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International Journal of and Science 17 (2019) 100154

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International Journal of Gastronomy and Food Science

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Sauces: An undiscovered healthy complement in Mexican T Alicia Paulina Cárdenas-Castroa, Guadalupe del Carmen Perales-Vázqueza, Laura A. De la Rosab, Víctor Manuel Zamora-Gasgaa, Víctor Manuel Ruiz-Valdiviezoc, Emilio Alvarez-Parrillab, ∗ Sonia Guadalupe Sáyago-Ayerdia, a Tecnológico Nacional de México/Instituto Tecnológico de Tepic, Av. Tecnológico No. 2595, Col. Lagos del Country, CP 63175, Tepic, Nayarit, b Universidad Autónoma de Ciudad Juárez, Instituto de Ciencias Biomédicas, Departamento de Ciencias Químico-Biológicas, Anillo Envolvente del PRONAF y Estocolmo s/ n, Ciudad Juárez, , CP 32310, Mexico c Tecnológico Nacional de México/Instituto Tecnológico de Tuxtla Gutiérrez, Departamento de Ingeniería Química y Bioquímica, Laboratory of Molecular Biology, Carretera Panamericana km 1080, CP 29050, Tuxtla Gutiérrez, , Mexico

ARTICLE INFO ABSTRACT

Keywords: Gastronomic differences between the countries around the world were largely defined due to the di- Mexican versification of the use of and condiments during the European colonization of America, Asia and Africa. Hence, gastronomy tells the story of thousands of generations in a country and contains the culture of the population in multiple combinations of , types of or spices that depends on the geographical Hot pepper conditions. Particularly, the Mexican diet has been studied in a limited way but the findings of its consumption could ameliorate health status. Pre-Hispanic cultures developed many different dishes that still consumed Bioactive compounds nowadays. Surprisingly, Mexican population is developing acculturation, which includes lower intake of their most healthy , and so on, one of them are Mexican sauces, a mixture with hot pepper, tomato, tomato, , garlic, coriander and salt. It should be noted that the most common ingredients of Mexican sauces have been studied isolated but not combined, as they are frequently consumed. In addition, the potential health effects of the bioactive compounds (BC) that could be found in this staple Mexican food still undiscovered. In this review, the main BC present in common Mexican sauces ingredients and the effects of processing in the content of these compounds are stated in this review.

1. Introduction traditional and increased intake of added , high-fat diets, and processing foods. Data has demonstrated a correlational relation- In 2010, Mexican food was the first cuisine of a country accepted by ship between consumption of fat and refined sugars with obesity, dia- the Intergovernmental Committee for the Safeguarding of the betes and other chronic diseases (Flores et al., 2010; Garcia et al., Intangible Cultural Heritage of UNESCO in the Representative List of 2012), which are some of the main diseases among the Mexican po- the Intangible Cultural Heritage of Humanity (Gálvez and Salinas, pulation (ENSANUT, 2016). 2015). The studies targeted to evaluate the health benefits of the con- Gastronomic differences between countries cuisines around the sumption of Mexican diet are limited but they conclude that the con- world were largely defined due to the diversification of the use of spices sumption of this diet (including its representative culinary dishes, in- and condiments during the European colonization of America, Asia, and gredients, endemic , and vegetables) could exert important Africa in the 15th-17th Centuries (García-Casal et al., 2016). Indeed, benefits to ameliorate the metabolic disorders presented during chronic there are a lot of discrepancies about the origins of crop plants due to diseases (Avila-Nava et al., 2017; Santiago-Torres et al., 2015). the globalization that began during the European colonization (Mann, Nevertheless, Mexico has been going through nutritional transition 2011). The mixture of vegetables, fruits, oil, , fish, , spices, with important changes in food consumption, developing acculturation and condiments is called “”, and it is used to flavor foods and to the western diets (Zamora-Gasga et al., 2017), and consequently, enhance their aroma, appearance, and texture. Then, sauces could be only 14% of the Mexican population has healthy nutritional habits, applied to different foods, from pancakes, egg dishes to vegetables while the remaining 86% presents nutritional problems (del Castillo, dishes and meats (Nachay, 2011). The wide variety of spices, condi- 2013). This has been associated with lower intake of their most healthy ments, as well as, all the elements that contain a sauce, results in the

