Recent updates on bioaccessibility of phytonutrients

Trends in Food Science & Technology 97 (2020) 366–380

Contents lists available at ScienceDirect

Trends in Food Science & Technology journal homepage: www.elsevier.com/locate/tifs

Recent updates on bioaccessibility of phytonutrients a

a,∗

b

T a

a

Nitasha Thakur , Pinky Raigond , Yeshwant Singh , Tanuja Mishra , Brajesh Singh , Milan Kumar Lala, Som Dutta a b

Division of Crop Physiology, Biochemistry and Post Harvest Technology, Central Potato Research Institute, Shimla, 171001, India Analytical Development Division, Sun Pharma Advanced Research Company (SPARC), Vadodara, Gujarat, 390 020, India

A R T I C LE I N FO

A B S T R A C T

Keywords: Bioaccessibility Bioavailability Cooking Food matrix Phytonutrients

Background: Fruits and vegetables are rich source of phytonutrients. These phytonutrients are present in high concentrations in raw form, and decrease to some extent after processing. The major phytonutrients present in fruits and vegetables are vitamins, carotenoids, polyphenols, curcuminoids, polyunsaturated fatty acids, proteins, peptides, dietary fibers, oligosaccharides, and minerals that exhibit multiple beneficial effects on human health. Lots of research work has been carried out on assessing these phytonutrients in various fruits and vegetables however very limited knowledge is available on assessment of how much of these phytonutrients are available to exert their biological function in the human body. Scope and approach: In this review we attempted to provide updated information regarding the methods used for assessing bioaccessibility, extent of bioaccessibile phytonutrients from different food matrix and effect of different processing (boiling, microwaving, frying) and preservation techniques (dehydration and freezing) on bioaccessibility of phytonutrients. Key Finding and Conclusions: Food matrix, processing and preservation methods have major influence on the bioaccessibility of phytonutrients. Cooking, frying and pasteurization increased the bioaccessibility of polyphenols and carotenoids in fruits and vegetables. Dehydration can be a good technique to enhance the bioaccessibility of carotenoids. Freezing showed contradictory response on bioaccessibility as it increased bioaccessibility of phytonutrients in some fruits and decreased in others. To achieve maximum bioaccessibility of carotenoids, thermal treatment along with addition of oil is the best; to enhance ascorbic acid and polyphenols bioaccessibility thermal treatment is the best and for enhanced bioaccessibility of mineral and tocopherols high pressure-processing is most suitable.

1. Introduction Plant foods including fruits, vegetables and processed foods contain numerous types of phytonutrients such as vitamins, carotenoids, polyphenols, curcuminoids, polyunsaturated fatty acids, proteins, peptides, dietary fibers, oligosaccharides, and minerals that have many beneficial effects on human health (Espin, Garcia-Conesa, & Tomas-Barberan, 2007; Hur, Lim, Decker, & McClements, 2011; Wildman, 2007). However, to achieve any health beneficial effects, the phytonutrient compounds must be bioavailable viz. effectively absorbed from the gut into the circulatory system and delivered to the appropriate target location (Actis-Goretta et al., 2013; Fernández-García et al., 2012). The term bioavailability is defined as the part of ingested nutrient that reaches the systematic circulation and available for utilization in normal physiological functions (Wood, 2005). Two additional terms i.e. bioactivity

and bioaccessibility comes under bioavailability. Bioaccessibility can be defined as the part of ingested compound released from its food matrix and becomes available for absorption in intestine. The second definition describes it as material available after digestive transformations of food for assimilation, absorption into intestinal epithelium cells and lastly, the pre-systemic intestinal and hepatic metabolism (Cardoso, Afonso, Lourenço, Costa, & Nunes, 2015). On the other hand, term ‘Bioactivity’ includes all the physiological effects it generates i.e. how the compound reaches the systemic circulation, transported to the target cell and interacted with biomolecules (Fig. 1). In-vitro bioaccessibility/bioavailability methods provide the in depth knowledge regarding interactions between nutrients and its food components, effect of pH and enzymes, food preparation and processing practices on either micronutrient absorbability or on the potential for a nutrient to be absorbed (Sandberg, 2005). Thus, knowledge of

∗

Corresponding author. E-mail addresses: [email protected] (N. Thakur), [email protected] (P. Raigond), [email protected] (Y. Singh), mishri_tanu@rediffmail.com (T. Mishra), [email protected] (B. Singh), [email protected] (M.K. Lal), [email protected] (S. Dutt). https://doi.org/10.1016/j.tifs.2020.01.019 Received 26 August 2019; Received in revised form 7 January 2020; Accepted 12 January 2020 Available online 23 January 2020 0924-2244/ © 2020 Elsevier Ltd. All rights reserved.

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

Fig. 1. Events occurring during bioavailability.

2. Methods for bioaccessibility determination

bioaccessibility is important to ascertain the nutritional quality of a nutrient. On the other hand, bioavailability of a component is determined in-vivo in animals or humans as area of compound obtained under curve after administration of an acute dose of an isolated compound (Actis-Goretta et al., 2013). In-vivo method of estimation is tedious and requires human subject. There are various methods for determination of bioaccessibility. In recent years researchers developed many in-vitro methods for estimating bioaccessibility. In-vitro digestion and dialysis methods for simulating the gastro-intestinal conditions are being extensively used for evaluation of bioaccessibility, sometimes followed by Caco-2 cell uptake since they are rapid, safe, and do not have ethical restrictions as in case of in-vivo methods as discussed above (You, Zhao, Regenstein, & Ren, 2010). The bioavailability of phytonutrient compounds depend on food matrix and its release from matrix, changes during digestion, uptake, metabolism and biodistribution (Actis-Goretta et al., 2013; Bohn et al., 2015; Brown, 2004; Porter, Trevaskis, & Charman, 2007; Pouton & Porter, 2008). Many physiological processes are responsible for the low bioavailability of phytonutrients such as less release from the food matrix (Moelants et al., 2012), low solubility or formation of insoluble complexes in the gastrointestinal tract (Porter et al., 2007; Pouton & Porter, 2008; Rimbach, Pallauf, Moehring, Kraemer, & Minihane, 2008), low permeability across the mucus layer and molecular transformations at molecular level in the gastro-intestinal tract (ActisGoretta et al., 2013; Fernández-García et al., 2012; Martinez & Amidon, 2002). Food processing is one of the main determining factors for estimating the bioaccessibility because it can either increase or decrease the bioaccessibility of nutrients and bioactive compounds. Thermal processing has been used previously to preserve fruit and vegetable products, however, now-a-days due to increase in consumer demand for more natural products many high-end technologies have been implicated such as high-pressure processing, high pressure homogenization and pulse electric fields (Aschoff et al., 2015; Dewanto, Wu, Adom, & Liu, 2002; Gil-Izquierdo, Gil, Ferreres, & Tomas-Barberan, 2001; GilIzquierdo, Zafrilla, & Tomas-Barberan, 2002; Lemmens, Van Buggenhout, Oey, Van Loey, & Hendrickx, 2009). However, it is important that bioaccessibility of major components such as phytonutrients should not be adversely affected by any preservation method employed during food processing. As we know plant-derived foods are rich sources of phytonutrients and nutritional value of food is generally based on concentration of various phytonutrients, therefore attention has been focussed in assessing how much of these phytonutrients are available to exert their biological function in the human body. Thus, the present review is an attempt to provide updated information regarding the bioaccessibility of phytonutrients from different food matrix and effect of processing techniques on bioaccessibility.

Bioavailability and bioaccessibility of phytonutrient compounds can be analysed by different in-vivo and in-vitro methods. Bioavailability studies of these compounds are carried out in-vivo in human or animal subjects. In-vivo studies provide more specific information about the bioavailability of phytonutrients but these studies involve more cost, more time and have ethical constraints and difficulties in data interpretation. Animal studies are generally less expensive than the human studies but the main disadvantages are the differences in metabolism between animals and humans, making interpretation of results difficult (Wienk, Marx, & Beynen, 1999). Therefore, as an alternative, in-vitro methodologies have been developed for bioaccessibility of different food constituents that are comparatively simple, cheap and produce reproducible results (Failla, Huo, & Thakkar, 2008). One such approach of in-vitro methodologies is in-vitro gastro-intestinal digestion. In-vitro gastrointestinal digestion is considered useful for the estimation of pre absorptive events such as stability and bioaccessibility of nutrients/phytonutrients from different food matrix. In-vitro gastrointestinal digestion methods are used as substitutes for predictive purposes. Most of these studies have been reviewed by several authors and reported significant differences in the procedures such as type of digestion phases (mouth, stomach, small intestine and large intestine), composition and concentration of digestive fluids (enzymes, salts, buffer, biological polymers) and also length of incubation time of samples in each digestive stage (Hur et al., 2011; Ting, Zhao, Xia, & Huang, 2015). The concentration, composition of enzymes and time of digestion should be adjusted according to sample. If concentration of target material (protein, carbohydrate or lipids) is increased, then concentration of enzymes or digestion time should also be increased. A short change in time within small intestine may limit absorption of bioactive lipophilic compounds thereby reducing their bioavailability (Hur et al., 2011). Despite of their broad applicability and potential, invitro methodologies does not fully mimic whole processes that occur in in-vivo studies. Therefore, in-vivo studies should be used for validation of in-vitro methods to maximum extent (Cardoso et al., 2015). Foods are usually digested to simulate human digestive system through two in-vitro digestion steps (sometimes three steps) that includes gastric and small intestine digestion. The initial steps of food breakdown are achieved during gastric digestion by addition of pepsin (from porcine stomach) prior to acidification of the samples to pH 2. Most of polymeric and oligomeric structures such as proteins and carbohydrates breakdown by acidic conditions of gastric phase (Wood, 2005). Pepsin denatures itself, lose its activity at pH greater than 5, therefore, acidification of samples to pH 2 is important. Samples were neutralized to pH 5.5 before the start of intestinal digestion followed by addition of pancreatin and bile salts and finally readjusted to pH 7. Activity of gastric enzymes gets changed due to significant increase in pH during intestinal digestion (Duchateau & Klaffke, 2009). Release of 367

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

sodium taurocholate along with porcine bile extract and porcine pancreatin at pH 7 for 2 h at 37 °C. Bioaccessibility of digested food can either be measured via solubility, dialyzability or gastrointestinal models. The intestinal digests are centrifuged to yield supernatant and precipitated for solubility assay. The compound present in supernatant represent the soluble compounds and are analysed by atomic absorption spectrophotometry (AAS), mass spectrometry (MS), spectrophotometry and high-performance liquid chromatography (HPLC). The amount of soluble compound relative to total amount of compound in the test sample calculates the percent solubility. In-vitro gastro-intestinal digestion is followed by determination of phytonutrients that are capable of crossing semipermeable membrane and simulates passive diffusion of these compounds through intestinal epithelium. Dializability methods have been shown to be useful in accessing the bioaccessibility of compounds such as phenolic acids, flavonoids, anthocyanins, vitamin C and minerals (Perez-Vicente, Angel Gil-Izquierdo, & Garcia-Viguera, 2002; Bouayed, Deuber, Hoffmann, & Bohn, 2012; Bouayed et al., 2011). Simulated gastrointestinal digestion can be performed using two models viz. static models and dynamic models. In static models, digestion products do not mimic physical processes such as shear, mixing, hydration and thus mainly remain immobile. In dynamic models, gradual modifications in pH and enzymes concentration can also be done, thereby providing better simulating environment in relation to the actual in-vivo situation. In-vitro bioaccessibility assay based on measurements of soluble or dialyzable compounds can further be improved by use of cell cultures. The most validated intestinal epithelium cell model which is commonly used by researchers is CaCo-2 cell model. Although colonic in origin, CaCo-2 cells have ability to undergo spontaneous differentiation to form a monolayer cells, having many of functional and morphological properties typical of mature human enterocytes found in small intestine (Pinto et al., 1983).

