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Nutrient Interactions and Toxicity
Research Communication

Total Fumonisins Are Reduced in Tortillas Using the Traditional Nixtamalization Method of Mayan Communities^1,2

Edwin Palencia, Olga Torres, Winston Hagler^*, Filmore I. Meredith, Lonnie D. Williams and Ronald T. Riley^,3

Instituto de Nutricion de Centro America Y Panama (INCAP), Calzada Roosevelt, Zone 11, 09001 Guatemala; ^* Department of Poultry Science, North Carolina State University, Raleigh, NC 27695; and Toxicology and Mycotoxin Research Unit, R. B. Russell Agricultural Research Center U.S. Department of Agriculture/ARS, Athens, GA 30604

³To whom correspondence should be addressed. E-mail: rriley{at}saa.ars.usda.gov.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Fumonisin B₁ (FB₁) is a maize mycotoxin. In tortilla preparation, maize is treated with lime (nixtamalization), producing hydrolyzed FB₁ (HFB₁) due to loss of the tricarballylic acid side chains. This study determined the following: 1) whether nixtamalization by Mayan communities reduces total fumonisins, and 2) the steps in the process at which reduction occurs. Tortillas prepared by the traditional process contained FB₁, FB₂ and FB₃ and their hydrolyzed counterparts. There were equimolar amounts of FB₁ and HFB₁ in the tortillas, but the total fumonisins were reduced 50%. The total FB₁ plus HFB₁ in the residual lime water and water washes of the nixtamal accounted for 50% of the total FB₁ in the uncooked maize. HFB₁ and FB₁ were present in a 1:1 mol/L ratio in the water washes of the nixtamal, the masa dough and the cooked tortillas, whereas the ratio of HFB₁:FB₁ in lime water after steeping was 21. Water washes contained 11% of the FB₁ that was in the uncooked maize. The results show that the traditional method reduced the total fumonisins in tortillas and reduced the sphinganine elevation (a biomarker closely correlated with fumonisin toxicity) in cells treated with extracts of tortillas compared with cells treated with extracts of contaminated maize.

KEY WORDS: • fumonisin B₁ • hydrolyzed fumonisin B₁ • maize • nixtamalization • tortillas

Fumonisin B₁ (FB₁)³ is a fungal contaminant of maize worldwide and is responsible for diseases of farm animals (1). It is a liver and kidney carcinogen in rodents and was recently evaluated to be possibly carcinogenic for humans (2). Fumonisins are not DNA reactive, and renal or liver damage is a prerequisite for carcinogenicity (3). Fumonisins (including FB₁, FB₂, and FB₃) are inhibitors of ceramide synthase, a key enzyme in the de novo sphingolipid biosynthesis pathway (1). Their toxicity and carcinogenicity are closely correlated with disruption of sphingolipid metabolism (3). Because toxicity is a prerequisite for carcinogenicity, a no observable effect level (NOEL) has been determined for both toxicity and carcinogenicity. A provisional maximum tolerable daily intake (PMTDI) of 2 µg/(kg body · d) for fumonisins B₁, B₂ and B₃, alone or in combination has been proposed (3). The PMTDI was calculated on the basis of a safety factor of 100 and a NOEL of 0.2 mg/(kg body · d) for the critical target (rat kidney). Processing methods that reduce the amount of fumonisins in food will reduce fumonisin intake, thereby protecting consumers from the possible adverse effects associated with exceeding the PMTDI.

In the preparation of tortillas, maize is treated with lime, which when heated hydrolyzes the tricarballylic acid side chains, reducing a portion of the FB₁ to the aminopentol backbone (HFB₁) (1). Alkali processing to prepare tortillas is practiced throughout the Americas including Guatemala, other parts of Central America, and Mexico. The process is known as nixtamalization (4). A similar process is used commercially in the United States (5), which has a growing population of immigrants from Mexico and Central and South America. Thus, understanding the comparative safety of nixtamalized products using traditional and commercial processes is of importance to consumers in the United States and elsewhere.

