (DC) shows significant lower values (ca. 0.02%) since these yogurts (CDY and CPDY) are less deformable before breaking its structure. In add-ition, Figure 2 shows the evolution elastic and viscous moduli (G0 and G00, respectively) of prepared yogurts.
All yogurts present a predominantly elastic response (G0>G00) over the whole frequency range studied as
well as both moduli showed a slight dependence on frequency. This behaviour is typical of a weak visco-elastic gel (Sert et al., 2017). In fact, in order to com-pare different systems, tan d5 and G05 are shown in
Table 6. As can be observed, no significant differences
Table 5. pH values, reducing power and water holding capacity (WHC) of different samples of yogurt (natural yogurt (NY), yogurt with cantaloupe puree (CPY), yogurt with dry cantaloupe (CDY) and yogurt with cantaloupe puree and dry cantaloupe (CPDY)) during storage period (first, seventh, 14th, 21st and 28th days)
Parameters Sample Day 1 Day 7 Day 14 Day 21 Day 28 pH
reducing power (mgGAE/100 g)
NY 4.39 0.01dA 4.39 0.01dA 4.38 0.01dA 4.33 0.01dB 3.98 0.01dC CPY 4.42 0.01cA 4.42 0.01cA 4.41 0.01cA 4.38 0.01cB 4.00 0.01cC CDY 4.54 0.01aA 4.50 0.01aB 4.49 0.01aB 4.44 0.01aC 4.11 0.01aD CPDY 4.51 0.01bA 4.49 0.01bB 4.48 0.01bB 4.38 0.01bC 4.08 0.01bD NY 2.32 0.02dD 2.70 0.03dC 4.15 0.01dA 2.96 0.01dB 1.63 0.02dE CPY 2.83 0.02cD 3.14 0.05cC 4.32 0.02cA 3.28 0.02cB 1.96 0.02cE CDY 6.35 0.01aD 6.83 0.05aC 9.32 0.01aA 7.24 0.02aB 3.83 0.03aE CPDY 5.96 0.01bD 6.35 0.03bC 8.49 0.01bA 6.50 0.03bB 3.37 0.01bE WHC (%) NY 61.73 0.23cE 62.56 0.15cD 63.33 0.11cC 63.86 0.11cB 64.93 0.11cA CPY 59.60 0.20dE 60.40 0.20dD 60.93 0.11dC 61.73 0.11dB 62.86 0.11dA CDY 68.43 0.05aE 69.46 0.11aD 69.86 0.11aC 70.43 0.05aB 71.83 0.15aA CPDY 63.60 0.20bE 64.33 0.11bD 65.03 0.15bC 65.66 0.11bB 66.20 0.20bA
GAE: gallic acid equivalent.
Different uppercase letters (A–B–C–D–E) represent significant differences in the same rows (P < 0.05). Different lowercase letters (a–b–c–d) represent significant differences in the same column (P < 0.05).
in tan d5are found with values about 0.16–0.19
corres-ponding to a predominant elastic behaviour but no extremely solid behaviour (tan d < 0.1). Once again, the higher G0
5observed in DC content samples (CDY
and CPDY) reveals that these yogurts evidence a more rigid texture, consistent with the less deformable behav-iour previously observed from the critical strain values. There was a link between WHC and the rheological parameter (Spada et al., 2015).
Steady-state shear properties. Viscosity () is a qual-ity attribute of yogurts and can be affected by formu-lation composition (e.g. total soluble solid content and stabilizer), type of starter cultures, heat treatment and processing methods (Sun-Waterhouse et al., 2013). As commonly observed, with shear rate increases, decreases (Figure 3), due to the structural breakdown and rearrangement induced by the shear stress. This behaviour corresponds to a shear thinning behaviour. Once again, some parameters are selected (viscosity at
0.01 s1(0.01) and flow index (n)) in Table 6 to compare
different samples. In this case, although the tendency of the curve is very similar, the shear thinning behaviours are more apparent in the DC content samples (CDY and CPDY) since the flow index (n) is practically zero. However, in the range of shear rates evaluated, the vis-cosity of NY and CPY presents higher viscosities prob-ably due to the different texture, less influenced by the deformation. This fact is related to the higher critical strains found in these systems (NY and CPY).