∗ Corresponding author. E-mail address: [email protected] (S.G. Sáyago-Ayerdi). https://doi.org/10.1016/j.ijgfs.2019.100154 Received 1 February 2019; Received in revised form 10 April 2019; Accepted 12 April 2019 Available online 16 April 2019 1878-450X/ © 2019 Elsevier B.V. All rights reserved. A.P. Cárdenas-Castro, et al. International Journal of Gastronomy and Food Science 17 (2019) 100154 formulation of a large number of representative sauces for each this sense, over the years, she has learned that a sauce prepared in the country. Chinese, American, Japanese, Indonesian, and Mexican cui- “” gives off a more pleasant flavor than those made in a sines were among the top 10 of producers and consumers of sauces blender, due to the perfect integration of the ingredients and the flavor during the 2011–2013 period. Ketchup, , , soy of past grindings impregnated in the “molcajete” (“molcajete” comes sauce, fish sauce, and barbecue sauce are some of the most worldwide from the Nahuátl words “mollicaxtli” and “temolcaxitl”, which mean known sauces (García-Casal et al., 2016). Particularly, the Mexican “stone bowl for sauce”). As the chemical engineer , Jaime Ortega said: sauces were born when one of the most representative and consumed “the sauces have an unparalleled flavor when they are “molcajeteadas”.In vegetables in Mexico, hot pepper ( annuum L.), was mixed with this mortar used since the pre-Hispanic period for the grinding of grains and tomato (Solanum lycopersicum L.) or husk tomato (Physalis ixocarpa spices, the ingredients release all their essences and oils, mixing with each Brot. ex. Horm), “Guaje” (Leucaena leucocephala (Lam) de Wit), and other, compare to the blender that only grinds tomato without incorporate its some other aromatic endemic plants like “Epazote” (Dysphania am- ”. Although the use of “molcajete” is currently decreasing, it is still brosioides L.), “Pipicha” (Porophyllum linaria (Cay) DC) and “Pápalo” produced in volcanic or basalt stone, rounding the stone with percus- ( (Jacq.) Cass.) (Flores y Escalante, 2004). When sion, and always polishing it with a hammer and chisel (Moreno Rojas, the sauces contain hot pepper, they are known around the world as “hot 2013). Therefore, hot pepper, among is a symbol of identity sauces” (because not only Mexican sauces contain hot pepper), and they and an indispensable part of their family . In this sense: “Sauces are mainly consumed in Asia, US, and Mexico. In contrast, hot sauces and hot pepper are not simply dishes, they are part of Mexican identity, and (as part of traditional foods) are less consumed in most European the second thing is that for sure, sauce runs through Mexican's veins” countries. Therefore, food preferences among individuals are most in- (Montes, 2016). fluenced by the life history of specific ethnic groups, culinary cultures, Mexican sauces are prepared, mainly, with the following in- and traditional recipes. That is why, cross-cultural studies are important gredients: hot pepper, tomato, onion, garlic, and spices. Indeed, a to know the food preferences of consumers from different countries common and general formulation of a Mexican sauce includes: 85% (Rozin and Schiller, 1980). Interestingly, a cross-cultural study was tomato, 5 and 4% of hot pepper and onion, respectively, 2% salt and 1% conducted in order to understand the acceptance levels of hot sauces garlic (Escobedo-Avellaneda et al., 2011; Martínez-Padilla and Rivera- among different culinary cultures. In this study, Kim et al. (2018) found Vargas, 2005), but that formulation and recipes of sauces preparation that the US individuals did not like hot sauces with sweet and weak varies between the regions of Mexico (Muñoz Zurita, 2008). Also, the spiciness, whereas the Korean and Danish subjects disliked hot sauces quantities of ingredients vary since their availability in each region when they were too spicy and not sweet enough. Consequently, the responds to climatic and geographical conditions. Mexican sauce is authors concluded that the consumption of hot sauces with specific used to accompany popular and typical Mexican culinary dishes like food dishes is culture-dependent. Nowadays, Mexican sauces are char- “”, “”, “tostadas”, roast and . The most re- acterized by the mixture of tomato (Solanum lycopersicum L.) or husk presentative Mexican sauces, popularly called as “basics” and “indis- tomato (Physalis ixocarpa Brot. ex. Horm) or “” (Physalis phi- pensables” are “ roja” (red sauce), “” (Mexican sauce), ladelphica Lam.), (which are the two Physalis varieties most consumed and “” (green sauce) (Fig. 1)(Tatum, 2014; Torres Siller, in Mexico) (Elizalde-González and Hernández-Ogarcía, 2007), hot 2017). pepper (Capsicum annuum L.), garlic (Allium sativum L.), onion (Allium In that sense, red sauce is made with cooked tomato, “Chile De cepa L.), coriander (Coriandrum sativum L.) and other spices or condi- Árbol” (Capsicum annuum ‘De árbol’) (dried red in maturity stage ‘tree’ ments. Also, they are considered a timeless and unifying element that hot pepper), garlic, onion, and salt. These ingredients are toasted in a relates to the story of a miscegenation culture (Torres Siller, 2017). “” (flat pan) and homogenized in the “molcajete” or in a blender. Indeed, gastronomy tells the past and present of thousands of genera- The green sauce is made with raw or cooked husk tomato or tomatillo, tions; it contains the culture of the people. Then, Mexican gastronomy ‘Serrano’ hot peppers, onion, garlic, salt, and coriander. These in- reflects its wonderful essence, traditions, colors,and spirit (Fernández, gredients can be toasted in a “comal” or could be cooked in water and 1985). then, ground in the “molcajete”. Finally, “pico de gallo” is a sauce made with raw tomato, ‘Serrano’ hot peppers (which are the most used in 2. Mexican sauces and their predominant ingredients green and Mexican sauce preparation), onion and coriander cut into cubes. Garlic, salt, lemon , and can be added. This parti- For more than eight centuries, hot pepper has been consumed in cularly sauce is well known as “Mexican sauce” due to its colors, (green Mexico as food and as a condiment (Contreras-Padilla and Yahia, from hot peppers and coriander, white from onion and red from to- 1998). In this sense, “Hot pepper (a word derived from the Náhuatl, “chili”, mato), which refer to the colors of the Mexican flag (Muñoz Zurita, in Spanish, the translation of hot pepper is “chile”) is an excellent re- 2008). presentative of Mexican food. Which is one of the most consumed around the The most important ingredient of a Mexican sauce is hot pepper world and it has the greatest variety due to its different climatic and geo- (Capsicum species), which as a reported consumption of 20 g/person/ graphical characteristics that allow along the whole country can be culti- day in Mexico (Ornelas-Paz et al., 2009). Tomato is named in Mexico vated the hot peppers species”, mentioned by the chemical engineer Jaime “jitomate” which derives from the Náhuatl name “jitomatl”. And for this Ortega Zaldivar, who organized in 2013 the first hot pepper festival, reason, it has been suggested that Mexico was the land where the to- sauces and “” in the Community Center Ex Convent of Cul- mato was domesticated, and later on introduced to Europe (Jenkins, huacán of the Mexican National Institute of Anthropology and History 1948; Blanca et al., 2012). Nowadays, in Europe and the US, tomatoes (Moreno Rojas, 2013). Engineer Ortega noted that the consumption of are the second most consumed cultivar and they are used in the food this product is so recurrent in Mexico because when hot pepper is industry for the production of sauces, , and purees (Navarro- consumed, dopamine is released, a hormone involved in some culinary González et al., 2011). pleasure sensations, so it is easy to understand why 90% of the Mexican Another very important in Mexican diet, very popular dishes contain it. However, Mexico has a wide variety of hot peppers ingredient in Mexican sauces, mainly due to its unique and slightly with more than 50 different species from which 20 of them are the most acidic flavor (due to citric acid content) is the husk tomato (Physalis used in . Moreover, for Doña Zaldivar Fig- ixocarpa Brot. ex. Horm), a small green tomato with husk (Bock et al., ueroa, an 87-year-old woman, the best way that a Mexican would re- 1995; McGorrin and Gimelfarb, 1998). Around 78% of the 90 husk ceive their guests is to offer them “A tasty “molcajeteada” (made in the tomato species Physalis L. (Solanaceae) are cultivated in Mexico “molcajete”, a traditional stone mortar from , widely used in (Valdivia-Mares et al., 2016). Husk tomato or “tomatillo” (Physalis phi- Mexico) sauce, which will delight the palate and encourage the ”.In ladelphica Lam.) is the major ingredient of fresh and cooked green

2 A.P. Cárdenas-Castro, et al. International Journal of Gastronomy and Food Science 17 (2019) 100154

Fig. 1. Sauces from Mexico. a) Red sauce with cooked tomato, b) Green sauce with cooked husk tomato, c) Mexican sauce with raw tomato, onion and hot pepper (‘Serrano’ variety), d) Green sauce with raw husk tomato.