Nixtamalized maize products provide the majority of the daily energy for a large proportion of the population in the Central Highlands of Guatemala. A recent survey conducted in the Central Highlands (unpublished data) found that 100% of the population surveyed consumed maize as tortillas and that the mean daily consumption was 14 tortillas. The consumption of maize derived from products other than tortillas was 145 g. Bressani (4) reported that the daily per capita maize consumption in Guatemala was 318 g. Because of the large amount of maize products consumed by communities in the Central Highlands of Guatemala, even relatively low levels of fumonisins in maize could pose a health risk. For example, at 1 µg total fumonisins/g of maize product, a 60-kg person consuming 318 g would exceed the PMTDI by a factor of 2.65. Several studies have shown that nixtamalization, when conducted in laboratory or full-scale commercial settings, reduced the total fumonisin content of maize (6,7).

The purpose of this study was as follows: 1) to determine whether the traditional method of nixtamalization as practiced by rural Kaqchikel-speaking Mayan communities in the Central Highlands of Guatemala reduced the level of fumonisins in tortillas produced from fumonisin-contaminated maize, and 2) to determine the steps in the traditional process at which reduction in fumonisin levels were most likely to occur.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Maize for preparing tortillas.

Maize contaminated with fumonisins was obtained from North Carolina in 1999. The maize was shelled and segregated so that it contained predominately intact kernels and shipped to the INCAP where it was used to prepare tortillas using the traditional process of the rural Kaqchikel-speaking Mayan communities.

Preparation of tortillas.

Maize was mixed and divided into three equal lots. Approximately 400 g from each lot was placed in steel pots, and samples were removed and stored frozen for analysis by HPLC for FB₁ and HFB₁ and by LC-MS for FB₂, FB₃ and HFB₂ and HFB₃. Coarsely ground lime (CaO, 82 g) was added to 1 L of water; 0.2 L of this stock lime solution was added to each pot followed by an additional 1.1 L of water. The lime water/maize preparation was boiled for 1.75 h; as water evaporated, fresh water was added. The mixture was allowed to cool and steep for 15 h. The steep water was collected and the alkali-treated cooked maize (nixtamal) was rinsed three times with 1.1 L of water. The nixtamal was ground into masa. The volume of the steep water and the rinse water and the wet weight of the nixtamal and masa dough were recorded for each lot. Samples were removed and stored frozen for HPLC analysis. Tortillas were shaped by hand. The mean weight of an uncooked and cooked tortilla was 42 and 16 g, respectively. The tortillas were cooked on a comal (a dish made with clay) over a wood fire. Cooking temperatures varied from 170°C on the outer edge to 212°C at the center of the plate (4). Tortillas were typically 0.5–1 cm thick and 10 cm in diameter. The time of cooking tortillas was 3.5 min. A total of 10 tortillas were prepared from each lot. After drying at 38°C, the tortillas were weighed and stored frozen for later HPLC analysis of FB₁ and HFB₁ and for LC-MS analysis for FB₂, FB₃ and HFB₂ and HFB₃.

Analysis for FB₁ and HFB₁.

After drying, 2–3 g of each tortilla (10/lot) and samples of the uncooked maize (1/lot) were extracted with 25 mL of acetonitrile/water (1:1; pH adjusted to 4.5) as described previously (7). For uncooked maize and cooked tortillas, a second acetonitrile/water extraction was done and samples from both extractions were derivatized using ortho-phthalaldehyde (OPA) (Pierce, Rockford, IL) according to previously described methods (8,9) and analyzed by HPLC with fluorescence detection (8,9). Alkaline steep water and water rinses were centrifuged (500 x g for 10 min) to remove solids and then acetonitrile/water 1:1 (600 µL) and OPA-derivatizing reagent (500 µL) were added directly to 50 µL of the clear liquid sample (pH 4.5) and analyzed by HPLC for FB₁ and HFB₁. LC-MS analysis was similar to that described previously (7) and was used to confirm the presence of other fumonisins. The analytical standard of FB₁ was prepared using the method of Meredith et al. (9), and the purity (>96%) was determined by the procedure of Plattner and Branham (10). The HFB₁ was prepared by the method of Poling and Plattner (11), and MS data were used to verify the purity of FB₁ and HFB₁ standards (9). Standards for HFB₂ and HFB₃ were provided by Ronald Plattner (USDA, Peoria, IL). Results of the HPLC analysis for FB₁ and HFB₁ are presented in nmol/g so that the amount of HFB₁ recovered in each fraction could be compared with the amount of FB₁ in the contaminated maize used to prepare the tortillas.

