Effect of nutritionally fortified tortillas on growth and physical development in the pig

Nutrition Research 25 (2005) 711 – 716 www.elsevier.com/locate/nutres

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Effect of nutritionally fortified tortillas on growth and physical development in the pig Juan de Dios Figueroa Ca´rdenasa,T, Marı´a Guadalupe Acero Godı´nezb,c, Teo´dulo Quezada Trista´nc, Esmeralda Rebollar Serranob a

Research Center of Advanced Studies – IPN, Campus Queretaro (CINVESTAV – Queretaro), Libramiento Noroponiente No. 2000 Fracc., Real de Juriquilla, Queretaro, Qro 76230, Mexico b Interdisciplinary Program of Animal Science (PICP), University of Colima, Av. Universidad 333, Colima, Col. 28040, Mexico c Autonomous University of Aguascalientes, Centro de Ciencias Agropecuarias, Blvd. Universidad No. 940, Fracc. Bosques del Prado Aguascalientes, Ags. 20100, Mexico Received 5 August 2004; revised 17 March 2005; accepted 23 June 2005

Abstract The physical development of muscle, bone, and blood in pigs fed diets containing different forms of tortillas was evaluated. The tortilla products included corn tortillas (TN), TN with a mixture of 0.15% vitamins and minerals (TNV), TN with 4% (as is) defatted soy paste (TNS), corn flour tortillas (TH), TH with vitamins (THV), and TH with soy paste (THS). The femur weight of pigs fed the TNS and THS diets was higher ( P N .05) than those of pigs fed TN, TNV, TH, and THV diets. Calcium in femurs was lower for the TN and TH diets compared with TNV, THV, TNS, and THS diets. Blood analysis showed that the hematocrit, hemoglobin, and erythrocytes values were optimal in pigs fed TNS and THS. Tortilla fortification with soy may have important nutritional benefits based on the evaluation in the pig growth and development model. D 2005 Elsevier Inc. All rights reserved. Keywords: Tortilla fortification; Pig; Calcium assimilation

1. Introduction Mexico has the highest annual consumption of corn tortillas (TN) in the world which is 120 kg per capita or approximately 328 g/d [1,2]. In the rural areas of Mexico, 65% of dietary nutrients come from tortillas, 15% from beans, and the rest from 20 other food items [3]. T Corresponding author. Tel.: +52 442 441 4915; fax: +52 442 441 4938. E-mail addresses: [email protected], [email protected] (J. de Dios Figueroa Ca´rdenas). 0271-5317/$ – see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.nutres.2005.06.006

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Tortillas alone cannot provide the population with all the nutrients required for adequate growth and development [2], but the nutritional status of low-income groups can be significantly upgraded by the use of fortified tortillas [2,3]. Several methods for improving the nutritional status of developing countries have been studied [4,5]. One important aspect to consider is diet performance and, in this regard, is to determine the effects of tortillas on pig growth as a model for rapid development. The purpose of our research was to evaluate the nutritional effects of diets consisting of commercial tortillas and traditional nixtamal tortillas fortified with a vitamin and mineral mixture as well as with defatted soy flour meal on the physical development of tissues in the young pig.