pancreatic and bile enzymes facilitate the emulsification of lipids into micelles (Kalantzi et al., 2006). Analysis of liposoluble compounds such as carotenoids is usually obtained by low speed centrifugation or ultracentrifugation of intestinal digest thus obtaining micellar fraction (Fernández-García et al., 2012). In intestinal cells only those lipids can be absorbed which are incorporated into micelles (Trevaskis & Charman, 2008). Sometimes third step which generally precedes the gastric phase in in-vitro digestion is introduced which involves digestion by alpha amylase that results in breakdown of glycosidic bonds of starch molecules. Variations in conditions such as pH, incubation period and concentration/type of enzymes/salts used in oral, gastric and intestinal phases were observed in literature. For the bioaccessibility studies of carotenoids, polyphenols and vitamins, the α-amylase was used in oral phase with pH ranged between 6.5 and 6.8 and this phase continued for 5–10 min at 37 °C (Granado-Lorencio et al., 2007; Failla et al., 2018; Gawlik-Dziki, 2019; Shim, 2012; Werner and Bohm, 2011;; Mandalari et al., 2013). In gastric phase, porcine pepsin was used for carotenoid bioaccessibility at pH 2.5 with 1 h incubation at 37 °C (Failla et al., 2018; Hedren, Dian & Svanberg, 2002). Reboul et al., 2006 maintained the same conditions for gastric phase except pH which was adjusted to 4. For polyphenol bioaccessibility, Gil-Izquierdo et al., 2001 and Bermudez-Soto, Tomas-Barberan, & Garcia-Conesa, 2007 used porcine pepsin at pH 2 with 2 h incubation at 37 °C, however, Gawlik-Dziki, 2012 and Shim, 2012 used 1hr incubation period. Porcine pepsin at pH 4 was used for vitamin E bioaccessibility with 30 min incubation period at 37 °C (Mandalari et al., 2013; Reboul et al., 2006; Werner & Bohm, 2011). During intestinal phase, for carotenoid bioaccessibility GranadoLorencio et al., 2007 used bovine bile, porcine pancreatin, human pancreatic lipase, colipase, cholesterol esterase, phospholipid, taurocholate salts at pH 7.8 for 2 h at 37 °C. Failla et al., 2018 used porcine carboxyl ester lipase and lipase at pH 6.5 for 2 h at 37 °C. However, Colle, Van Buggenhout, Lemmens, Van Loey,& Hendrickx, 2012 and Cilia et al., 2012 used porcine pancreatin, porcine bile salt at pH 6.5 to 6.9 for 2 h at 37 °C. For polyphenolic bioaccessibility, porcine bile extract, porcine pancreatin and lipase were used at pH 7 to 7.5 for 2 h at 37 °C (Bouayed, Hoffmann, & Bohn, 2011; Gawlik-Dziki, 2012, Shim, 2012; Gil-Izquierdo et al., 2001). Reboul et al., 2006 and Werner and Bohm et al., 2011 used porcine bile extract and porcine pancreatin at pH 6.5 to 7 with 30 min incubation at 37 °C for vitamin E bioaccessibility. However, Mandalari et al., 2013 used lecithin, cholesterol,

3. Bioaccessibility of phytonutrients in vegetables and fruits 3.1. Bioaccessibility of carotenoids Carotenoids possess pro-vitamin A activity, act as antioxidants and contain more than 700 naturally occurring fat-soluble plant pigments synthesized by plants, algae, and photosynthetic bacteria. They play an important role in human health by their powerful antioxidant potential hence are associated with anti-aging, anti-inflammation, anti-ulcer, and anticancer properties (Fernández-García et al., 2012). Yellow and

Fig. 2. Biosynthetic pathway of lycopene and β carotene. 368

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

violaxanthin, neoxanthin and β-carotene. Bioaccessibility in 12 potato clones ranged from 55 to 160% in case of lutein and 24–388% in case of zeaxanthin, respectively (Andre et al., 2015). However, in another study it was reported that in yellow fleshed potatoes, bioaccessibility of lutein ranged from 33 to 71% and zeaxanthin between 51% and 71% (Burgos et al., 2013). Jeffery, Turner, & King, 2012 reported bioaccessibility studies of βcarotene and lutein in butternut squash, carrot, sweet potato and tomato and observed that bioassessibility percentage varied widely between foods for each carotenoid. The percent bioaccessibility of βcarotene was 16.5% for butter squash, 21.6% for carrot, 13.7% for sweet potato and 15.5% for tomato. Lutein bioaccessibility was 15.9% for butternut squash, 40.5% for carrot and 58.6% for tomato, however, it was not detectable in sweet potato. Bioaccessibility studies of β-carotene, β-cryptoxanthin, zeaxanthin and lutein was conducted by O'Sullivan, Jiwan, Daly, O'Brien, & Aherne, 2010 in different varieties of bell pepper and chilli peppers. It was found that bioaccessibility in bell peppers and chilli peppers varied from 6.2 to 112.8% and 11.6–106.9% respectively, depending on carotenoid type. Zeaxanthins were more bioaccessible in both bell and chilli pepper than β-carotene, β-cryptoxanthin and lutein. Granado-Lorencio et al., 2007 reported invitro bioaccessibility of carotenoids from fruits and vegetables and their results showed that bioaccessibility of β-carotene was maximum in tomato paste (100%) followed by pine apple (98.7%), red pepper (70.6) and spinach (25.5%). Kaulmann, Andre, Schneider, Hoffmann, & Bohn, 2016 compared plum and cabbage for bioaccessibility of carotenoid and observed that there was no significant difference between Prunus and Brassicaceae varieties. However, bioaccessibility of β-carotene ranged from 0.9% to 6.8% in cabbage and 3.4%–11.0% in plum, respectively. Dehydration is a technique that restricts microbial growth, enhance the shelf life of food and thus affect the content of bioactive components and their bioaccessibility. Studies were conducted to evaluate the effect of dehydration on bioaccessibility of total carotenoids in mixture of green gram and amaranth leaves and mixture of chick pea and amaranthus. Dehydration resulted in increase in the total carotenoid bioaccessibility from 2.72% (fresh) to 5.17% (dehydrated) and 3% (fresh) to 5% (dehydrated) in green gram-amaranth leaves mixture and chick peaamaranthus mixture, respectively (Oghbaei & Prakash, 2013; Prakash & Oghbaei, 2015). Their results indicated that among processing methods, dehydration can be a good technique to enhance bioaccessibility of carotenoids. The quality of fruits and vegetables based products is affected by processing methods. In a study conducted by Koh & Loh, 2018 it was observed that thermal processes increased bioaccessiblility of β-carotene in pumpkin and butternut squash. Bioaccessible β-carotene in raw pumpkin and raw butternut squash was 10.56% and 1.65% respectively. Bioaccessibility of β-carotene in deep-fried pumpkin (68.86%) and butternut squash (22.32%) were significantly higher than their raw sample indicating enhancement in bioaccessibility of β-carotene by deep frying method in both samples. Hedren, Diaz, & Svanberg, 2002 found that cooking may cause efficient release of carotenoids from the food matrix by softening the cell structure so that the digestive enzymes work more efficiently. Raw carrots released 3% of the β-carotene while homogenized carrots released 21% of β-carotene. Cooked pulp increased the bioaccessibility by 27% while adding cooking oil to the cooked pulp further increased the bioaccessible fraction to 39%. Thus, it can be concluded that heat treatment enhanced the release of βcarotene about two fold in carrot pieces and 1.3 times in homogenized carrots. Lemmens et al., 2009 reported that different thermal processing increased β-carotene in-vitro bioaccessibility ranging from 5.12% (raw) to 34.35% (cooked) in carrots. Bioaccessibility of different carotenoid species present together in the same food source was highly variable. Reboul et al., 2006 observed that carrot juice and processed tomatoes were the most bioaccessible sources for β-carotene. The bioaccessibility of β-carotene from raw carrots was 2.56% compared to 14.1% for carrot juice. β-carotene bioaccessibility ranged from less than 0.1% in crude

orange fruits as well as dark green vegetables are the main sources of carotenoids. β-carotene, α-carotene, and β-cryptoxanthin (carotenoids with pro-vitamin A activity), lycopene, lutein, and zeaxanthin (no provitamin A activity) are the six most common dietary carotenoids (Fig. 2). The biosynthesis and concentration of these carotenoids is affected by environmental conditions. Brandt, Pewk, Barna, Lugasi, & Helyes, 2006 studied the effect of temperature and photosynthetically active radiation on lycopene content of tomato fruits during different stages of fruit maturity. They reported that lycopene content decreased as the temperature of fruit exceeds 30 °C. The lycopene content at different harvesting time ranged from 36.8 to 68.9 mg/kg and it showed positive correlation with respect to colour values. Ombodi, 2014 studied the effect of water supply on carotenoid and tocopherol content of carrot. Water supply and bioactive compounds showed negative correlation with each other however within the carotenoid and tocopherol positive correlation was observed. Increasing water supply decreased the concentration of these phytochemicals, however, the composition remained unaffected. Similarly, Berki, Daood, & Helyes, 2014 reported that 100% irrigation yielded tomatoes with lowest level of carotenoids and polyphenols whereas non irrigated tomato varieties showed higher amount of bioactive compounds. Pek, Helyes, & Lugasi, 2010 studied the effect of ripening conditions (storage of detached tomato fruits at 15 and 30 °C and ripened on vine) of tomato on lycopene, ascorbic acid and polyphenols content. Storage temperature showed positive effect on ascorbic acid, negative effect on lycopene content whereas polyphenols did not show any differences at different ripening conditions. Response of external supplementation of tocopherol on retention of natural colorants in paprika was studied by Koncsek, Kruppai, Helyes, Bori, & Daood, 2015. With addition of tocopherol, the carotenoid degradation was retarded by 28, 32 and 40% in paprika prepared from conventional, organic and frost-damaged peppers, respectively. Carrots contain different types of carotenoids based on their color. Metzger & Barnes, 2009 evaluated carotenoids from two commercial carrot varieties, one wild carrot variety and thirteen colored carrot varieties. They reported maximum lycopene content in atomic red carrot and lutein, α carotene and β carotene in purple haze and comic purple carrots. Carotenoids released from the food matrix get incorporated into mixed micelles before being available for absorption. Bioaccessibility of carotenoids depend on formation of micelles as they are responsible for transporting liposoluble compounds to the intestine. Digestibility and absorption of carotenoids depends on food matrix (i.e. presence of other carotenoids, dietary fat and fiber), food processing, co-ingested food and nutrients status (van het Hof, West, Weststrate, & Hautvast, 2000). During gastric digestion, presence of dietary fiber reduces carotenoids micellization as fluids become soluble in the gel. The fat solubility of these compounds is modified by esterification of xanthophylls with fatty acids. Different food processing methods such as cooking, microwaving, and pasteurization disrupts protein-carotenoid complexes and soften cell wall resulting in increase in carotenoid release, and in turn its bioaccessibility (Parker, 1996). The literature pertaining to the bioaccessibility of carotenoids and effect of processing on carotenoids has been summarized in Table 1. Pro-vitamin A (β-carotene, α-carotene, β-cryptoxanthin) is the main precursor of vitamin A and involved in decreasing risk of many chronic diseases. Estevez-Santiago, Olmedilla-Alonso, & Fernandez-Jalao, 2016 evaluated bioaccessibility of pro-vitamin A carotenoids from fruits (Loquat, Mandarin, Orange, Peach, Pepper, Persimmon and watermelon). Bioaccessibility of β-cryptoxanthin and β-carotene ranged from 0.02% to 9.8% and 0.1%–9.1%, respectively. They also reported that bioaccessibility of α-carotene varied between 0% and 4.6% and observed increase in carotenoid bioaccessibility by different food processing methods when compared with raw food. Bioaccessibility of carotenoids were estimated using in-vitro gastro-intestinal digestion method from 12 Andean potato clones. The potato carotenoids were dominated by lutein, zeaxanthin, followed by antheraxanthin, 369

Spinach, tomato paste, pineapple, red pepper Fresh tomato; Sun-dried; canned tomato Heat processed Sweet potato Control (No Fat): Cylinders (Boiling; steaming; microwave heating) Slices (Low temperature blanching+ boiling; boiling) With Fat (2.5%) Cylinders (Boiling; steaming; microwave heating) Slices (Low temperature Blanching+ boiling; boiling) Raw carrot; raw + cooked; low temperature blanching +Ca + cooked; high pressure + Ca + cooked; high temperature blanching + cooked Bell peppers (red, green and yellow)

6. 7. 8.