Mexican sauces (McGorrin and Gimelfarb, 1998). At least 6 recipes of than protein (3.67–33.06 g/100 g). Interestingly, total dietary fiber Mexican sauces contain husk tomato as the main ingredient (Montes (TDF) is one of the main carbohydrates that the main ingredients of and Aguirre, 1994). Mexican sauces contain. The highest content of TDF has been reported Certain plants were introduced to the pre-Hispanic Mexican cuisine for ‘Serrano’ hot pepper (3.7 g/100 g fresh product) but studies have by the European colonizers, and nowadays are essential ingredients in shown that tomato and husk tomato are also good sources of TDF. The most of the Mexican gastronomy. One of these cultured plants that were tomato peel fiber is the 86.15 g/100 g of TDF of the whole tomato. TDF brought to America from the Caucasus region is coriander (Coriandrum is the sum of insoluble dietary fiber (IDF) and soluble dietary fiber sativum L.). World production of coriander is tricky to estimate. Official (SDF), which the content of IDF and SIF of tomato peel is 71.82 g/100 g statistics do not restrain figures of this crop but it is estimated that the and 14.33 g/100 g, respectively (Navarro-González et al., 2011). The main producers of coriander are Russia, Ukraine, Morocco, Argentina, pectin in husk tomato has been reported between 0.41 and 1.04 g/100 g Mexico, India, and Romania (Nadeem et al., 2013). Leaves and seeds (Bock et al., 1995). Recently, Morales-Contreras et al. (2018) obtained possess different sensorial features; therefore, they are utilized in cui- pectin from husk tomato; this result could lead to applications of pectin sine for different purposes. Particularly, coriander is an important extracted from husk tomato in foods formulations. Also, are condiment or used in the Indian, Thai, and to considered an important source of fructooligosaccharides, a SDF type prepare pastes and fresh leaves are used to season many ethnic (Slimestad et al., 2007). Garlic presented the highest content of protein dishes like salads, soups , and sauces (Gil et al., 2002; Singletary, 2016). among these vegetables (Table 1), however, Orellana-Escobedo et al. In Mexican cuisine, the coriander (included leaves and stem) is essential (2013) reported that 15 commercial of dry hot peppers (‘Serrano’ to prepare the Mexican sauce’s recipes; without this ingredient, overall, variety was evaluated) constitute a good source of protein compared to green Mexican sauces are incomplete. other vegetables used in Mexican cuisine. As it is shown in Table 1, Another two main ingredients of the Mexican sauces, which are garlic and coriander possess the highest content of minerals and vita- species of the genus Allium are onion (Allium cepa L.) and garlic (Allium mins. Both have been reported high levels of phosphorus, potassium, sativum L.). These species were consumed as medicine by the ancient sulfur, and zinc (Lawson, 1996; Peter, 2004). The content of fat among Egyptians (Gorinstein et al., 2008) and their first citation is found in the the main ingredients of the Mexican sauces has been reported between Codex Ebers (1550 BCE) recipes (Lanzotti, 2006). Violet, gold or yellow 0.10 and 1.2 g/100 g fresh base. Particularly, α-linolenic acid (ALA) and white onions represent the most known and consumed varieties of was predominant in coriander leaves (Neffati and Marzouk, 2008). ALA Allium cepa L. (Prakash et al., 2007) but the white onion is the most has been studied due to its cardiovascular and anti-inflammatory effects used in the preparation of the Mexican sauces (Muñoz Zurita, 2008). (Kim et al., 2014). In this sense, scientific research on onion and garlic It is noteworthy that 39% of theexican population consume sauces began with the discovery of the anti-bacterial properties of garlic, and it from a supermarket. Then, at least, the per capita consumption of was in 1858 with Louis Pasteur. Even today, knowledge of the potential Mexican sauces (purchased in a supermarket) is 4 kg/year (Ghirardelly benefits of garlic consumption continues growing (Lanzotti, 2006). and Carranza, 2016). The nutritional composition of the main in- Overall, the biological effects of the intake of the main the ingredients gredients of Mexican sauces are shown in Table 1 ( of the Mexican sauces and vegetables are attributed to their content of Department of - USDA, 2018). Water is the main component particular compounds known as bioactive compounds (BC) and the in all the vegetables used for sauces (89–94 g/100 g). Protein content profile of BC is unique in each vegetable crop. ranged between 0.88 and 6.36 g/100 g fresh product whereas total lipid content is between 0.10 and 1.02 g/100 g fresh product. All vegetables used for sauces present low-fat content. Carbohydrates content is higher

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Table 1 Nutritional composition of raw tomato, husk tomato, coriander, garlic, hot pepper and onion.a

Nutrient Unit Tomatob Husk tomatoc Corianderd Garlice ‘Serrano’ hot pepper f Oniong

Proximate composition Water g 94.52 91.63 92.21 58.58 90.25 89.11 Energy kcal 18 32 23 149 32 40 Protein g 0.88 0.96 2.13 6.36 1.74 1.10 Total lipid (fat) g 0.20 1.02 0.52 0.50 0.44 0.10 Carbohydrate, by difference g 3.89 5.84 3.67 33.06 6.70 9.34 Total dietary fiber g 1.2 1.9 2.8 2.1 3.7 1.7 Sugars, total g 2.63 3.93 0.87 1 3.83 4.24 Minerals Calcium, Ca mg 10 7 67 181 11 23 Iron, Fe mg 0.27 0.62 1.77 1.70 0.86 0.21 Magnesium, Mg mg 11 20 26 25 22 10 Phosphorus, P mg 24 39 48 153 40 29 Potassium, K mg 237 268 521 401 305 146 Sodium, Na mg 5 1 46 17 10 4 Zinc, Zn mg 0.17 0.22 0.50 1.16 0.26 0.17 Vitamins Vitamin C, total ascorbic acid mg 13.7 11.7 27 31.2 44.9 7.4 Thiamin mg 0.037 0.044 0.067 0.200 0.054 0.046 Riboflavin mg 0.019 0.035 0.162 0.110 0.081 0.027 Niacin mg 0.594 1.850 1.114 0.700 1.537 0.116 Vitamin B-6 mg 0.080 0.056 0.149 1.235 0.505 0.120 Folate, DFE μg 15 7 62 3 23 19 Vitamin A, RAE μg 42 6 337 0 47 0 Vitamin A, IU IU 833 114 6748 9 937 2 Vitamin E (alpha-tocopherol) mg 0.54 0.38 2.50 0.080 0.69 0.02 Vitamin K (phylloquinone) μg 7.9 10.1 310 1.7 11.8 0.4 Lipids Fatty acids, total saturated g 0.028 0.139 0.014 0.089 0.059 0.042 Fatty acids, total monounsaturated g 0.031 0.155 0.275 0.011 0.023 0.013 Fatty acids, total polyunsaturated g 0.083 0.417 0.040 0.249 0.222 0.017