2. Methods and materials 2.1. Tortillas and diets The nixtamal tortillas were made by the traditional process [3]. The vitamin and mineral premix consisted of thiamin mononitrate, 53.920 g; riboflavin, 33.330 g; nicotinamide, 383.850 g; folic acid, 6.165 g; reduced iron (Fe), 321.430 g; zinc oxide, 130.760 g; and maltodextrin to complete 1000 g. Soy flour was produced commercially by heating the soy grain and making flakes; hexane was used to extract the fat until a level of less than 1% fat was reached. The defatted flakes were cooked and milled with a Pulvex mill model 200 (Maquinaria para Moliendas y Mezclas, SA de CV, Mexico DF), with a 0.1-mm screen to get soy flour. The nixtamal masa was prepared using the traditional process as indicated elsewhere [3]. The nixtamal (corn cooked with lime) was prepared following the traditional process as indicated elsewhere [3]. This nixtamal was mixed with 4% defatted soybean flour (as is) and then milled to obtain the masa used to make the tortillas (or nixtamal masa fortified with 4% soy paste [TNS]). The 0.15% vitamin premix, diluted in water, was added to the nixtamal during the milling step to facilitate the homogenization of the materials and referred to nixtamal masa fortified with 0.15% vitamin mix (TNV). The masa made from instant corn flour (TH) was prepared with an instant commercial corn flour (without vitamins) hydrated in a commercial blender (Tecnomaı´z SA de CV, Mexico DF), adding water to achieve a masa consistency for making tortillas. The masa made from instant corn flour with 4% soy paste (THS) contained defatted soybean paste (milled using a hammer mill, Pulvex mill Model 200 Maquinaria para Moliendas y Mezclas, SA de CV, Mexico DF) with a US 60 screen plus added instant commercial corn flour. The material was mixed in a commercial blender and hydrated with water to obtain a masa for making tortillas. The masa made from instant corn flour with 0.15% vitamin premix (THV) contained the ingredients previously described and mixed in a commercial blender and hydrated with the addition of water to achieve a masa for making tortillas. The diets evaluated were as follows: nixtamal tortillas (TN), nixtamal tortillas with 0.15% premix of hydrosoluble vitamins and minerals (TNV), nixtamal tortillas with 4% defatted soy flour (TNS), tortillas made from instant corn flour (TH), tortillas made from instant corn flour with a 0.15% premix of vitamins (THV), and tortillas made from instant corn flour with 4%

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defatted soy flour (THS). The proportion of vitamin and mineral premix or defatted soy flour added to the masa was calculated by weighing the masa or nixtamalized corn before the milling step. 2.2. Pigs and biologic assays Eighteen castrated male hybrid pigs from a York-Landrace mother line and a Hampshire boar line were selected. They were 45 days old, with an initial weight of 11.7 F 1.3 kg. Three animals were randomly assigned for each diet. The pigs were housed in individual cages, and the water and different diets were provided ad libitum during 23 weeks. Diets were supplied at least once every 24 hours. Animal care and protocol were approved by the ethical committee of the National Polytechnic Institute. Following animal and institutional guidelines, 5 mL of blood from the jugular vein was collected from pigs with a 21-gauge  38-mm Vacutainer needle. The blood samples were then centrifuged at 2000 rpm for 5 minutes, and serum was stored in a freezer ( 208C) for subsequent analysis. Blood samples were collected in Vacutainer tubes with EDTA. The blood parameters were performed according to the technique described by Coles [6]. The pigs were killed following the Mexican Official Standard regulations (MOM-033200-1995). Animals were humanely killed, and exsanguinated and bled by cutting the cava artery under. Samples of femurs that had been calcined using AACC procedure 08-12 for ash [7] were placed in glass beakers with 20 mL of HCl (1:1) and analyzed for calcium and mineral analysis by inductive coupled plasma following the procedure described by Figueroa et al [3]. The measurement of zinc and iron in femurs was determined by atomic absorption emission [3]. The design of the experiment and collection of samples followed a completely random design for analysis of variance. Where significant differences were found, a Duncan multiple comparison test was performed. The Statistical Analysis System [8] program (version 6, SAS Institute Inc, Cary, NC) was used to analyze the data. 3. Results and discussion The parameters of tissues (muscle, bone femur dry weight, and length) of pigs fed different diets are shown in Table 1. A greater muscle weight was found in pigs fed the TNS diet, followed by those for the THS diet of 19.86 and 16.28 kg, respectively. The pigs fed tortillas Table 1 Muscle and femur measurements in pigs fed different tortilla dietsT Diet

Muscle (kg)

TN TNV TNS TH THV THS

c

9.70 9.80c 19.86a 8.32c 9.57c 16.28b

Head weight (kg) cd

1.53 1.89bc 2.23ab 1.50d 1.60cd 2.35a

Femur dry weight (g) b

131.5 143.2b 188.7a 114.6c 112.0c 147.2b

T Means in columns with different superscripts are significant ( P b .05).