370

Yellow fleshed potatoes

Orange segment; orange homogenate; juice fresh; juice fresh pasteurized; juice pasteurized Yellow fleshed potato (Boiled 12 potato tuber clones)

Chick pea and amaranthus mixture

Cabbage (Duchy, Kale, Scots Kale, Kalorama, mean cabbage) Plum (Cherry plum, Plum 620, Ersinger, Italian plum, mean plum) Loquat; mandarin; orange; peach; pepper; persimmon; watermelon

14.

15.

17.

18.

20.

19.

16.

Raw pumpkin; boiled pumpkin; steamed pumpkin; deep fried pumpkin Raw butternut squash; boiled butternut squash; steamed butternut squash; deep fried squash

Green gram + amaranth leaves mixture

13.

12.

Raw tomato; Raw tomato+ low temperature blanching; Raw tomato+ high temperature blanching Butternut squash, carrot, sweet potato, tomato

11.

10.

9.

4. 5.

3.

Chilli peppers (red kenya, red turkey, green kenya, green turkey)

Raw carrot; homogenized (pulped) carrot; cooking; addition of oil to cooked pulp Raw tomato+ 2 min heating at 88 °C Raw tomato+ 15 min heating at 88 °C Raw tomato+ 30 min heating at 88 °C Carrot (carrot canned; carrot juice; carrot puree; carrot raw) Spinach (spinach boiled; spinach leaves; spanich minced) Tomato (tomato raw; tomato processed) Crude Tomato; Tomato Sauce Crude carrot; cooked carrot; cooked carrot containing 10% olive oil

1.

2.

Food/processing Methods

Sr No.

β - carotene

β - carotene

β – cryptoxanthin

β- carotene

Lutein Zeaxanthin Total carotenoids

Lutein Zeaxanthin β - carotene

6.6%; 6.8%, 0.9%; 3.6%; 4.5% 3.6%; 11.0%; 9.0%; 3.4%; 6.8% 0.02%; 0.28%, 1.07%; 3.35%; 6.31%; 0.80%; 9.84% 0.10%; 1.51%; 1.80%; 1.55%; 3.46%; 9.08%; 6.10% 10.56%; 11.42; 12.76%; 68.86% 1.65%; 2.03%; 2.38%; 22.32%

33–71% 51–71% 10.8%; 11.9%; 28.3%; 37.6%; 39.6% 55–160% 24–388% 3% (fresh); 5% (dehydrated)

16.5%; 21.6; 13.7%, 15.5 15.9%, 40.5%, ND, 58.6% 2.72% (fresh); 5.17% (dehydrated)

β - carotene Lutein Total carotenoids

β - carotene β - carotene β - cryptoxanthin Lutein Zeaxanthin β - carotene β - cryptoxanthin Lutein Zeaxanthin Lycopene

0.86%; 0.88%; 0.53 1.10%; 0.95%

25.5%; 100%; 98.7%; 70.6% 28.67%; 58.05%; 21.83%

54% 171% 164% 2.68%; 14.14%; 4.39; 2.56% 17.45%; 2.43%; 5.20% < 0.1%; 5.97% 0.1%, 1.6% 29%; 52%; 80%

3%; 21%; 27%; 39%

Bioaccessibility (%)

19.87%; 20.20%; 11.25% 21.75%; 18.73% 5.12%; 34.35%; 16.09%; 10.36%; 31.42% 6.2%; 13.4%; 12.7% 33.1%; 74.7%; 112.8% 54.3%; 45.9%; 63.7% 87.6%; 66.2%; 76.5% 16.9%; 11.6%; 15.1%; 8.2% 78.3%; 30.3%; 34.7%; 59.1% 106.2%; 67.0%; 40.0%; 36.3% 64.2%; 86.1%, 106.9%; 34.1% 5.1%, 9.2%, 9.7%

β - carotene Lycopene Trans β - carotene

Lycopene β - carotene

β - carotene

Lycopene

Carotenoids

Type of carotenoids

Table 1 Effect of in-vitro gastro-intestinal simulated digestion on bioaccessibility of carotenoids.

Deep-frying enhanced the bioaccessibility of β carotene

–

Dehydration increased bioaccessibility of total carotenoids –

Pasteurization increased bioaccessibility of β carotene –

Dehydration increased bioaccessibility of total carotenoids –

–

Processing increased bioaccessibility

–

Thermal processing increased bioaccessibility

Processing increased bioaccessibility Cooking and addition of oil increased bioaccessibility – Sun-drying increased bioaccessibility of lycopene Addition of fat increased bioaccessibility of trans β - carotene

Processing increased bioaccessibility

Cooking and addition of oil increased bioaccessibility Heating increased bioaccessibility of lycopene

Effect of processing on bioaccessibility

(continued on next page)

Koh and Loh (2018)

Estévez-Santiago, OlmedillaAlonso, and Fernández-Jalao (2016)

Kaulmann et al. (2016)

Prakash and Oghbaei (2015)

Andre et al. (2015)

Aschoff et al. (2015)

Burgoes et al. (2013)

Oghbaei and Prakash (2013)

Jeffery et al. (2012)

Svelander et al. (2010)

O'Sullivan et al. (2010)

Lemmens et al. (2009)

Reboul et al. (2006) Hornero-Méndez and MínguezMosquera (2007) Granado-Lorencio et al. (2007) Karakaya and Yilmaz (2007) Bengtson et al. (2009)

Reboul et al. (2006)

Dewanto et al. (2002)

Hedrén, Diaz, and Svanberg (2002)

Reference

N. Thakur, et al.

Trends in Food Science & Technology 97 (2020) 366–380

Trends in Food Science & Technology 97 (2020) 366–380

Lycopene Tomato sauce tomato sauce homogenized tomato sauce homogenized tomato sauce homogenized tomato sauce homogenized

0.5% 1.9% 1.5% 1.9% 4.7%

Addition of extra virgin oil alone and in combination with heating increased bioaccessibility

Tomas et al. (2019)

tomato to around 17% in boiled spinach. In a study conducted by Bengtsson, Alminger, & Svanberg, 2009, invitro digestion model was used to evaluate the bioaccessibility of βcarotene from differently heat processed sweet potato. The bioaccessibility of β-carotene varied between 0.5% and 1.1% in the heat-processed sweet potato without fat and addition of 2.5% cooking oil increased β-carotene bioaccessibility which ranged from 11% to 22%. These data suggest the importance of fat for enhancement of β-carotene bioaccessibility and also reported that short period of heat treatment was not sufficient for complete breakdown of the sweet potato cell matrix in case of microwaved samples. High in-vitro bioaccessibility of β-carotene from heat-processed sweet potato indicated that sweet potato can be considered as promising dietary source to overcome vitamin A deficiency. Hornero-Méndez & Mínguez-Mosquera, 2007 reported that thermal treatment during cooking of carrot have a positive effect on the micellarization of carotenes and thus significantly improve carotenoids bioaccessibility in carrots. The bioaccessibility of carrot was found to be higher in cooked carrots (52%) than raw carrots (29%) and further increase to 80% in carrots containing 10% olive oil. Fresh unprocessed orange segments, homogenized segments, freshly squeezed juice, pasteurized juice, flash-pasteurized juice were analysed for bioaccessibility of total carotenoids (Aschoff et al., 2015). A decrease in total carotenoid level was noted during the processing of fresh oranges (224 μg/100 g of Fresh weight (FW)) into pasteurized orange juices (178−184 μg/100 g of FW). Only 10.8% of the carotenoids in fresh orange segments were micellarized. Highest concentrations of bioaccessible carotenoids were observed in the flash-pasteurized (67.1 μg/100 g) and pasteurized (72.7 μg/100 g) juices. The bioaccessibility of total carotenoids was significantly higher in the pasteurized juices (37.6–39.5%) than in the freshly squeezed juice (28.3%). Reboul et al., 2006 conducted bioaccessibility studies in lycopene content of crude tomato and processed tomato and reported that the bioaccessibility of lycopene ranged from 0.1% to 1.6% in raw and processed tomato sauce, respectively. Increase in bioaccessibility in tomato sauce was found to be 16 fold indicating that heat treatment cause rupturing of cell wall which favours release of lycopene content from chloroplast and in turn enhance lycopene bioaccessibility. Karakaya & Yilmaz, 2007 reported that lycopene content was 1.74 mg/ 100 g, 5.51 mg/100 g and 3.55 mg/100 g in fresh, sun-dried and canned tomatoes, respectively. Highest bioaccessibility was observed in sun dried tomatoes (58.05%) followed by fresh tomatoes (28.67%) and canned tomatoes (21.83%). In-vitro bioaccessibility of lycopene significantly increased from 5.1% (raw tomato) to 9.2% (raw tomato + low temperature blanching) and 9.7% (raw tomato + high temperature blanching), however, further boiling showed no significant change in lycopene bioaccessibility (Svelander et al., 2010). The lycopene content in raw tomato (3.11 mg/g) increased to 3.11, 5.45 and 5.32 mg/g after 2, 15 and 30 min of heating at 88 °C as reported by Dewanto et al., 2002. Thermal processing enhanced nutritive value of tomato by increasing bioaccessible lycopene content from 54 to 164% with increase in heating at 88 °C. Tomas, Sagdic, Catalkaya, Kahveci, & Capanoglu, 2019 reported bioaccessibility of lycopene in raw tomato sauce to be 0.5% that increased significantly by addition of extra virgin olive oil. The lycopene bioaccessibility increased by 1.9% and 1.5% by addition of extra virgin olive oil at 5% and 10%, respectively. Bioaccessibility was further increased to 4.7% (8.5 fold) by cooking + addition of extra virgin olive oil compared to control tomato sauce (without oil and cooking). Overall the results indicated that cooking methods have significant effect on bioaccessibility of carotenoids. 3.2. Bioaccessibility of polyphenols Polyphenols are considered as the largest group of food components that contain thousands of compounds found in various fruits and vegetables. Polyphenols can be divided into two groups i.e. flavonoids and

21.

Sr No.