a Value per 100 g of fresh product. Source: USDA Food Composition Databases (2018). b Tomatoes, red, ripe, raw. c Tomatoes, red, ripe, cooked. d Coriander leaves, raw. e Garlic, raw. f Peppers, Serrano, raw. g Onions, raw.

3. Bioactive compounds in Mexican sauces: what could be the arthritis. Besides, they could exert hypolipidemic, hypocholesterolemic, benefits of the Mexican sauces consumption? anti-inflammatory, antioxidant and anti-tumor activities (Srinivasan, 2005). On the other hand, tomato is the most important source of ly- Beyond the nutritional content of the main ingredients of the copene in the western diet, this compound is well known for its health Mexican sauces, these crops contain BC which have gained scientific benefits (Ranveer, 2018). Among the main ingredients of the Mexican interest due to their intriguing biological activities in order to prevent sauces, the tomato is the only vegetable that contains lycopene several chronic diseases such as cancer and cardiovascular diseases. (Table 2), a carotenoid known due to their antioxidant and anti-in- Moreover, the consumption of the mentioned ingredients has been re- flammatory properties (Campos et al., 2017), responsible of the red lated with the decrease of chronic diseases development (Raigond et al., color of this crop (Georgé et al., 2011). This BC is characterized by a 2018). As far as we know, there are no studies of the specific benefits of high antioxidant potential, the highest among carotenoids. For this the Mexican sauces consumption but Mexican sauces are a mixture of reason, lycopene has been suggested to display many beneficial effects, vegetables that contain particular compounds that have been isolated, including its potential cardioprotective role, evaluated in human stu- identified and studied for their health benefits. In Table 2, we high- dies (Costa-Rodrigues et al., 2017). Although, the antioxidant proper- lighted the particularly BC of the main ingredients of the Mexican ties of lycopene are thought to be primarily responsible for its beneficial sauces. According to this Table, in Fig. 2 are shown the chemical properties, the accumulated evidence suggest that other mechanisms, structures of the most abundant BC. such as hormonal and immune system modulation, and metabolic In this sense, an important feature of hot peppers is their pathways, may also be involved (Kong et al., 2010). Regarding husk which varies not only between varieties but also between samples of the tomato (Table 2), β-carotene and lutein are they main BC compounds same variety due to agronomical differences. ‘’ hot pepper (Elizalde-González and Hernández-Ogarcía, 2007). Chung et al. (2017) ( Jacq.) is one of the most pungent varieties and red reported the anti-inflammatory effects of lutein in coronary artery bell pepper (Capsicum annum L. var. annuum) presents low or any disease patients. pungency. This pungency is due to capsaicinoids, a group of alkaloids It is noteworthy that the phenolic compounds (PC) profile is dif- found only in the Capsicum species. The most important capsaicinoids ferent between coriander crop (Table 2) grown in different countries. are capsaicin, dihydrocapsaicin, and nordihydrocapsaicin (Schweiggert Thus, quercetin derivatives were the major PC reported in coriander et al., 2006). The content of capsaicinoids in ‘Serrano’ hot pepper from (Barros et al., 2012) and phenolic acids were the most (Table 2) was 3330.9 μg/g dry weight (DW) (Alvarez-Parrilla et al., predominant BC identified in coriander leaves from Brazil (de Almeida 2011). Beyond the sensory importance of capsaicinoids, they are used Melo et al., 2005). However, Oganesyan et al. (2007) identified 21 PC to ease the pain associated with neuropathy, cluster headaches, and in coriander grass from Russia. They summarize that due to the content

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Table 2 Bioactive compounds content of the main ingredients of Mexican saucesa.

Corianderb Garlicc ‘Serrano’ hot pepperd Onione Husk tomato/Tomatillof Tomatog

Total Polyphenols Content (mg GAE/100 g DW) 101.39 ± 1.12 1940 ± 120 1032 ± 95 2449 ± 120 8651 ± 403 190.5 ± 7.9 Cinnamic acids derivatives (μg/g DW) Caffeic acid d 8.6 ± 0.7 nd 0.1 ± 0.01 nd 22.48 ± 0.47 Caffeic acid-O-hexoside nd nd nd nd nd 23.63 ± 1.63 Chlorogenic acid nd nd nd 0.98 ± 0.07 nd 113.93 ± 4.08 Ferulic acid d 0.3 ± 0.03 nd 1.77 ± 0.30 nd 8.34 ± 0.27 Ferulic acid-O-hexoside nd nd nd nd nd 69.96 ± 5.30 Ferulic acid glucoside 122.29 ± 12.32 nd nd nd nd nd ρ-coumaric acid nd 0.2 ± 0.02 nd 0.4 ± 0.03 nd nd ρ-coumaroylquinic acid 303.83 ± 9.27 nd nd nd nd nd Sinapic acid nd 0.5 ± 0.04 nd 2.6 ± 0.2 nd nd Benzoic acids derivatives (μg/g DW) Gallic acid d nd nd 64.90 ± 1.22 nd 3.88 ± 0.05 Protocatechuic acid nd 3.6 ± 0.3 nd 1.2 ± 0.1 nd 3.78 ± 0.08 Vanillic acid nd 2.7 ± 0.2 nd 6.3 ± 0.5 nd nd ρ-hidroxybenzoic acid nd 6.1 ± 0.5 nd 44.0 ± 3.0 nd nd Flavonol (μg/g DW) Quercetin d 80.6 ± 6 nd 488.0 ± 33 nd 14.78 ± 0.17 Quercetin-3-O-rutinoside 3296.16 ± 15.50 nd nd nd nd nd Quercetin-3-O-glucuronide 1237.13 ± 22.72 nd nd nd nd nd Quercetin-3-O-glucoside 405.36 ± 10.93 nd nd nd nd nd Quercetin-3,4′-diglucoside nd nd nd 42.7 ± 5.0 nd nd Quercetin-4′-glucoside nd nd nd 21.3 ± 2.5 nd nd Kaempferol nd 1 ± 0.01 nd 5.0 ± 0.4 nd nd Kaempferol-3-O-rutinoside 320.86 ± 20.76 nd nd nd nd 7.19 ± 0.25 Rutin d nd nd nd nd 289.73 ± 4.85 Myricetin nd 693.0 ± 0.05 nd nd nd nd Flavone (μg/g DW) Apigenin d 217 ± 0.02 nd nd nd nd Orientin d nd nd nd nd nd Luteolin d nd nd nd nd nd Flavanone (μg/g DW) Naringenin nd nd nd nd nd 54.47 ± 0.03 Naringenin-7-O-glucoside nd nd nd nd nd 17.61 ± 0.44 Hesperidin d nd nd nd nd nd Alkaloids (μg/g DW) Total capsaicinoids nd nd 3330.9 ± 115 nd nd nd Capsaicin nd nd 1606.1 ± 59.2 nd nd nd Dihydrocapsaicin nd nd 1499.9 ± 49.0 nd nd nd Nordihydrocapsaicin nd nd 224.9 ± 18.1 nd nd nd Carotenoids (mg/100 g DW) β-carotene 73.64 ± 0.26 nd nd nd 253.01 ± 36.1 67.51 ± 9.12 Lycopene nd nd nd nd nd 18.24 ± 0.10 Lutein nd nd nd nd 144.57 ± 12.0 nd