Femur length (cm) 14.8a 16.0a 16.6a 15.5a 14.8a 16.2a

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fortified with a premix of vitamins and those without fortification demonstrated lower muscle weights and were significantly different ( P b .05) from those fed tortillas fortified with soy paste (TNS and THS diets). The dry femur weight was higher for pigs fed the TNS diet (188.7 g) and the THS diet (147.2 g) compared with a range of values (112.6-147.2 g) for pigs fed the TN, TNV, TH, THV, and THS diets (Table 1). The femur weights of pigs fed the TN and TH diets were lower than all other values for pigs (Table 1). The lower femur weights might suggest less calcium assimilation. The calcium content of femurs for the pigs fed the TN and TH diets were 11.64 and 10.73%, respectively, and, compared with 15.54% for TNV, 14.39% for THV, 22.02% for TNS, and 19.81% for the THS diets, appeared lower, although the values were not significantly different (Table 2). Thus, the calcium content of the femurs of pigs fed tortillas fortified with soy paste (TNS and THS) diets was twice as high as those pigs fed the TN and TH diets. The calcium content of the femurs has been used as an indicator of the bioavailability of calcium and is also related to the retention of calcium [9]. Several researchers reported that the calcium in tortillas has a bioavailability of 85% to 93% and that tortillas are an inexpensive source of this mineral in the Mexican diet [10]. Lime is an inexpensive source of calcium used for nixtamalization, with levels of calcium as high as 47.0% to 52.2%, compared with some commercial sources of calcium used in bread fortification which have levels from 12% to 36.5% [9,11]. A similar trend was found for Fe; however, in the pigs fed tortillas fortified with a premix of vitamins and minerals, the Fe level is modestly different from that in tortillas fortified with soy paste. Blood parameters of pigs fed the different diets are presented in Table 3. The pigs fed tortillas fortified with soy paste (TNS and THS). The tortillas fortified with a premix of vitamins and minerals (Fe and Zn), in general, showed higher values compared with their nonfortified counterparts but lower values than those of tortillas fortified with soy paste, except for the MCV (mean corpuscular or globular volume) of some pigs fed the TNV diet which was outside the reference range. The low level of hemoglobin in pigs fed TH and the high variation of MCV with values outside the MCV reference range of 50 to 67 lm3 seem to indicate microcytic anemia for some pigs fed TH, which may be due to Fe deficiency and poor Fe absorption. Hemoglobin is a good indicator of the relative bioavailability (RBV) of an iron-fortified compound [12]. As indicated previously, the levels of iron increase in all the tortilla diets in comparison with unprocessed corn except for the TH diet. Lime impurities, specifically iron oxide, are the main source of Fe in the TN and TH diets. In the TNS and THS diets, the source of iron is lime impurities and also iron native to soy paste, and in the case of the TNV and THV diets, the iron source is lime impurities and also reduced elemental Table 2 Chemical analyses of femurs from pigs fed different tortilla diets Diet

Organic matter (%)

Ash (%)

Calcium (%)

Iron (%)

TN TNV TNS TH THV THS

30.56 35.72 31.48 29.80 33.26 37.57

69.44 64.28 68.52 70.20 66.74 62.43

11.64 15.54 22.02 10.73 14.39 19.81

0.16 0.32 0.28 0.15 0.31 0.24

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Table 3 Blood measurements in plasma of pigs fed different tortilla diets Diets

Hemoglobin (g/100 mL)

Hematocrit (%)

Erythrocyte (mm)