Table 1 (continued)

with with with with

5% extra virgin oil 10% extra virgin oil 5% extra virgin oil+ heating 10% extra virgin oil+ heating

Type of carotenoids Food/processing Methods

Bioaccessibility (%)

Effect of processing on bioaccessibility

Reference

N. Thakur, et al.

371

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

Fig. 3. Types of polyphenols.

non-flavonoids. Flavonoids consist of the flavonols, flavones, isoflavones, flavanones, anthocyanidins, and flavanols, however, non-flavonoids comprise the phenolic acids (hydrobenzoic and hydroxycinnamic acids), lignans, and stillbenes (Fig. 3). Polyphenols are associated with the prevention of cardiovascular heart disease, cancers, inflammatory diseases, neurodegenerative diseases, and gastrointestinal disorders (Gonzalez-Gallego, Garcia-Mediavilla, SanchezCampos, & Tuno, 2010; Scalbert & Williamson, 2000). Polyphenolic concentration can be affected by various factors such as soil type, rainfall, fruit yield, mode of cultivation (cultured in greenhouses or in fields), etc. (Manach, Scalbert, Morand, Remesy, & Jimenez, 2004). Nagy, Daood, Ambrozy, & Helyes, 2015 studied the effect of ripening stages of new hybrids of chili peppers and reported that most dominant polyphenols in hybrids either increased or remained unchanged during ripening. Effect of irrigation and foliar sulfur addition on phytochemical compounds of brocolli was studied by Pek, 2012. Only gallic acid increased significantly by foliar sulfur application in irrigated treatment. Polyphenols present in food are usually attached with carbohydrate moiety. During gastrointestinal digestion polyphenols get detached from its carbohydrate moiety making it more bioaccessible. Bioaccessibility of some polyphenols, like quercetin and hesperidin depend upon the type of attached sugar also (Scholz & Williamson, 2007). Reduction in bioaccessibility of the procyanidins compound was observed due to formation of protein-procyanidins complex (Keogh, McInerney, & Clifton, 2007). Polyphenols when absorbed undergoes various processes like methylation, sulfation, and glucuronidation inside intestinal cells. Unabsorbed polyphenols reach the colon where the microflora hydrolyze the glycosides into aglycones and convert them into aromatic acids such as hydroxyphenylacetic acids, hydroxyphenylpropionic acids and flavanones etc. (Manach, Scalbert, Morand, Remesy, & Jimenez, 2004). Some part of polyphenols absorption might take place in the large intestine. The data generated by previous researchers on bioaccessibility of polyphenols and effect of processing on polyphenols had been compiled in Table 2. Based on an in vitro study carried out in grapes, it was observed that only 62% of polyphenols were bioaccessible in grapes (Tagliazucchi, Verzelloni, Bertolini, & Conte, 2010). The amount of bioaccessible total polyphenols, flavonoids and anthocyanins decreased as the environment changed from acidic gastric phase to alkaline intestinal phase. At the end of entire phase of digestion the total flavonoids and anthocyanin bioaccessible fraction correspond to 56.1% and 7.6%, respectively. Andre et al., 2015 reported that phenolic profile of 12 potato clone extracts was dominated by chlorogenic acid followed by neochlorogenic acid, cryptochlorogenic acid, caffeic acid, rutin,

kaempferol-3-rutinoside and ferulic acid. Bioaccessibility of total chlorogenic acid ranged from 12 to 82%, however mean bioaccessibility value for total chlorogenic acid was 24.5%. Bioaccessibility of anthocyanins in purple-fleshed potato clones ranged from 40 to 81%. Miranda, Deuber, & Evers, 2013 conducted a study to evaluate the bioaccessibility of polyphenols in boiled tubers of two potato varieties (Vitelotte and Nicola) and sweet potato. Chlorogenic acid was the most dominated polyphenol in Vitelotte, Nicola and sweet potato followed by cryptochlorogenic acid, neochlorogenic acid and caffeic acid. Results showed that the concentration of polyphenols were higher in gastric and intestinal filtrate compared to its concentration in boiled potatoes and sweet potato. The percentages of initial amount of polyphenols present in gastric and intestinal filtrate were 234.8%, 520.6%, 117.5% and 126.5%, 541.8%, 163.1% in Nicola, Vitelotte and sweet potato, respectively. Bermudez-Soto et al., 2007 investigated effects of in-vitro gastic and intestinal digestion on bioaccessibility of polyphenols in chokeberry juice. They reported that during gastric digestion no significant effect was observed on major phenolic compounds viz. anthocyanins, flavan-3-ols, flavonols and caffeic acid derivatives in chokeberry. However, these compounds varied significantly during pancreatic digestion. Approximately 43% of anthocyanins lost during intestinal digestion, flavonols and flavan-3-ols decreased by 26% and 19%, respectively. Neochlorogenic acid decreased after digestion by 28% whereas an increase was observed in chlorogenic acid by 24%. Kamiloglu & Capanoglu, 2013 observed that intestinal fraction of the whole-fresh yellow and purple figs contain 10% and 6% of the initial chlorogenic acid values, respectively. In case of rutin content, intestinal fractions contained 12% for whole-fresh yellow and 16% for purple figs. Percent recoveries of both chlorogenic acid and rutin were higher in pulp compared with skin for each variety. Sun-drying of fig fruit resulted in increased bioaccessibility of chlorogenic acid in yellow figs (33%) as well as purple figs (73%). Effect of dehydration was studied on bioaccessibility of polyphenols and flavonoids in green gram amaranthus mixture (Oghbaei & Prakash, 2013). Dehydration resulted in decrease in polyphenol and was 50.5% in fresh and 48.5% in dehydrated mixture. Flavonoids were 37.9% in fresh mixture and 32.9% in dehydrated mixture. In another study carried out by Prakash & Oghbaei, 2015, similar results of dehydration process was obtained in chick pea amaranthus mixture where polyphenol reduced from 50% (fresh) to 39% (dehydrated) and flavonoid from 40% to 36% (dehydrated). They concluded that during dehydration heat sensitive antioxidants reduced, however concentration of heat stable ones remains same. The total extractable polyphenols bioaccessible fraction for whole cashew-apple juice showed bioaccessibility up to 39%, while low 372

Orange juice hand squeezing

Orange juice commercial pasteurized Strawberry

1.

2.

Mulberry

Green gram and amaranth leaves (Fresh, Dehydrated)

5.

6.

373

Cabbage (Duchy, Kale, Scots Kale, Kalorama, mean cabbage) Plum (Cherry plum, Plum 620, Ersinger, Italian plum, mean plum) Brown rice Improved Extrusion Cooking treatment (IECT) Wheat IECT Oat IECT Raw cardoon; cardoon fried in olive oil; cardoon fried in sunflower oil; cardoon griddled Fresh apples; Conventional dried apples; Frozen apples with liquid nitrogen; freeze + dried apples Beetroot (Fresh; Freezing with liquid nitrogen,-80 °C

13.

17.

16.

15.

14.

12.

Chick pea and amaranthus mixture (fresh and dehydrated) Black carrot jam + marmalades (fresh, heating)

Potato cv. Nicola Potato cv. Vitelotte Sweet potato Cashew apple juice Cashew apple fibre Potato clone extracts

Total Polyphenolic compound Total Polyphenolic content Total Polyphenolic content Antioxidant Activity

Phenol

Total Polyphenols

Total Chlorogenic acids Total Anthocyanins Polyphenols Flavonoids Total Phenols

Total polyphenols

Chlorogenic acid Rutin Chlorogenic acid Rutin Polyphenols

46% (Fresh beetroot); 55% Frozen beetroot 53% (Fresh beetroot); 68% Frozen beetroot

68%; 53%, 41%; 45%

20.87% (Raw) 20.57% (IECT) 11.60% (raw) 12.48% (IECT) 29.83 (raw) 21.78% (IECT) 1.96%; 66.84%; 64.17%; 60.01%

ND; 0.14%; 0.38%; 0.27%; 0.26%

Dehydration decreased bioaccessibility of polyphenols and flavonoids

Andre et al. (2015) Oghbaei &Prakash (2015) Kamiloglu et al. (2015) Kaulmann et al. (2016)

– Dehydration decreased bioaccessibility of polyphenols and flavonoids

–

Freezing increased bioaccessibility of total polyphenols and antioxidant activity in beetroot

Freezing decreased bioaccessibility of polyphenolic compounds

Frying in olive oil increased bioaccessibility of polyphenolic compounds

Improved Extrusion Cooking treatment increased bioaccessibility of phenols in wheat however decreased in brown rice and oat

(continued on next page)

Dalmau et al. (2019)

Dalmau et al. (2017)

Juániz et al. (2017)

Zang et al. (2016)

De Lima et al. (2014)

Bioaccessibility is more in cashew apple juice as compared to cashew apple fibre

Heating increased bioaccessibility of phenols

Miranda et al. (2013)

–

Kamiloglu & Capanoglu (2013)

Oghbaei &Prakesh (2013)

Liang et al. (2012)

–

–

Bermudez-Soto et al. (2007) Tagliazucchi et al. (2010)

Gil- Izquierdo et al. (2002)

Gil- Izquierdo et al. (2001)

Reference

–

Jam formation decreased bioaccessibility of individual polyphenols

Pasteurized technique increased bioaccessibility of soluble flavonoids

Effect of processing on bioaccessibility

Drying of yellow figs increased chlorogenic acid and rutin bioaccessibility, however, in purple figs drying increased chlorogenic acid but decreased rutin bioaccessibility

62.4% 56.1% 7.6% 0.34% 7.33% 50.5% (fresh); 48.5% (dehydrated) 37.9% (fresh); 32.9% (dehydrated)

56.7%; 81.2%; 71.6%; 123.6%

2.3%; 3.7%; 3.8%; 6.1%; 9.7%; 6.1%; 12.0

6.6%; 12.6%; 11.7%; 20.6%; 172.8%; 28.3%; 27.4%

10.5%; 16.2%; 12.0%; 18.6% 31.1%; 37.3%; 35.8%; 29.9%

Bioaccessibility (%)

10%; 33% 12%; 13% 6%; 73% 16%; 9% 126.5% 541.8% 163.1% 39% 18.6% 12–82% 40–81% 50% (fresh); 39% (dehydrated) 40% (fresh); 38% (dehydrated) 4.9%–12.5% (fresh); 7.2%–17.5% (heating) ND; 6.3%; ND; ND; 6.3%

Cyanidin-3-glucoside, Pelargonidin-3-glucoside, Pelargonidin-rutinoside, Ellagicacid-arabinoside, Ellagic acid, Quercetin-3- glucoside, Kaempferol-3glucoside Cyanidin-3-glucoside, Pelargonidin-3-glucoside, Pelargonidin-rutinoside, Ellagicacid-arabinoside, Ellagic acid, Quercetin-3- glucoside, Kaempferol-3glucoside Cyanidin-3-glucoside, Quercetin-3-glucoside, neochlorogenic acid, chlorogenic acid Total polyphenols Total Flavonoids Anthocyanins Anthocyanins Phenols Total Polyphenols Total Flavonoids

Soluble Flavonoids (Narirutin, Hesperidin, Total flavanones, Vicenin 2) (Narirutin, Hesperidin, Total flavanones, Vicenin 2)

Type of polyphenols

11.

10.

9.

8.

Fresh purple figs; dried purple figs

Fresh yellow figs; dried yellow figs

Grapes

4.

7.

Chokeberry

3.

Strawberry jam

Food/Processing method

Sr No.

Table 2 Effect of in-vitro gastro-intestinal simulated digestion on bioaccessibility of polyphenols.

N. Thakur, et al.

Trends in Food Science & Technology 97 (2020) 366–380

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

Total Anthocyanin content

Strawberries(Fresh; Frozen) 18.