a d = detected but no-quantified, nd = no detected, DW = dry weight. b Barros et al. (2012), Oganesyan et al. (2007). c Miean and Mohamed (2001), Gorinstein et al. (2008). d Alvarez-Parrilla et al. (2011). e Bonaccorsi et al. (2008), Liguori et al. (2017), Gorinstein et al. (2008). f Elizalde-González and Hernández-Ogarcía (2007) (Physalis philadeplphica for carotene and lycopene), Medina-Medrano et al. (2015) (Physalis hederifolia for total polyphenol content). g Georgé et al. (2011), Vallverdú-Queralt et al. (2011). of the PC identified, coriander preparations can be promising for the neuron degeneration involve in the development of Parkinson’s disease prophylaxis of cardiovascular diseases. Due to the high BC content of C. (Huang et al., 2018). sativum, the prominent biological properties of this plant include neu- Beyond the biological activities related to BC from the main in- roprotective, anxiolytic, and anti-convulsant effects (Prachayasittikul gredients of Mexican sauces, the effects that could exert in the human et al., 2018). Interestingly, all parts of coriander have shown medicinal body when they are mixture may increase due to a synergy effect properties, i.e., coriander seeds and essential oils have been in- among the main BC present (Williamson and Clifford, 2017). However, vestigated for their anti-microbial, hypoglycemic, hypolipidemic, an- this biological potential depends of the release of BC from the food algesic, and anti-inflammatory biological activities (Laribi et al., 2015). matrix during the gastrointestinal digestion, which must be available Regarding PC, flavonols and benzoic acids derivatives are the most for intestinal absorption, a term known as bioaccessibility (Guerra abundant in onions. It has been identified quercetin and their glyco- et al., 2012). Several factors will modify the bioaccessibility of BC such sides (Table 2)(Bonaccorsi et al., 2008; Liguori et al., 2017). It has been as the interactions with the food matrix compounds (carbohydrates, reported that anti-carcinogenic, anti-inflammatory and anti-viral ac- dietary fiber, and protein) and processing (Bohn, 2014). It has been tivities may exerted when is consumed quercetin (Li, et al., 2016b). reported that the method can affect the nutrition quality of Also, as it is shown in Table 2, quercetin and myricetin are the most food and increase or decrease the content of BC. Therefore, knowing the abundant BC in garlic (Miean and Mohamed, 2001; Gorinstein et al., kinetics of degradation of nutrients and BC during the processing and 2008). It has been reported that myricetin could reduce dopaminergic cooking processes may help the food processor, or consumer to

5 A.P. Cárdenas-Castro, et al. International Journal of Gastronomy and Food Science 17 (2019) 100154

Fig. 2. Chemical structures o f the main bioactive compounds identified in the main ingredients of Mexican sauces. Bioactive compound mainly found in: a) Coriander, b) Tomato, c) Onion,d)Hot pepper, e) Garlic, f) Husk tomato. limit losses, preserve or even better, enhance food quality (Fabbri and to the ability of garlic to reduce the nitrite concentration in the gastric Crosby, 2016). tract. A protective association of onion consumption against lung Recently, Pérez-Burillo et al. (2018) established a relation among cancer has been reported (Buiatti et al., 1989; Xing et al., 1982, Le the cooking method (steamed, boiled, roasted, fried, breaded and Marchand 2002). Nevertheless, the biological effects that Allium plants grilled), time of processing and antioxidant capacity during the in vitro may exert are related to the thiosulfinates and volatile sulfur com- gastrointestinal digestion and in vitro fermentation of 23 widely con- pounds, responsible for their characteristic pungent aroma and . sumed vegetables in Spain (included garlic, onion and hot pepper). Unfortunately, these compounds are unstable and give rise to trans- They concluded that breading is the culinary technique that causes formation products when they are cooked. more damage in BC content but thermal treatments (grilling and ) Then, new studies are focus on other BC that are more stable to could improve the availability of some molecules due to cell break cooking and to storage, such as sapogenins, saponins and flavonoids down enhancing their absorption in the small intestine (Miglio et al., (Lanzotti, 2006). Therefore, the processing methods applied to the main 2007). Likewise, during the in vitro fermentation (large intestine) the ingredients of the Mexican sauces will influence their BC content as antioxidant capacity was higher when vegetables were boiled, steamed, well as their bioaccessibility. Thus: how should be consumed and roasted or raw (less thermally damaged). This indicated that the sub- cooked the main ingredients of Mexican sauces to maximize their strates that reach the colon are modified by cooking technique and that beneficial effects? In order to answer this question, in Table 3 is sum- the BC of vegetables less thermally damaged would be more bioacces- marize the effect of the cooking method in the BC content of the main sible in the large intestine where they will be biotransformed by gut ingredients of Mexican sauces. microbiota into metabolites which will exert the final health effects of Surprisingly, to author’s knowledge, there are no studies of the BC (Espín et al., 2017). cooking or heating effect in coriander leaves but this effect has been Interestingly, even before the profile of BC of garlic and onion were tested in coriander seeds. Zhang et al. (2015) identified the BC profile of known, they have been used for the treatment of many diseases since raw and roasted coriander seeds (Table 3). In both samples, they found ancient times (Lanzotti, 2006), i.e., Egyptian medical papyrus reports identical BC profile and the predominant component found was tripe- several therapeutic formulas based on these Allium species for treatment troselinin. Besides, BC from raw and roasted coriander seeds inhibited of heart diseases, headache, bites, worms and tumors (Block, 1985). the in vitro growth of human tumor cells. Animal studies showed that Regarding the prevention of tumors development, it has been related the consumption of coriander fresh leaves produced a dose-dependent the decrease of gastric cancer risk with the increase of garlic intake due improvement in the memory scopes and reversed the memory deficits