Microstructural characterization: CLSM
Representative micrographs from cantaloupe and each yogurt type are shown in Figure 4. It can be seen that the incorporation of the dry fruit promotes a signiEcant change in the sample microstructure, compared to the fresh sample. This fact can be related to increase in the
Table 6. Rheological parameters of different samples of yogurt (natural yogurt (NY), yogurt with cantaloupe puree (CPY), yogurt with dry cantaloupe (CDY) and yogurt with cantaloupe puree and dry cantaloupe (CPDY)): Critical strain (gc),
elastic modulus and loss tangent at 5 rad/s (G0
5and tan d5, respectively) as well as viscosity at 0.01 s 1
(0.01) and flow
index (n) from Ostwald de Waele model
Sample gc(%) G05(Pa) tan d5 0.01(Pas) n
NY 0.11 0.01a 230.5 91.8a 0.16 0.01a 2350 608a 0.13 0.01a CPY 0.12 0.02a 148.2 12.3a 0.16 0.01a 2091 170a 0.12 0.01a CDY 0.018 0.002b 4186 1310b 0.19 0.01a 2120 379a 0.01 0.01b CPDY 0.024 0.002b 4591 403b 0.18 0.01a 1058 59a 0.02 0.01b
Different lowercase letters (a-b-c-d) represent significant differences in the same column (P < 0.05).
104 103 102 101 100 10–1 10–2 101 100 101 Shear rate/(1/s) Viscosity/(Pa·s) CDPY CDY CPY NY
Figure 3. Steady-state shear flow tests (apparent viscosity as a function of shear rate) of prepared yogurts: NY, CPY, CDY and CPDY.
CDY: yogurt with dry cantaloupe; CPDY: yogurt with dry cantaloupe and cantaloupe puree; CPY: yogurt with can-taloupe puree; NY: natural yogurt.
104 103 102 101 100 10–1 100 101 102 Frequency/(rad/s) G', G''/(P a) G' G''
System CDPY CDY CPY NY
Figure 2. Frequency sweeps (elastic modulus (G0) and
viscous modulus (G00) versus angular frequency (o)) of
solid concentration which can promote a network for-mation. This fact is already noted by the results of WHC. Indeed, by comparing the NY with CPY and CDY, it is observed that there is an improvement in the level of protein in yogurt when the cantaloupe is added. In addition, the content is higher in the case of CDY because DC is richer in proteins (3.37%) than CP (0.57%). Through our results, we confirm the hypoth-esis that there is a link between the microscopic ana-lysis, the WHC and the rheological parameter (Spada et al., 2015).
Charge of lactic flora
The results concerning the lactic flora (S. thermophilus and L. bulgaricus) are shown in Table 7, which clearly shows their perfect conformity with the standards. The cultivation of this flora is more satisfactory (higher charge of lactic flora in the case of a yogurt based on cantaloupe than in the case of NY). As we can see, for the two lactic flora (S. thermophilus and L. bulgaricus), they are the most numerous in CDY, followed by CPDY, CPY and NY. These results were in agreement with those reported in Boycheva et al. (2011). Also, we
confirm the hypothesis that the added cantaloupe fruit to the NY enriched with different nutrients. This enrichment depends closely on its composition, as we have already pointed out, in the previous sections. The dry fruit is richer in solids (sugars, proteins, etc.) com-pared to the fresh fruit which is rich rather in water. Therefore, these compounds have probably stimulated the development of lactic acid bacteria.
Figure 4. CLSM images for CP, NY, CPYs and CDY. Arrows correspond to protein aggregates.
CDY: yogurt with dry cantaloupe; CP: cantaloupe puree; CPY: yogurt with cantaloupe puree; NY: natural yogurt.
Table 7. Lactic flora charge (S. thermophilus and L. bul-garicus) in formulated yogurts (natural yogurt (NY), yogurt with cantaloupe puree (CPY), yogurt with dry cantaloupe (CDY) and yogurt with cantaloupe puree and dry canta-loupe (CPDY))
Sample S. thermophilus L. bulgaricus NY 1.56108 1.41106 CDY 9.7108 1.74107 CPY 8.62108 1.65107 CPDY 9.2108 1.70107 Standards 108 105
CONCLUSIONS
The addition of cantaloupe fruit to the NY has increased its nutritional quality such as amino acids, antioxidant compounds (polyphenols, carotenoids), ashes (which have increased significantly) and fat con-tent (which has decreased significantly). On the other hand, it modified its physicochemical properties by sig-nificantly reducing its pH and by increasing its WHC, as well as its microbial flora. These parameters have positively influenced the rheology of newly formulated products. Yogurt with added cantaloupe fruit (fresh and dried samples) is a new product that can be man-ufactured and successfully marketed due to its nutri-tional properties.
ACKNOWLEDGEMENTS
The authors thank the Microscopy and Microanalysis ser-vices (CITIUS – Universidad de Sevilla) for providing full access and assistance to the ZEISS LSM7 DUO microscopy and LECO CHNS-932 equipment, respectively. We also want to thank Mr. MORS Faouzi, the head of the research and development department, DANONE (AKBOU, Bejaia, Algeria), for his positive collaboration.
DECLARATION OF CONFLICTING INTERESTS
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
FUNDING
The author(s) received no financial support for the research, authorship, and/or publication of this article.
ORCID ID
M Fe´lix http://orcid.org/0000-0002-3608-7035
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