Table 2 (continued)

Total Polyphenolic content Total Flavonoid content

94% (Fresh strawberries); 105% (Frozen strawberries) 64% (Fresh strawberries); 91% (Frozen strawberries) 47% (Fresh strawberries); 83% (Frozen strawberries)

Freezing increased bioaccessibility of polyphenols, flavonoids and anthocyanin content in strawberries

Kamiloglu (2019)

bioaccessiblility was observed for the cashew-apple fibre (De Lima et al., 2014). High bioaccessibility in cashew-apple juice compared to cashew-apple fibre is due to presence of low concentration of phytates and tannins in fruit juice, hence the consumption of cashew apple juice was highly recommended. Jyothi lakshmi & Kaul, 2011 found that bioaccessibility of total polyphenols was quite low and differed within cabbage and plum varieties with highest bioaccessibility obtained in cabbage kale (6.3%) and lowest in plum 620 (0.1%). Black carrot jams + marmalades are considered as good sources of polyphenols with high bioaccessibility levels ranging from 4.9 to 17.5% (Kamiloglu, Pasli, Ozcelik, Van Camp, & Capanoglu, 2015). In addition, jam and marmalade processing led to increase in bioaccessiblility of total phenolics (7.2%–12.6%). The reason may be heat treatment applied during jam and marmalade processing causing structural changes that would end up with higher bioaccessibility of phenolics and this increase can be related to the release of bound antioxidants as a result of heat treatment. Studies on in-vitro simulation was conducted by Gil-Izquierdo, Zafrilla, & Tomas-Barberan, 2001 and soluble flavonoids (narirutin, hesperidin, total flavanones and vicenin 2) were analysed in both handsqueezed and pasteurized commercial orange juices. The bioaccessibility of total flavonoids ranged from 10.5% to 31.1% (narirutin), 16.2%–37.3% (hesperidin), 12.0%–35.8% (total flavanones) and 18.6%–29.9% (vicenin 2) indicating that pasteurization increased the bioaccessibility of polyphenols in orange juice. In another study, GilIzquierdo, Zafrilla & Tomas-Barberan, 2002 found that bioaccessibility of individual phenolic was considerably low in strawberry jams (2.3%–12.0%) as compared to strawberry (6.6%–172.8%) in the dialyzed fraction. These results showed that during digestion strawberry anthocyanins gets degraded and ellagitannins converted to free ellagic acid resulting in a ten-fold increase of this compound. Zeng, Liu, Luo, Chen, & Gong, 2016 reported that bioaccessiblility of phenolics was maximum for brown rice followed by oat and wheat using Improved Extrusion Cooking Treatment (IECT). Bioaccessibility of phenolics decreased significantly in oat by 29.83% (raw) to 21.78% (IECT) while effect on brown rice and wheat was minimum. Thus, it can be concluded that bioaccessibility of phenolic content varied in cereals depending on cereal matrix. Cooking process/heat treatment exerts a positive effect on the bioaccessibility of polyphenols due to softening of cell wall (Palermo, Pellegrini, & Fogliano, 2014). After gastrointestinal digestion only 2% of phenolic compounds were bioaccessible in raw cardoon (Cynara cardunculus). In cooked cardoon samples, maximum bioaccessibility was achieved in cardoon fried in olive oil (66.84%) followed by cardoon fried in sunflower oil (64.17%) as observed by Juániz et al., 2017. Their study indicated that bioaccessibility of antioxidants is influenced by cooking medium as well. Bioaccessibility of anthocyanins and phenolics decreased after the intestinal digestion and the recoveries were only 0.34% and 7.33% in anthocyanins and phenolics, respectively (Liang et al., 2012). The decrease in content of anthocyanins is still unclear, however it was hypothesized that during heat treatment anthocyanin metabolized or degraded into another form that escapes detection. Perez-Vicente et al., 2002 reported that bioavailability of anthocyanins depends upon stability of molecule and in mild alkaline environment of the small intestine anthocyanins were highly unstable resulting in low bioavailability of these compounds. Freezing is common method used to preserve food. In case of fruits and vegetables, this technique cause structural changes resulting in softening of tissue and in turn affect the bioaccessibility of phytonutrients. Dalmau, Liabres, Eim, Rossello, & Simal, 2019 studied the effect of freezing on bioaccessibility of bioactive compounds in beetroot. They reported that liquid nitrogen resulted in increase in antioxidants’ bioaccessibility from 53% (fresh beetroot) to 68% (frozen beetroot samples). Bioaccessibility of total phenols in beetroot increased from 46% (fresh beetroot) to 55% (frozen beetroot samples). In another study, Dalmau, Bornhorst, Eim, Rossello, & Simal, 2017 reported that total polyphenol content decreased significantly in frozen 374

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

(5.1–2.7mgGAE/g), freeze dried (2.9–1.3mgGAE/g) and conventional dried apples (4.4–3.0mgGAE/g) during in-vitro gastric digestion. Raw apples showed minor decrease during in-vitro gastric digestion i.e. from 4.4 to 3.0mgGAE/g and retained maximum concentration of polyphenolic compounds. Kamiloglu, 2019 evaluated bioaccessibility of polyphenols in frozen strawberries and reported increase in bioaccessibility of total flavonoids (90.8%) and total anthocyanins (83.4%) in frozen strawberries as compared to fresh strawberries where bioaccessibility of total flavonoids was 64.4% and total anthocyanin was 47.2%. 3.3. Bioaccessibility of vitamin C and vitamin E Vitamins present in the fruits and vegetable are essential for human health and helps to maintain metabolism of body. Vitamin C and Vitamin E intake reduces the risk of several cardiovascular, neurodegenerative diseases and age related eye diseases (Harrison & May 2009). Vitamin C is considered as an important water-soluble antioxidant which mainly occurs in citrus fruits, green peppers, cabbage and green leafy vegetables (Fig. 4). The content of vitamin C is affect by environmental conditions and processing methods. In case of chili peppers, vitamin C content increased with increasing ripening stage (Nagy et al., 2015). Koncsek, Daood, & Helyes, 2016 observed that paprika spice colour stability was dependent upon temperature, drying of fresh crop and processing technology and quality of paprika spice was best preserved at 10-20 °C. Home produced spice paprika was found to be more stable than imported sun dried product due to high level of vitamin C (2028 μg/g). Vitamin C acts as antioxidant mainly in

Fig. 4. Biosynthetic pathway of Vitamin C.

Fig. 5. Biosynthetic pathway of Vitamin E. 375

Trends in Food Science & Technology 97 (2020) 366–380

Andre et al. (2015) Al-Yafeai and Böhm (2018)

Bioaccessibility of vitamin C is more in cashew apple juice as compared to cashew apple fibre – –

De Lima et al. (2014)

water soluble environments by preventing oxidation of other compounds (Padayatty & Levine, 2001). It also plays protective role in lipids by regenerating vitamin E to its active α-tocopherol form (Schlueter & Johnston, 2011). It is ingested in both reduced (ascorbic acid) and oxidised form (dehydroascorbic acid). Vitamin C is absorbed throughout the small intestine epithelium by different transporters. Ascorbic acid is absorbed mainly in ileum and jejunum via sodiumdependent active transport (SVCT 1), however, dehydroascorbic acid is absorbed by facilitated diffusion in duodenum and jejunum with glucose transporters (Malo & Wilson, 2000). The main metabolic role of vitamin E as a rapid soluble potent antioxidant is to protect the cell from reactive oxygen species produced from oxidation of lipids (Fig. 5). The most common sources of vitamin E are oil containing grains and vegetables. Besides liposoluble antioxidants, it also exhibits non antioxidant activities such as gene expression modulation, regulation/inhibition of cell proliferation and aggregation of platelet cell (Borel, Preveraud, & Desmarchelier, 2013). The first phase of digestion-absorption process is dissolution of vitamin E, emulsification process occurs during both gastric and duodenal phase for formation of lipid droplets. It was found that vitamin E does not degrade/absorbed in the stomach, however, was absorbed through passive process across intestinal mucosa and incorporated into micelles/chylomicrons (Reboul et al., 2006). Vitamin E can be absorbed directly from epithelial cells into circulation by HDL efflux. Pancreatic enzyme aids absorption of vitamin E (Kiela & Ghishan, 2016). After intestinal absorption α-tocopherol is transported to liver parenchymal cells where most of fat soluble vitamins are stored (Drevon, 1991). Literature on bioaccessibility of vitamin C and vitamin E has been tabulated in Table 3. Reboul et al., 2006 found that the bioaccessibility of vitamin E varied for different dietary sources and is dependent on food matrix. Bioaccessibility of α-tocopherol in almonds, apples, bananas, cereals and hazel nuts were 14.18%, 0.47%, 98.80%, 53.29% and 10.49%, respectively. Bioaccessibility of β-tocopherol ranged from 6.54% to 47.50%. Maximum bioaccessibility of α-tocopherol and βtocopherol was obtained in bananas and cereals, respectively, as compared to almonds, apples and hazel nut. O'Callaghan & O'Brien, 2010 obtained 11% bioaccessibility of α-tocopherol in apple sauce. Al-Yafeai & Böhm, 2018 observed that vitamin E bio-accessibility in tomato paste significantly increased after treatment with fructozym enzyme (highly concentrated pectolytic enzyme prepared for quick and complete pectin hydrolysis) and reported 78% bioaccessibility of vitamin E during simulated digestion. Perez-Vicente et al., 2002 reported that after pepsin digestion of pomegranate juice 29% loss was observed in vitamin C, however, after intestinal digestion greater than 95% degradation of vitamin C occurred. Bioaccessibility of vitamin C in pomegranate juice after complete digestion was only 2.5%. It has been reported that vitamin C is strongly affected by changes in pH during gastric and intestinal phase. The acidic conditions of gastric environment protect vitamin C against enzymatic or chemical oxidation hence less degradation occurred in gastric phase, however, vitamin C get easily oxidised at pH greater than 4 in intestinal phase and degraded by interactions with metal ions (Jeney-Nagymate & Fodor, 2008). In another study, the bioaccessibility of vitamin C in broccoli inflorescence was analysed by Fernando Vallejo, Gil-Izquierdo, Perez-Vicente, & Garcia-Viguera, 2003. Bioaccessible content of vitamin C was only 2.2 mg/100 g of the initial concentration (63.8 mg/100 g) which corresponds to 3.4% bioaccessibility of vitamin C in broccoli inflorescence. They reported slight loss (6.7%) after pepsin digestion whereas there was significant decrease in vitamin C (96.6%) after in vitro intestinal digestion. A high vitamin C bioaccessibility range (44%–83.7%) has been reported by Cilla et al., 2011 in blended fruit juices made with grape, sweet orange, apricot and peach after 135 days of storage. Cilla et al., 2012 reported 12.8% bioaccessibility of vitamin C in the beverages prepared from mixture of fruit juices (orange, pineapple, kiwi and mango) + soymilk. De Lima et al., 2014 compared the bioaccessibility of vitamin C using in vitro

Vitamin C Vitamin E

26.2% 10.2% 16%–46.08% 78%

O'Callaghan & O'Brien. (2010) Cilla et al. (2011) Cilla et al. (2012) – – –

8. 9.

7.

Apple sauce Blended fruit juices (grape, sweet orange, apricot and peach) Drink made up of fruit juices (orange, pine apple, kiwi, mango) + soymilk Cashew apple juice Cashew apple fibre Boiled potato (12 potato clones) Tomato paste 4. 5. 6.

Vitamin C

Perez-Vicente et al. (2002) Vallejo et al. (2003) Reboul et al. (2006) – – – Pomegranate juice Broccoli Almonds; apples; bananas; cereals; hazel nut 1. 2. 3.

Vitamin C Vitamin C Vitamin E (α-tocopherol) (β-tocopherol) Vitamin E (α-tocopherol) Vitamin C Vitamin C

2.5% 3.4% 14.18; 0.47; 98.80; 53.29; 10.49 19.76; 6.54; 6.88; 47.50; 24.52 11% 44–83.7% 12.8%

Reference Effect of processing on bioaccessibility Bioaccessibility (%) Vitamins Food/processing methods Sr No.

Table 3 Effect of in-vitro gastro-intestinal simulated digestion on bioaccessibility of Vitamin C and Vitamin E.

N. Thakur, et al.

376

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

Table 4 Effect of in-vitro gastro-intestinal simulated digestion on bioaccessibility of minerals. Sr No.

Food/processing method

Minerals

Bioaccessibility (%)

Effect of processing on bioaccessibility

Reference

1.

Wheat grain Commercial wheat grass Cucumber Squash Apple Whole meal (watermelon seed) Defatted flour (watermelon seed) Pakchoi Malabar spinach Cashew apple juice Cashew apple fibre Boiled Potatoes (12 Potato clones) Sweet potato (grown in Satipo) Sweet potato (grown in San Ramon) Berries

K, Mn, Zn, Fe K, Mn, Zn, Fe Fe, Zn Fe, Zn Fe, Zn Fe, Zn, Ca

37.6%, 23.1%, 23.2%, 8.8% 45.7%, 27.7%, 42.9%, 31.1% 12%, 11% 6.8%, 10% 9.7%, 55% 8.7%, 24.5%, 8.1%

–

Kulkarni et al. (2007)

–

Khouzam et al. (2011)

–

Jyothi lakshmi and Kaul (2011)

Fe, Zn, Ca

8.3%, 18.7%, 16.1%

Cd, Cd, Cu, Cu, Fe

36.8%, 20% 39.1%, 23.9% 15, 11.5, 3.7 4.0, 1.2, 2.2 63.7%–79%

–

Fu and Cui (2013)

Bioaccessibility of minerals is more in cashew apple juice as compared to cashew apple fibre -

De Lima et al. (2014) Andre et al. (2015)

53%–67.7%

-

Andre et al. (2018)

-

Pereira et al. (2018)

2.