6 A.P. Cárdenas-Castro, et al. International Journal of Gastronomy and Food Science 17 (2019) 100154

Table 3 Effects of cooking methods on the bioactive compounds (BC) content in the main ingredients of Mexican sauces.

Ingredient BC Content: Best way Biological activities attributed Cooking effect conclusion consumption

Coriandera The BC profile did not change for raw and cooked Raw seeds and Inhibition of human tumor cells growth (gastric, Raw seeds seeds and its functional quality. Tripetroselinin was leaves prostate, colon, breast and lung carcinoma) (I). Roasted seeds (Seeds were roasted on a the most abundant component. Enhancement of memory (A). stove-top in a frying pan until they Regarding raw coriander leaves, they contain ascorbic were brown color) acid, cineole, borneol. Raw leaves Garlicb Raw: (↑) allicin content (90% bioaccessible). Raw Ajoene showed inhibition of pancreatic tumor cells (I). Raw Processing (↓) content of phenolic compounds. Studies indicated that consumption of garlic reduce Stir-fry (sunflower oil, heated 180 °C, Stir-fry: (↑) organosulfur compounds (OSCs, as ajoene) parameters associated with cardiovascular disease (I). 5 min, chopped garlic) content (52–87% bioaccessible). Boil (100 °C, 10 min) Fry (Without fat, in a pan, 100 °C, 10 min) Hot pepperc Boiling: (↓) capsaicinoids content Grilled Reduction of blood glucose in diabetic rats by elevation Raw Grilling: (↑) capsaicinoids and phenolic compounds of the insulin level and inhibition of glucose absorption Boil (96 °C in a covered pan) content. (A) Grill (210 °C on a hot plate) Even boiling reduced moderately the content of capsaicinoids, cooking increase the phenolic compounds content in pungent peppers. Husk tomatod Cooking: (↓) β-carotene and lutein content. Raw β-carotene showed anti-inflammation properties (A) and Raw Outstanding, sucrose esters were identified on the lutein has showed prevention of macular degeneration Boil (94 °C in a covered pot) sticky substance coating the surface of . Raw (I). Pressure cooker (15 psi) or cooked (The sticky material covers the entire peel of Sucrose esters showed antiinflammatory activity similar the . It is therefore integrated in foods prepared to aspirin or ibuprofen (I). with husk tomato) Onione Raw onions showed the greatest in vitro human Raw and fried Quercetin and its derivatives have showed antioxidant Raw exposure. (< 10 min) and antiinflammatory activities with cyclooxygenase-1 Fry (10 mL sunflower oil, heated 160 °C, Thermal processing (> 10 min): (↓) quercetin and (COX-1) and 12-lypoxygenase (12-LOX) assay using 5,10 and 15 min, 100 g diced diglucoside and glucoside content in all samples. human platelets (E). onion) Frying (< 10 min): Best for retention of quercetin Bake (Domestic oven pre-heated 180 °C, glycosides concentrations. 100 g onion were baked in the Even frying less than 10 min is the best cooking center of the oven for 5, 10 and method for retention of quercetin glycosides, raw 15 min) consumption is considered the best due heat treatment Steam (100 g onion were steamed in a longer than 10 min decreases the content of quercetin Tefal steam for 5, 10 and 15 min) diglucoside and glucoside. Tomatof Cooking: (↑) lycopene (> 50%) content. Thermal Boiled Lycopene has been suggested to display potential Raw processing makes lycopene more accessible. cardioprotective role. 225 volunteers consume tomato Heat treatment (88 °C, 2, 15 and Thermal processing increases the bioaccessibility and and lycopene elicited an improvement in high density 30 min) in a well-sealed pressure content of lycopene. lipoprotein functionality (H). Stephan cooker

*(I) = In vitro assays, (A) = Animal studies, (E) = Ex vivo assays, (H) = Human trials. a Zhang., et al., 2015; Mani and Parle, 2009. b Gorinstein et al., 2008; Torres-Palazzolo et al., 2018; Lee et al., 2019. c Ornelas-Paz et al., 2009; Zhang et al., 2018. d Elizalde-González and Hernández-Ogarcía, 2007; Saini et al., 2015; Steiner et al., 2018; Zhang et al., 2016. e Harris et al., 2015; Lesjak et al., 2018. f Dewanto et al., 2002; Li et al., 2016a; Costa-Rodrigues et al., 2017. of young and aged Wistar rats with amnesia (induced by scopolamine). while OSCs were 52–87% bioaccessible in cooked garlic. Further re- Then, coriander leaves may be possible candidates for improving search around garlic compounds metabolism is needed to understand memory (Mani and Parle, 2009). the true biological activities that consumption of raw or cooked garlic In 2008, Gorinstein et al. found that boiling and frying decreases the may exert on the organism. content of polyphenols in garlic. In vitro studies reported the ability of The effect of thermal treatment on the content of capsaicinoids and garlic (and its bioactive constituents) to reduce parameters associated PC in Mexican hot peppers (among them ‘Serrano’, ‘Jalapeño’ and with cardiovascular disease (Rahman and Lowe, 2006). Recently, ‘Habanero’) has been evaluated and is showed in Table 3. Boiling (96 °C Torres-Palazzolo et al. (2018) reported the influence of cooking on in a covered pan) and grilling (210 °C in a hot plate) was carried out organosulfurade compounds (OSCs) bioaccessibility in raw and cooked according to traditional techniques of the Mexican cuisine. The contents (stir-fry) chopped garlic. When garlic is chopped, allicin is formed by of capsaicinoids in raw and cooked hot peppers varied widely among the enzyme allinase. Allicin can be transformed through different cu- hot peppers varieties. Boiling prompted a decrease in capsaicinoids linary methods into diverse OSCs i.e., ajoene (Block, 2010; Locatelli content (1.1–28.1%), while grilling caused a significant increase et al., 2015)(Table 3). These compounds have shown anti-tumoral, (2.6–924.9%). PC content increased in ‘Jalapeño’ and ‘Serrano’ hot anti-microbial, anti-viral and immune enhancement using in vitro assays pepper during boiling and grilling compared to the content of raw (Corzo-Martínez et al., 2007) and recently, ajoene showed in vitro in- samples. This increase could be attributed to a dehydration of the food hibition of pancreatic tumor cells (Lee et al., 2019). Torres-Palazzolo matrix, liberation of conjugated or bound capsaicinoids and PC to cell et al. (2018) concluded that digestion and stir-frying process did not wall due to thermal process and inactivation of capsaicinoids-de- considerably affected OSCs bioaccessibility, observing that only allicin stroying enzymes (peroxidases) (Harrison and Harris, 1985; Huffman was quantified in raw garlic (90% of allicin remained bioaccessible) et al., 1978; Lee and Howard, 1999; Schweiggert et al., 2006). Thus,