TN TNV TNS TH THV THS Reference range

11 F 1.06 12 F 1.06 12 F 0.70 10 F 1.32 11 F 0.00 13 F 0.28 10 - 16

33 F 2.12 37 F 4.24 39 F 1.82 32 F 5.19 39 F 5.19 39 F 1.15 32 - 50

5.4 F 0.69 5.5 F 0.62 5.6 F 0.25 5.7 F 3.05 5.6 F 1.00 6.2 F 1.24 5 - 8  106

     

106 106 106 106 106 106

Medium globular volume (lm3) 60.36 F 71.59 F 65.86 F 57.51 F 61.94 F 63.93 F 50 - 67

4.90 15.57 1.57 20.26 10.2 8.67

iron added to the premix. However, as indicated by several researchers, some elemental or reduced iron powders (325 mesh) are normally absorbed with an RBV of 49% to 54% [13] for animals and humans, whereas most of them are so poorly absorbed (RBV, 25% to 27%) [14] that they would be expected to have little or no nutritional impact [13]. On the other hand, the data suggest that the iron from lime impurities and that found naturally in soy paste are absorbed well by the pigs as indicated by the bone and blood analyses. Acknowledgment The authors thank the Consejo de Ciencia y Tecnologı´a de Quere´taro (CONCYTEQ) for their financial support for this study. References [1] Del Valle FR, Pe´rez-Villasen˜or J. Enrichment of tortillas with soy proteins by lime cooking of whole raw corn–soybean mixtures. J Food Sci 1974;39:244 - 7. [2] Figueroa JDC. La tortilla vitaminada. Avance y perspectiva 1999;18:149 - 58. [3] Figueroa JDC, Acero GMG, Vasco MNL, Lozano GA, Flores ALM. Nutritional quality of nixtamal tortillas fortified with vitamins and soy proteins. Int J Food Sci Nutr 2003;54(3):189 - 200. [4] Green JR, Lawhon JT, Carter CM, Mattil KF. Utilization of whole undefatted glandless cottonseed kernels and soybean to protein-fortify corn tortillas. J Food Sci 1977;42(3):790 - 4. [5] Collins JL, Sa´nchez JF. Quality parameters of tortillas fortified with soy and cheese. J Food Sci 1980;45:667 - 70. [6] Coles HE. Diagno´stico y patologı´a. Capı´tulo 2. Eritrocitos. 4a ed. Me´xico (DF)7 Mc Graw-Hill; 1986. p. 12 - 43. [7] AACC. Approved Methods of American Association of Cereal Chemists. 9th ed. St Paul, MN: The Association; 1995. [8] Statistical Analysis System (SAS). 4th ed. SAS User’s Guide Version 6, vol. 1. Cary (NC)7 SAS Institute Inc; 1990. p. 943. [9] Ranhotra GS, Gelroth JA, Leinen SD, Schneller FE. Bioavailability of calcium in bread fortified with different calcium sources. Cereal Chem 1997;74(4):361 - 3. [10] Serna-Saldivar SO, Rooney LO, Greene LG. Effect of lime treatment on the availability of calcium in diets of tortilla and beans: rat growth and balance studies. Cereal Chem 1991;68(6):565 - 70. [11] Ranhotra GS. Grain products as a source of dietary calcium. Cereal Foods World 1986;31(8):535 - 6.

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[12] Forbes AL, Adams CE, Arnaud MJ, Chichester CO, Cook JD, Harrison BN, et al. Comparison of in vitro, animal and clinical determination of iron bioavailability: International Nutrition Anemia Consultative Group task force report on iron bioavailability. Am J Clin Nutr 1989;49:225 - 38. [13] Hurrel RF, Furniss DE, Burri J, Whittaker P, Lynch SR, Cook JD. Iron fortification of infant cereals: a proposal for the use of ferrous fumarate or ferrous succinate. Am J Clin Nutr 1989;49:1274 - 82. [14] Sacks PV, Houchin DN. Comparative bioavailability of elemental iron powders for repair of iron deficiency anemia in rats: studies of efficiency and toxicity of carbonyl iron. Am J Clin Nutr 1978;31(4):566 - 71.