3.

4. 5. 6. 7.

8.

Pb Pb Fe, Zn Fe, Zn

Fe

24.9%–64.3% Al, Ba, Cu, Fe, Mn, Zn

10%, 74%, 41%, 9%, 34%, 18%

gastro-intestinal method in cashew apple juice and cashew apple fibre. The results showed that bioaccessibility of vitamin C is more in cashew apple juice (26.2%) when compared with cashew apple fibre (10.2%). Bioaccessibility studies for vitamin C in boiled tubers of 12 potato clone extracts was conducted and bioaccessibility of vitamin C in range from 16% to 46.08% was reported (Andre et al., 2015). Processing method significantly influenced the bioaccessibility of vitamins.

bioaccessibility in the samples varies according to their polyphenolic content. Results shown that maximum bioaccessibility occurred in Ba followed by Cu and Mn, while lower values were obtained in case of Al, Fe and Zn. The phytates and fibres present in fruit form complexes (soluble or insoluble) with minerals in the gastro-intestinal tract resulting in poor bioaccessibility of Zn and Fe. Kulkarni, Acharya, Rajurkar, & Reddy, 2007 reported that bioaccessibilities of potassium (K), Mn, Zn and Fe were higher for wheatgrass as compared to wheat grain. It was observed that bioaccessibility percentage was higher in intestinal phase than gastric phase in all the tested samples. The percent bioaccessibility of K, Mn, Zn and Fe ranged from 8.8% to 37.6% in wheat grain and 27.7%–45.7% in wheat grass. In both wheat grass and wheat grain, potassium appeared to be most bioaccessible element. In another study, Fu & Cui, 2013 reported that the average bioaccessibility of cadmium (Cd) for pakchoi was 68.2% in the gastric phase and 36.8% in the small intestine. Average Cd bioaccessibility was 50.8% (gastric phase) and 39.1% (intestine phase) for Malabar spinach, respectively. The results showed that maximum bioaccessibility for Cd was obtained in the gastric phase whereas lead (Pb) bioaccessibility was higher in the small intestinal phase. In the gastric phase, the average Pb bioaccessibility was 10.8% and 15.6% for the pakchoi and Malabar spinach, respectively, whereas in small intestinal phase, the average Pb bioaccessibility was 20.2% for pakchoi and 23.9% for Malabar spinach, respectively. De Lima et al., 2014 carried out bioaccessibility studies of minerals in cashew apple juice and cashew apple fibre and reported that copper and iron were 15% and 11.5% bioaccessible, however only 3.7% of zinc was bioaccessible in whole cashew apple juice. In the cashew apple fibre, the bioaccessibility of Cu, Fe and Zn were found to be 4.0%, 1.2% and 2.2%, respectively. Jyothi lakshmi & Kaul, 2011 observed that the bioaccessibility of Fe, Zn and calcium were 8.7%, 24.5% and 8.1% in watermelon seeds. Bioaccessibility of Fe (8.3%), Zn (18.7%) and calcium (16.1%) was lower in defatted flour of watermelon seeds. Khouzam, Pohl, & Lobinski, 2011 reported that only 6.8%–12% iron content is bioaccessible in vegetable and fruits. It was noticed that many factors were responsible for decreasing the absorption of iron such as presence of phytate, oxalic acid, carbonate and polyphenols, low concentrations of proteins and amino acids. The bioaccessibility of Zn in cucumber and squash were quite low (11% in cucumber and 10% in squash) as compared to apple which was 5 times higher (55%) than cucumber and squash.

3.4. Bioaccessibility of minerals Minerals such as iron, zinc, magnesium, copper, phosphorus, potassium are inorganic elements that help body in growth, development and to stay healthy. The body uses minerals to perform many different functions viz. maintaining bone health, reducing muscular dystrophy, promoting bones strength, maintaining blood vessels function, promoting dental health, improving brain functions etc. After digestion, the food enters stomach and bulk of mineral absorption occurs in the small intestine and transported into the bloodstream through active and passive process by means of different transporters. It is believed that enhancement in bioaccessibility of minerals can be achieved by thermal treatment because of softening, release of protein-bound minerals of the food matrix (Hemalatha, Platel, & Srinivasan, 2007) and modification of solubility inhibitors such as oxalates, phytates, tannins and phenolic compounds (Viadel, Barbera, & Farre, 2006). The literature pertaining to bioaccessibility of minerals has been presented in Table 4. Andre et al., 2018 evaluated bioaccessibility of iron in six sweet potato clones grown in two locations viz Satipo and San Ramonin Peru following in vitro gastro-intestinal digestion method. Iron bioaccessibility for six sweet potato clones varied from 53% to 67.7% in Satipo and from 24.9% to 64.3% in San Ramon location. The average value was 61.9% and 46.5% for sweet potato clones grown in Sapito and San Ramon, respectively. Andre et al., 2015 reported that bioaccessibility of iron ranged from 63.7% to 79% in extract of 12 potato clones, with average value of 70.6%. Authors found strong positive relationship between iron concentration in boiled tuber and iron recovered after in vitro digestion, suggesting that tuber iron can be good indicators of the bioaccessible amount. Pereira et al., 2018 evaluated bioaccessibility of elements {Aluminium (Al), Barium (Ba), Copper (Cu), Iron (Fe), Manganese (Mn), Zinc (Zn)} in blackberry, raspberry, blueberry and strawberry. Bioaccessibility percentage for Al, Ba, Cu, Fe, Mn and Zn were found to be approximately 10%, 74%, 41%, 9%, 34% and 18% respectively on an average in berries. It was observed that 377

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

4. Conclusion

Burgos, G., Muñoa, L., Sosa, P., Bonierbale, M., zum Felde, T., & Díaz, C. (2013). In vitro bioaccessibility of lutein and zeaxanthin of yellow fleshed boiled potatoes. Plant Foods for Human Nutrition, 68(4), 385–390. https://doi.org/10.1007/s11130-0130381-x. Cardoso, C., Afonso, C., Lourenço, H., Costa, S., & Nunes, M. L. (2015). January 1). Bioaccessibility assessment methodologies and their consequences for the risk-benefit evaluation of food. Trends in Food Science & Technology. https://doi.org/10.1016/j. tifs.2014.08.008 Elsevier. Cilla, A., Alegría, A., De Ancos, B., Sánchez-Moreno, C., Cano, M. P., Plaza, L., et al. (2012). Bioaccessibility of tocopherols, carotenoids, and ascorbic acid from milk- and soy-based fruit beverages: Influence of food matrix and processing. Journal of Agricultural and Food Chemistry, 60(29), 7282–7290. https://doi.org/10.1021/ jf301165r. Cilla, A., Perales, S., Lagarda, M. J., Barberá, R., Clemente, G., & Farré, R. (2011). Influence of storage and in vitro gastrointestinal digestion on total antioxidant capacity of fruit beverages. Journal of Food Composition and Analysis, 24(1), 87–94. https://doi.org/10.1016/j.jfca.2010.03.029. Colle, I., Van Buggenhout, S., Lemmens, L., Van Loey, A. M., & Hendrickx, M. E. (2012). The type and quantity of lipids present during digestion influence the in-vitro bioaccessibility of lycopene from raw tomato pulp. Food Research International, 45, 250–255. Dalmau, M. E., Bornhorst, G. M., Eim, V., Rossello, C., & Simal, S. (2017). Effects of freezing, freeze drying and convective drying on in vitro gastric digestion of apples. Food Chemistry, 215, 7–16. Dalmau, M. E., Liabres, P. J., Eim, V. S., Rossello, C., & Simal, S. (2019). Influence of freezing on the bioaccessibility of beetroot (Beta vulgaris) bioactive compounds during in vitro gastric digestion. Journal of the Science of Food and Agriculture, 99(3), 1055–1065. https://doi.org/10.1002/jsfa.9272. De Lima, A. C. S., Soares, D. J., da Silva, L. M. R., de Figueiredo, R. W., de Sousa, P. H. M., & de Abreu Menezes, E. (2014). In vitro bioaccessibility of copper, iron, zinc and antioxidant compounds of whole cashew apple juice and cashew apple fibre (Anacardium occidentale L.) following simulated gastro-intestinal digestion. Food Chemistry, 161, 142–147. https://doi.org/10.1016/J.FOODCHEM.2014.03.123. Dewanto, V., Wu, X., Adom, K. K., & Liu, R. H. (2002). Thermal processing enhances the nutritional value of tomatoes by increasing total antioxidant activity. Journal of Agricultural and Food Chemistry, 50, 3010–3014. Drevon, C. A. (1991). Absorption, transport and metabolism of vitamin E. Free Radical Research, 14(4), 229–246. https://doi.org/10.3109/10715769109088952. Duchateau, G. S. M. J. E., & Klaffke, W. (2009). Health food product composition, structure and bioavailability. In designing functional foods: Measuring and controlling food structure breakdown and nutrient absorption, Vol. 3, Springer US647–675. https://doi.org/10. 1533/9781845696603.3.647. Espín, J. C., García-Conesa, M. T., & Tomás-Barberán, F. A. (2007). Nutraceuticals: Facts and fiction. Phytochemistry. https://doi.org/10.1016/j.phytochem.2007.09.014 Pergamon. Estévez-Santiago, R., Olmedilla-Alonso, B., & Fernández-Jalao, I. (2016). Bioaccessibility of provitamin A carotenoids from fruits: Application of a standardised static in vitro digestion method. Food and Function, 7(3), 1354–1366. https://doi.org/10.1039/ c5fo01242b. Failla, M. L., Huo, T., & Thakkar, S. K. (2008). In vitro screening of relative bioaccessibility of carotenoids from foods. Asia Pacific Journal of Clinical Nutrition, 17(Suppl 1), 200–203. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/18296337. Fernández-García, E., Carvajal-Lérida, I., Jarén-Galán, M., Garrido-Fernández, J., PérezGálvez, A., & Hornero-Méndez, D. (2012). Carotenoids bioavailability from foods: From plant pigments to efficient biological activities. Food Research International. https://doi.org/10.1016/j.foodres.2011.06.007 Elsevier. Fu, J., & Cui, Y. (2013). In vitro digestion/Caco-2 cell model to estimate cadmium and lead bioaccessibility/bioavailability in two vegetables: The influence of cooking and additives. Food and Chemical Toxicology, 59, 215–221. https://doi.org/10.1016/j.fct. 2013.06.014. Gawlik-Dziki, U. (2012). Changes in the antioxidant activities of vegetables as a consequence of interactions between active compounds. Journal of Functional Food, 4, 872–882. Gil-Izquierdo, A., Gil, M. I., Ferreres, F., & Tomas-Barberan, F. A. (2001). In vitro availability of flavonoids and other phenolics in orange juice. Journal of Agricultural and Food Chemistry, 49(2), 1035–1041. https://doi.org/10.1021/jf0000528. Gil-Izquierdo, A., Zafrilla, P., & Tomás-Barberán, F. A. (2002). An in vitro method to simulate phenolic compound release from the food matrix in the gastrointestinal tract. European Food Research and Technology, 214(2), 155–159. https://doi.org/10. 1007/s00217-001-0428-3. González-Gallego, J., García-Mediavilla, M. V., Sánchez-Campos, S., & Tuñó, M. J. (2010). Fruit polyphenols, immunity and inflammation. British Journal of Nutrition. https:// doi.org/10.1017/S0007114510003910 Cambridge University Press. Granado-Lorencio, F., Olmedilla-Alonso, B., Herrero-Barbudo, C., Pérez-Sacristán, B., Blanco-Navarro, I., & Blázquez-García, S. (2007). Comparative in vitro bioaccessibility of carotenoids from relevant contributors to carotenoid intake. Journal of Agricultural and Food Chemistry, 55(15), 6387–6394. https://doi.org/10.1021/ jf070301t. Harrison, F. E., & May, J. M. (2009). March 15). Vitamin C function in the brain: Vital role of the ascorbate transporter SVCT2. Free Radical Biology and Medicine. https://doi. org/10.1016/j.freeradbiomed.2008.12.018 Pergamon. Hedrén, E., Diaz, V., & Svanberg, U. (2002). Estimation of carotenoid accessibility from carrots determined by an in vitro digestion method. European Journal of Clinical Nutrition, 56(5), 425–430. https://doi.org/10.1038/sj.ejcn.1601329. Hemalatha, S., Platel, K., & Srinivasan, K. (2007). Zinc and iron contents and their bioaccessibility in cereals and pulses consumed in India. Food Chemistry, 102(4),