7 A.P. Cárdenas-Castro, et al. International Journal of Gastronomy and Food Science 17 (2019) 100154 household cooking of Mexican endemic gastronomic techniques can bioaccessibility of this carotenoid, and interestingly, the addition of the cause decreases or increases in the BC content in hot peppers (Ornelas- -oil-in water emulsion increased the bioaccessibility of lycopene. Paz et al., 2009). It is noteworthy that capsaicinoids significantly re- Then, ingesting tomatoes with may enhance the chemical duced the blood glucose in diabetic rats (Zhang et al., 2018). stability and bioaccessibility of carotenoids such as lycopene due its Elizalde-González and Hernández-Ogarcía (2007) evaluated the ef- hydrophobic chemical structure. Thus, processing the main ingredients fect of cooking on the content of β-carotene and lutein of two “toma- of Mexican sauces may enhance or decrease the BC content. tillo” varieties cooked in pot boiling (time was recorded when water reached its boiling point) or in a pressure cooker (15 psi) (Table 3). The 4. Conclusions concentration of β-carotene and lutein in fresh husk tomatoes (Physalis ixocarpa) and tomatillos (Physalis philadelphica) was higher compared to The effect of processing in BC content of the predominant in- cooked tomatoes. β-carotene has been one of the most investigated gredients of Mexican sauces as well as the possible biological activities carotenoids due its biological properties (i.e. anti-inflammation) tested that may exert are summarized in Table 3. These activities are mainly in animal experimental models (Saini et al., 2015) and lutein has shown related with anti-inflammatory and anti-carcinogenic effects. Mexican prevention of macular degeneration, role in the development of the sauces could exert different health benefits that still unknown, and have visual, evaluated in human retinal pigment epithelial cells (Steiner to be evaluated. The knowledge reported herein may influence the et al., 2018). It is noteworthy that when the husk of tomatillo is re- development of further scientific studies of Mexican sauces and their moved, a sticky-waxy substance on the surface of the fruit is exposed. possible functional properties besides to introduce a staple food of This material is not washable by water and it is consequently integrated Mexican gastronomy, which represents the miscegenation culture that into foods prepared with husk tomato. Without this vegetable, green was born during the European colonization in America. Mexican sauces cannot be made (Montes and Aguirre, 1994). Then, green Mexican sauces will contain the sticky material. Recently, Zhang Declarations et al. (2016) identified and isolated new sucrose esters present on the sticky substance coating the surface of tomatillos. These compounds As a review paper, no participants were tested in this paper. showed anti-inflammatory activity similar to aspirin or ibuprofen using in vitro cyclooxygenase enzymes (COX-1 and -2) inhibitory assays. Consent for publication These results suggest possible functional properties of this vegetable. Further studies are needed to evaluate the resistance and bioavailability Approval to publish has been given where required. of these compounds after thermal treatment. As far as we know, no studies have been reported on the effects of thermal processing in BC Availability of data and material content of husk tomato, apart from McGorrin and Gimelfarb (1998) whom identified volatile and non-volatile compounds in fresh and There is no data or material to make available. cooked husk tomatoes, but they concluded that the relative flavor sig- nificance of these compounds in cooked tomatillos should be clarified Conflicts of interest by further research. Commonly, raw onion undergo thermal process before consumption Authors declared any conflict of interest. due to its harsh typical flavor; that is why Harris et al. (2015) evaluated the effect of thermal processing (frying, baking and steaming for 5, 10 Authors' contribution and 15 min) on 3,4′‘-O-quercetin-diglucoside and 4′‘-O-quercetin-glu- coside levels besides to determine their in vitro human exposure (μg/ Edition of the manuscript: De la Rosa, L. A., Zamora-Gasga, V.M., day) (Table 3), by assessing the quantity of each quercetin derivative Ruiz-Valdiviezo, V.M. and Alvarez-Parrilla, E. available for human absorption per gram of food (μg/g) multiplied by Writing of the manuscript: Cárdenas-Castro, A.P. and Perales- the quantity of food consumed per day (g/day). Frying (5 min) showed Vázquez, G.C. the highest increase of the compounds, suggesting that thermal treat- Corresponding author and final revision: Sáyago-Ayerdi, S.G. ment will possibly affect the wall structure of plant cells, increasing the BC extraction (Verkerk and Dekker, 2004), however, significant Funding thermal degradation of quercetin derivatives occurred for frying per- iods longer than 10 min. Besides, frying for 5 min showed the highest Authors would like to acknowledge the National Technological level of absorption of both types of quercetin derivate evaluated, Institute of Mexico. nevertheless, raw onion showed the highest 3,4′-O-quercetin-digluco- side and 4′-O-quercetin-glucoside level available for absorption (human Acknowledgments exposure). Therefore, for this study, raw consumption was considered best. It has been reported the antioxidant and anti-inflammatory ac- Cárdenas-Castro AP and Perales-Vázquez Guadalupe del Carmen tivities of quercetin and its derivatives (Lesjak et al., 2018). acknowledge the financial support to CONACYT, Mexico for a grant The thermal processing effect on lycopene has also been reported in (Registration number: 662703, 826985, respectively). tomatoes. Dewanto et al. (2002) evaluated the content of lycopene in raw and cooked tomatoes at 88 °C for 2, 15 and 30 min in a well-sealed List of abbreviations pressure Stephan cooker (Table 3). The content of lycopene in cooked tomato increased more than 50% compared with raw tomato content. BC Bioactive compounds Heat processing breaks down cell wall structures, reducing cellular TDF Total dietary fiber integrity (releasing bound lycopene to cell wall) that would make ly- IDF Insoluble dietary fiber copene more accessible (Shi and Maguer, 2000). Interestingly, in the SDF Soluble dietary fiber Mediterranean diet, vegetables are consumed with olive oil and this has ALA α-linolenic acid been related to potential health benefits of the Mediterranean diet, DW Dry weight therefore, Li et al. (2016a) evaluated the bioaccessibility of lycopene in PC Phenolic compounds raw and cooked (boiling: 100 °C, 10 min) tomatoes with a stock of olive- OSCs Organosulfur compounds oil-in-water emulsion. Thermal processing increased the