Domestic cooking significantly affects the nutritive value of fruits and vegetables due to various physical, chemical and enzymatic modifications. Higher bioaccessibility of polyphenols and carotenoids are obtained during cooking due to softening of cell wall, cell wall rupture and release of bound phytonutrients. Processing techniques such as pasteurization, thermal heating, dehydration, drying and frying has significant positive effect on bioaccessibility of many antioxidants. Freezing showed no clear trend. Bioaccessibility of phytonutrients enhanced further by addition of oil, fat and certain enzymes. Although studies on bioaccessibility of phytonutrients have already been done, studies related to structural changes during cooking, relationship with food matrix and its effect on bioaccessibility of phytonutrients should be focussed in future. Acknowledgements The research was supported by the Science and Engineering Research Board (Department of Science and Technology) funding agency. References Actis-Goretta, L., Lévèques, A., Rein, M., Teml, A., Schäfer, C., Hofmann, U., et al. (2013). Intestinal absorption, metabolism, and excretion of (-)-epicatechin in healthy humans assessed by using an intestinal perfusion technique. American Journal of Clinical Nutrition, 98(4), 924–933. https://doi.org/10.3945/ajcn.113.065789. Al-Yafeai, A., & Böhm, V. (2018). In vitro bioaccessibility of carotenoids and VitaminE in rosehip products and tomato paste as affected by pectin contents and food processing. Journal of Agricultural and Food Chemistry, 66(15), 3801–3809. https://doi.org/10. 1021/acs.jafc.7b05855. Andre, C. M., Burgo, G., Ziebel, J., Guignard, C., Hausmana, J. F., & Felde, T. (2018). In vitro iron bioaccessibility and uptake from orange-fleshed sweet potato (Ipomoea batatas (L.) Lam.) clones grown in Peru. Journal of Food Composition and Analysis, 68, 79–86. https://doi.org/10.1016/j.jfca.2017.07.035. Andre, C. M., Evers, D., Ziebel, J., Guignard, C., Hausman, J. F., Bonierbale, M., et al. (2015). In vitro bioaccessibility and bioavailability of iron from potatoes with varying vitamin C, carotenoid, and phenolic concentrations. Journal of Agricultural and Food Chemistry, 63(41), 9012–9021. https://doi.org/10.1021/acs.jafc.5b02904. Pérez-Vicente, A., Gil-Izquierdo, A., & García-Viguera, C. (2002). Vitro gastrointestinal digestion study of pomegranate juice phenolic compounds, anthocyanins, and vitamin C. https://doi.org/10.1021/JF0113833. Aschoff, J. K., Kaufmann, S., Kalkan, O., Neidhart, S., Carle, R., & Schweiggert, R. M. (2015). In vitro bioaccessibility of carotenoids, flavonoids, and vitamin C from differently processed oranges and orange juices [ Citrus sinensis (L.) osbeck]. Journal of Agricultural and Food Chemistry, 63(2), 578–587. https://doi.org/10.1021/jf505297t. Bengtsson, A., Alminger, M. L., & Svanberg, U. (2009). In vitro bioaccessibility of βcarotene from heat-processed orange-fleshed sweet potato. Journal of Agricultural and Food Chemistry, 57(20), 9693–9898. https://doi.org/10.1021/jf901692r. Berki, M., Daood, H. G., & Helyes, L. (2014). The influence of the water supply on the bioactive compounds of different tomato varieties. Acta Alimentaria, 43(Suppl), 21–28. https://doi.org/10.1556/AAlim.43.2014.Suppl.4 2014. Bermudez-Soto, M. J., Tomas-Barberan, F. A., & Garcia-Conesa, M. J. (2007). Stability of polyphenols in chokeberry (Aronia melanocarpa) subjected to in vitro gastric and pancreatic digestion. Food Chemistry, 102, 865–870. https://doi.org/10.1016/j. foodchem.2006.06.025. Bohn, T., Mcdougall, G. J., Alegría, A., Alminger, M., Arrigoni, E., Aura, A. M., et al. (2015 July 1). Mind the gap-deficits in our knowledge of aspects impacting the bioavailability of phytochemicals and their metabolites-a position paper focusing on carotenoids and polyphenols. Molecular Nutrition & Food Research. https://doi.org/ 10.1002/mnfr.201400745 John Wiley & Sons, Ltd. Borel, P., Preveraud, D., & Desmarchelier, C. (2013). Bioavailability of vitamin E in humans: An update. Nutrition Reviews, 71(6), 319–331. https://doi.org/10.1111/nure. 12026. Bouayed, J., Deußer, H., Hoffmann, L., & Bohn, T. (2012). Bioaccessible and dialysable polyphenols in selected apple varieties following in vitro digestion vs. their native patterns. Food Chemistry, 131(4), 1466–1472. https://doi.org/10.1016/j.foodchem. 2011.10.030. Bouayed, J., Hoffmann, L., & Bohn, T. (2011). Total phenolics, flavonoids, anthocyanins and antioxidant activity following simulated gastro-intestinal digestion and dialysis of apple varieties: Bioaccessibility and potential uptake. Food Chemistry, 128(1), 14–21. https://doi.org/10.1016/j.foodchem.2011.02.052. Brandt, S., Pewk, Z., Barna, E., Lugasi, A., & Helyes, L. (2006). Lycopene content and colour of ripening tomatoes as affected by environmental conditions. Journal of the Science of Food and Agriculture, 86, 568–572. https://doi.org/10.1002/jsfa.2390. Brown, I. L. (2004). Applications and uses of resistant starch. Journal of AOAC International, 87(3), 727–732.

378

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

simulated human digestion. Nutrition, 29(1), 338–344. Martinez, M. N., & Amidon, G. L. (2002). A mechanistic approach to understanding the factors affecting drug absorption: A review of fundamentals. The Journal of Clinical Pharmacology, 42(6), 620–643. https://doi.org/10.1177/00970002042006005. Metzger, B. T., & Barnes, D. M. (2009). Polyacetylene diversity and bioactivity in orange market and locally grown colored carrots (daucus carota L.). Journal of Agricultural and Food Chemistry, 57, 11134–11139. https://doi.org/10.1021/jf9025663. Miranda, L., Deuber, H., & Evers, D. (2013). The impact of in vitro digestion on bioaccessibility of polyphenols from potatoes and sweet potatoes and their influence on iron absorption by human intestinal cells. Food & Function, 4, 1595–1601. https:// doi.org/10.1039/c3fo60194c. Moelants, K. R. N., Lemmens, L., Vandebroeck, M., Van Buggenhout, S., Van Loey, A. M., & Hendrickx, M. E. (2012). Relation between particle size and carotenoid bioaccessibility in carrot- and tomato-derived suspensions. Journal of Agricultural and Food Chemistry, 60(48), 11995–12003. https://doi.org/10.1021/jf303502h. Nagy, Z., Daood, H., Ambrozy, Z., & Helyes, L. (2015). Determination of polyphenols, capsaicinoids and vitamin C in new hybrids of chili peppers. Journal of Analytical Methods in Chemistry, 1–10. https://doi.org/10.1155/2015/102125. Oghbaei, M., & Prakash, J. (2013). Effects of processing and digestive enzymes on retention, bioaccessibility and antioxidant activity of bioactive components in food mixes based on legumes and green leaves. Food Bioscience, 4, 21–30. https://doi.org/ 10.1016/J.FBIO.2013.08.001. Ombodi (2014). Carotenoid and tocopherol composition of an orange-colored carrot as affected by water supply. Horticulture Science, 49(6), 729–733. O'Callaghan, Y., & O'Brien, N. (2010). Bioaccessibility, cellular uptake and transepithelial transport of α-tocopherol and retinol from a range of supplemented foodstuffs assessed using the caco-2 cell model. International Journal of Food Science and Technology, 45(7), 1436–1442. https://doi.org/10.1111/j.1365-2621.2010.02285.x. O'Sullivan, L., Jiwan, M. A., Daly, T., O'Brien, N. M., & Aherne, S. A. (2010). Bioaccessibility, uptake, and transport of carotenoids from peppers (capsicum spp.) using the coupled in vitro digestion and human intestinal caco-2 cell model. Journal of Agricultural and Food Chemistry, 58(9), 5374–5379. https://doi.org/10.1021/ jf100413m. Padayatty, S. J., & Levine, M. (2001). New insights into the physiology and pharmacology of vitamin C. Canadian Medical Association Journal: Canadian Medical Association Journal = Journal de l’Association Medicale Canadienne, 164(3), 353–355. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11232136. Palermo, M., Pellegrini, N., & Fogliano, V. (2014). The effect of cooking on the phytochemical content of vegetables. Journal of the Science of Food and Agriculture, 94(6), 1057–1070. https://doi.org/10.1002/jsfa.6478. Parker, R. S. (1996). Absorption, metabolism, and transport of carotenoids. The FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 10(5), 542–551. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/ 8621054. Pek, Z. (2012). Yield and phytochemical compounds of broccoli as affected by temperature, irrigation, and foliar sulfur supplementation. Horticulture Science, 46(11), 1646–1652. Pek, Z., Helyes, L., & Lugasi, A. (2010). Color changes and antioxidant content of vine and postharvestripened tomato fruits. Horticulture Science, 45(3), 466–468. Pereira, C. C., do Nascimento da Silva, E., de Souza, A. O., Vieira, M. A., Ribeiro, A. S., & Cadore, S. (2018). Evaluation of the bioaccessibility of minerals from blackberries, raspberries, blueberries and strawberries. Journal of Food Composition and Analysis, 68, 73–78. https://doi.org/10.1016/J.JFCA.2016.12.001. Pinto, M., Robineleon, S., Appay, M. D., Kedinger, M., Triadou, N., Dussaulx, E., et al. (1983). Enterocyte-like differentiation and polarization of the human-colon carcinoma cell-line Caco-2 in culture. Retrieved from https://www.scienceopen.com/ document?vid=07f3fdcd-c23c-47d4-ad63-105346ef5453. Porter, C. J. H., Trevaskis, N. L., & Charman, W. N. (2007). Lipids and lipid-based formulations: Optimizing the oral delivery of lipophilic drugs. Nature Reviews Drug Discovery, 6(3), 231–248. https://doi.org/10.1038/nrd2197. Pouton, C. W., & Porter, C. J. H. (2008). Formulation of lipid-based delivery systems for oral administration: Materials, methods and strategies. Advanced Drug Delivery Reviews, 60(6), 625–637. https://doi.org/10.1016/j.addr.2007.10.010. Prakash, J., & Oghbaei, M. (2015). Antioxidant components and their in vitro bioaccessibility in processed and stored chickpea and amaranth greens mix. Hrvatski Časopis Za Prehrambenu Tehnologiju, Biotehnologiju i Nutricionizam, 10(1–2), 44–50. Reboul, E., Richelle, M., Perrot, E., Desmoulins-Malezet, C., Pirisi, V., & Borel, P. (2006). Bioaccessibility of carotenoids and vitamin E from their main dietary sources. Journal of Agricultural and Food Chemistry, 54(23), 8749–8755. https://doi.org/10.1021/ jf061818s. Rimbach, G., Pallauf, J., Moehring, J., Kraemer, K., & Minihane, A. M. (2008). Effect of dietary phytate and microbial phytase on mineral and trace element bioavailability: A literature review. Current Topics in Nutraceutical Research, 6(3), 131–144. Sandberg, A.-S. (2005). Methods and options for in vitro dialyzability; benefits and limitations. International Journal for Vitamin and Nutrition Research, 75(6), 395–404. https://doi.org/10.1024/0300-9831.75.6.395. Scalbert, A., & Williamson, G. (2000). Dietary intake and bioavailability of polyphenols. Journal of Nutrition, 130(8), 2073S–2085S. https://doi.org/10.1093/jn/130.8.2073S. Schlueter, A. K., & Johnston, C. S. (2011). Vitamin C: Overview and update. Journal of Evidence-Based Complementary & Alternative Medicine, 16(1), 49–57. https://doi.org/ 10.1177/1533210110392951. Scholz, & Williamson (2007). Interactions affecting the bioavailability of dietary polyphenols in vivo. International Journal for Vitamin and Nutrition Research, 77(3), 224–235. https://doi.org/10.1024/0300-9831.77.3.224. Shim, S. M. (2012). Changes in profiling of phenolic compounds, antioxidative effect and total phenolic content in Smilax China under in vitro physiological condition. Journal