8 A.P. Cárdenas-Castro, et al. International Journal of Gastronomy and Food Science 17 (2019) 100154

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Prachayasittikul, V., Prachayasittikul, S., Ruchirawat, S., Prachayasittikul, V., 2018. Cárdenas-Castro, A.P. has a master degree in Food Science by Technological Institute of Coriander (Coriandrum sativum): a promising functional food toward the well-being. Tepic and currently, she is ph. D. student at this University. Her scientific interests are the – Food Res. Int. 105, 305 323. https://doi.org/10.1016/j.foodres.2017.11.019. bioaccessibility in the small and large intestine of bioactive compounds from Mexican Prakash, D., Singh, B.N., Upadhyay, G., 2007. Antioxidant and free radical scavenging dishes and foods. She has published 2 articles. activities of phenols from onion (Allium cepa). Food Chem. 102 (4), 1389–1393. https://doi.org/10.1016/j.foodchem.2006.06.063. Rahman, K., Lowe, G.M., 2006. Garlic and cardiovascular disease: a critical review. J. Perales-Vázquez, G.C. has master degree in food science at the Technological Institute of ff Nutr. 136 (3), 736S–740S. https://doi.org/10.1093/jn/136.3.736S. Tepic. She is nutritionist interested in the research of the e ect of cooking processes in the Raigond, P., Kaundal, B., Sood, A., Devi, S., Dutt, S., Singh, B., 2018. Quantification of bioaccessibility of phenolic compounds. biguanide and related compounds (anti-diabetic) in vegetables and fruits. J. Food Compos. Anal. 74, 82–88. https://doi.org/10.1016/j.jfca.2018.09.001. De la Rosa, L. A. has a Ph. D. degree in Biology from the University of Santiago de Ranveer, R.C., 2018. Lycopene: A Natural Red Pigment Natural and Artificial Flavoring Compostela, Spain. She is a full-time professor at the Autonomous University of Ciudad Agents and Food Dyes. Academic Press. U.S.A. Juárez, Mexico. In the last 10 years she has been working with pecans and other dry Rozin, P., Schiller, D., 1980. The nature and acquisition of a preference for by fruits, evaluating their phytochemical content by both spectroscopic and chromato- humans. Motiv. Emot. 4 (1), 77–101. https://doi.org/10.1007/BF00995932. graphic technics. She has published more than 50 papers in international journals. Saini, R.K., Nile, S.H., Park, S.W., 2015. Carotenoids from fruits and vegetables: chem- istry, analysis, occurrence, bioavailability and biological activities. Food Res. Int. 76, Zamora-Gasga, V.M. is Ph. D. in Food Science at the Technological Institute of Tepic and 735–750. https://doi.org/10.1016/j.foodres.2015.07.047. he is research professor at this University. His research focus is on the effects of combined Santiago-Torres, M., Kratz, M., Lampe, J.W., Tapsoba, J.D.D., Breymeyer, K.L., Levy, L., and low-cost technologies on the preservation of processed foods in the region. Neuhouser, M.L., 2015. Metabolic responses to a traditional Mexican diet compared Additionally, he has worked on the identification of gut metabolites and its potential with a commonly consumed US diet in women of Mexican descent: a randomized effect on intestinal health using multivariate analysis tools. He has published more than 8 crossover feeding trial. Am. J. Clin. Nutr. 103 (2), 366–374. https://doi.org/10. articles in international journals. 3945/ajcn.115.119016. Schweiggert, U., Carle, R., Schieber, A., 2006. Characterization of major and minor Ruiz-Valdiviezo, V.M. received the Ph. D. degree in Biotechnology from Center for capsaicinoids and related compounds in chili pods (Capsicum frutescens L.) by high- Research and Advanced Studies of the National Polytechnic Institute (CINVESTAV-IPN) in performance liquid chromatography/atmospheric pressure chemical ionization mass , Mexico and he is currently research professor at Technological Institute of spectrometry. Anal. Chim. Acta 557 (1–2), 236–244. https://doi.org/10.1016/j.aca. Tuxtla Gutierrez, Chiapas, Mexico. His research interest is related to the biochemical and 2005.10.032. molecular analysis of the microbial communities present in extreme and agricultural Shi, J., Maguer, M.L., 2000. Lycopene in tomatoes: chemical and physical properties af- environments. He has published 47 articles in international journals. fected by food processing. Crit. Rev. Biotecnol. 40 (1), 1–42. https://doi.org/10.

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Alvarez-Parrilla, E. has a Ph.D. degree in Chemistry from the University of Santiago de Sáyago-Ayerdi, S.G. has a Ph.D. degree in Nutrition from the Complutense University of Compostela, Spain. He is a full-time professor at the Autonomous University of Ciudad Madrid, Spain. She is a full-time professor at Integral Food Research Laboratory in Juárez, Mexico since 2001. He has extensively work with the evaluation of processing Technological National of Mexico, Campus Tepic. Her research focus is on bioaccessibility techniques on the phytochemical characterization of hot pepper products. He has pub- of bioactive compounds, dietary fiber, antioxidant activity and in vitro colonic fermen- lished more than 60 papers in international journals. tation. She has published more than 60 papers in international journals.

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