1328–1336. https://doi.org/10.1016/j.foodchem.2006.07.015. van het Hof, K. H., West, C. E., Weststrate, J. A., & Hautvast, J. G. A. J. (2000). Dietary factors that affect the bioavailability of carotenoids. Journal of Nutrition, 130(3), 503–506. https://doi.org/10.1093/jn/130.3.503. Hornero-Méndez, D., & Mínguez-Mosquera, M. I. (2007). Bioaccessibility of carotenes from carrots: Effect of cooking and addition of oil. Innovative Food Science & Emerging Technologies, 8(3), 407–412. https://doi.org/10.1016/j.ifset.2007.03.014. Hur, S. J., Lim, B. O., Decker, E. A., & McClements, D. J. (2011). In vitro human digestion models for food applications. Food Chemistry. https://doi.org/10.1016/j.foodchem. 2010.08.036 Elsevier. Jeffery, J. L., Turner, N. D., & King, S. R. (2012). Carotenoid bioaccessibility from nine raw carotenoid-storing fruits and vegetables using an in vitro model. Journal of the Science of Food and Agriculture, 92(13), 2603–2610. https://doi.org/10.1002/jsfa. 5768. Jeney-Nagymate, E., & Fodor, P. (2008). The stability of vitamin C in different beverages. British Food Journal, 110(3), 296–309. https://doi.org/10.1108/ 00070700810858709. Juániz, I., Ludwig, I. A., Bresciani, L., Dall'Asta, M., Mena, P., Del Rio, D., et al. (2017). Bioaccessibility of (poly)phenolic compounds of raw and cooked cardoon (Cynara cardunculus L.) after simulated gastrointestinal digestion and fermentation by human colonic microbiota. Journal of Functional Foods, 32, 195–207. https://doi.org/10. 1016/j.jff.2017.02.033. Jyothi lakshmi, A., & Kaul, P. (2011). Nutritional potential, bioaccessibility of minerals and functionality of watermelon (Citrullus vulgaris) seeds. Lebensmittel-Wissenschaft und -Technologie- Food Science and Technology, 44(8), 1821–1826. https://doi.org/10. 1016/J.LWT.2011.04.001. Kalantzi, L., Goumas, K., Kalioras, V., Abrahamsson, B., Dressman, J. B., & Reppas, C. (2006). Characterization of the human upper gastrointestinal contents under conditions simulating bioavailability/bioequivalence studies. Pharmaceutical Research, 23(1), 165–176. https://doi.org/10.1007/s11095-005-8476-1. Kamiloglu, S. (2019). Effect of different freezing methods on the bioaccessibility of strawberry polyphenols. International Journal of Food Science and Technology, 54, 2652–2660. Kamiloglu, S., & Capanoglu, E. (2013). Investigating the in vitro bioaccessibility of polyphenols in fresh and sun-dried figs (Ficus carica L.). International Journal of Food Science and Technology, 48(12), 2621–2629. https://doi.org/10.1111/ijfs.12258. Kamiloglu, S., Pasli, A. A., Ozcelik, B., Van Camp, J., & Capanoglu, E. (2015). Influence of different processing and storage conditions on in vitro bioaccessibility of polyphenols in black carrot jams and marmalades. Food Chemistry, 186, 74–82. https://doi.org/ 10.1016/j.foodchem.2014.12.046. Karakaya, S., & Yilmaz, N. (2007). Lycopene content and antioxidant activity of fresh and processed tomatoes and in vitro bioavailability of lycopene. Journal of the Science of Food and Agriculture, 87, 2342–2347. Kaulmann, A., Andre, C. M., Schneider, Y., Hoffmann, L., & Bohn, T. (2016). Carotenoid and polyphenol bioaccessibility and cellular uptake from plum and cabbage varieties. Food Chemistry, 197, 325–332. https://doi.org/10.1016/j.foodchem.2015.10.049 pt A. Keogh, J. B., McInerney, J., & Clifton, P. M. (2007). The effect of milk protein on the bioavailability of cocoa polyphenols. Journal of Food Science, 72(3), S230–S233. https://doi.org/10.1111/j.1750-3841.2007.00314.x. Khouzam, R. B., Pohl, P., & Lobinski, R. (2011). Bioaccessibility of essential elements from white cheese, bread, fruit and vegetables. Talanta, 86(1), 425–428. https://doi. org/10.1016/j.talanta.2011.08.049. Kiela, P. R., & Ghishan, F. K. (2016). Physiology of intestinal absorption and secretion. Best practice and research: Clinical gastroenterology. Baillière Tindallhttps://doi.org/10. 1016/j.bpg.2016.02.007 April 1). Koh, S. H., & Loh, S. P. (2018). In vitro bioaccessibility of â-carotene in pumpkin and butternut squash subjected to different cooking methods. International Food Research Journal, 25(1), 188–195. Koncsek, A., Daood, H. G., & Helyes, L. (2016). Kinetics of carotenoid degradation in spice paprika as affected by storage temperature and seed addition. Acta Alimentaria, 45(4), 459–468. https://doi.org/10.1556/066.2016.45.4.1. Koncsek, A., Kruppai, L., Helyes, L., Bori, Z., & Daood, H. G. (2015). Storage stability of carotenoids in paprika from conventional, organic and frost-damaged spice red peppers as influenced by illumination and antioxidant supplementation. Journal of Food Processing and Preservation, 40, 453–462. https://doi.org/10.1111/jfpp.12623. Kulkarni, S. D., Acharya, R., Rajurkar, N. S., & Reddy, A. V. R. (2007). Evaluation of bioaccessibility of some essential elements from wheatgrass (Triticum aestivum L.) by in vitro digestion method. Food Chemistry, 103(2), 681–688. https://doi.org/10. 1016/j.foodchem.2006.07.057. Lemmens, L., Van Buggenhout, S., Oey, I., Van Loey, A., & Hendrickx, M. (2009). Towards a better understanding of the relationship between the β-carotene in vitro bio-accessibility and pectin structural changes: A case study on carrots. Food Research International, 42(9), 1323–1330. https://doi.org/10.1016/J.FOODRES.2009.04.006. Liang, L., Wu, X., Zhao, T., Zhao, J., Li, F., Zou, Y., et al. (2012). In vitro bioaccessibility and antioxidant activity of anthocyanins from mulberry (Morus atropurpurea Roxb.) following simulated gastro-intestinal digestion. Food Research International, 46(1), 76–82. https://doi.org/10.1016/J.FOODRES.2011.11.024. Malo, C., & Wilson, J. X. (2000). Glucose modulates vitamin C transport in adult human small intestinal brush border membrane vesicles. Journal of Nutrition, 130(1), 63–69. https://doi.org/10.1093/jn/130.1.63. Manach, C., Scalbert, A., Morand, C., Rémésy, C., & Jiménez, L. (2004). Polyphenols: Food sources and bioavailability. American Journal of Clinical Nutrition, 79(5), 727–747. https://doi.org/10.1093/ajcn/79.5.727. Mandalari, G., Bisignano, C., Filocamo, A., Chessa, S., Saro, M., Torre, G., et al. (2013). Bioaccessibility of pistachio polyphenols, xanthophylls, and tocopherols during

379

Trends in Food Science & Technology 97 (2020) 366–380

N. Thakur, et al.

Viadel, B., Barberá, R., & Farré, R. (2006). Uptake and retention of calcium, iron, and zinc from raw legumes and the effect of cooking on lentils in Caco-2 cells. Nutrition Research, 26(11), 591–596. https://doi.org/10.1016/J.NUTRES.2006.09.016. Werner, S., & Bohm, V. (2011). Bioaccessibility of carotenoids and vitamin E from pasta:evaluation of an in vitro digestion model. Journal of Agricultural and Food Chemistry, 59(4), 1163–1170. Wienk, K. J. H., Marx, J. J. M., & Beynen, A. C. (1999). The concept of iron bioavailability and its assessment. European Journal of Nutrition, 38(2), 51–75. https://doi.org/10. 1007/s003940050046. Wildman, R. E. C. (2007). Handbook of nutraceuticals and functional foods. CRC/Taylor & Francis. Retrieved from https://www.crcpress.com/Handbook-of-Nutraceuticalsand-Functional-Foods/author/p/book/9780849364099. Wood, R. J. (2005). Bioavailability: Definition, general aspects and fortificants. Encyclopedia of human nutrition (2nd ed.). Oxford: Elsevier Ltd. You, L., Zhao, M., Regenstein, J. M., & Ren, J. (2010). Changes in the antioxidant activity of loach (Misgurnus anguillicaudatus) protein hydrolysates during a simulated gastrointestinal digestion. Food Chemistry, 120(3), 810–816. https://doi.org/10.1016/J. FOODCHEM.2009.11.018. Zeng, Z., Liu, C., Luo, S., Chen, J., & Gong, E. (2016). The profile and bioaccessibility of phenolic compounds in cereals influenced by improved extrusion cooking treatment. PloS One, 11(8), e0161086. https://doi.org/10.1371/journal.pone.0161086.

of Food Biochemistry, 36 748–55. Svelander, C. A., Tiback, E. A., Ahane, L. M., Langton, M. I. B. C., Svanberg, U. S. O., & Alminger, M. A. G. (2010). Processing of tomato: Impact on in vitro bioaccessibility of lycopene and textural properties. Journal of the Science of Food and Agriculture, 90, 1665–1672. Tagliazucchi, D., Verzelloni, E., Bertolini, D., & Conte, A. (2010). In vitro bio-accessibility and antioxidant activity of grape polyphenols. Food Chemistry, 120(2), 599–606. https://doi.org/10.1016/J.FOODCHEM.2009.10.030. Ting, Y., Zhao, Q., Xia, C., & Huang, Q. (2015). Using in vitro and in vivo models to evaluate the oral bioavailability of nutraceuticals. Journal of Agricultural and Food Chemistry, 63(5), 1332–1338. https://doi.org/10.1021/jf5047464. Tomas, M., Sagdic, O., Catalkaya, G., Kahveci, D., & Capanoglu, E. (2019). Effects of cooking and extra virgin olive oil addition on bioaccessibility of carotenes in tomato sauce. Turkish Journal of Agriculture and Forestry, 43, 478–484. https://doi.org/10. 3906/tar-1801-127. Trevaskis, N. L., & Charman, W. N. (2008). Lipid-based delivery systems and intestinal lymphatic drug transport: A mechanistic update. Advanced Drug Delivery Reviews, 60(6), 702–716. https://doi.org/10.1016/J.ADDR.2007.09.007. Vallejo, F., Gil-Izquierdo, A., Pérez-Vicente, A., & García-Viguera, C. (2003). In vitro gastrointestinal digestion study of broccoli inflorescence phenolic compounds, glucosinolates, and vitamin C. https://doi.org/10.1021/JF0305128.

380