Bioassay method.

To determine the ability of fumonisins in tortillas and maize to disrupt sphingolipid metabolism (a biomarker for fumonisin exposure and toxicity), a porcine renal epithelial cell line (LLC-PK₁) was used (12,13). The test agents were acetonitrile/water extracts of the fumonisin-contaminated maize used to prepare the tortillas and extracts of the tortillas prepared from the fumonisin-contaminated maize. Clean maize (<0.4 µg FB₁/g) and commercial masa flour (<1 µg FB₁/g) were used for comparison purposes. Because maize extracts from samples even of the highest quality are toxic to cells in culture, preliminary experiments were conducted to determine the dilution and dosing duration that would avoid the acutely toxic effects of concentrated maize extracts on cultured cells. Residues from 1:1 acetonitrile/water (pH 4.5) extracts (25 mL) of 1.5 g of clean or contaminated maize dissolved in 30 mL of growth medium had no effect on ATP-dependent dome formation or tight junction integrity after 6 h of exposure based on visual observation using phase contrast light microscopy. Therefore, 5-g samples of each test agent were extracted and the dried residue was dissolved in complete growth medium (12,13) and diluted to 30% in complete growth medium. Cells were exposed for 6 h and then harvested, extracted as described previously (13) and analyzed for free sphingoid bases (12), a biomarker for ceramide synthase inhibition and fumonisin toxicity (1).

Statistical analysis.

Statistical analysis was done using Sigma Stat software (Jandel Scientific, San Rafael, CA). One-way ANOVA was used followed by tests for post-hoc multiple comparisons using Duncan’s multiple range test. All data were expressed as mean ± SD, and differences among means were considered significant if P 0.05.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The FB₁ concentration in the uncooked maize after two successive acetonitrile/water (1:1) extractions was 38.1 ± 7.4 µg FB₁/g (52.8 ± 7.4 nmol/g) of uncooked maize (n = 6). The FB₁ found in the second extraction of uncooked maize comprised 27 ± 7% of the total (n = 6). In tortillas, FB₁ and HFB₁ found in the second extraction comprised 24 ± 7 and 23 ± 9%, respectively (n = 29). The relative amounts of FB₁ and HFB₁ on a molar basis in the cooked tortillas were approximately equal (Fig. 1A). This was also the case in the uncooked masa dough in which the ratio of FB₁ to HFB₁, was 1.04 ± 0.39 (n = 3). On the basis of the LC-MS analysis, the ratio of the areas under the peaks for FB₁:FB₂:FB₃ (1:0.4:0.3) in the uncooked maize and the ratio under the peaks of FB₁, FB₂, FB₃ (Fig. 1B) and HFB₁, HFB₂ and HFB₃ (Fig. 1C) in the cooked tortillas did not differ.

View larger version (31K): [in this window] [in a new window]   FIGURE 1 The total (A) and relative (B, C) amounts of fumonisin B1 (FB1; black bars) and hydrolyzed fumonisin B1 (HFB1; gray bars) in cooked tortillas expressed as nmol FB1 and normalized to the calculated grams of uncooked maize required to prepare 1 g of tortilla. Values are means ± SD of 10 tortillas prepared from each lot of maize. FB1 or HFB1 means without a common letter are different, P 0.05. (B, C) Examples of the relative amounts of fumonisins in acetonitrile/water (1:1) extracts of cooked tortillas based on single ion monitoring LC-MS analysis. The y-axis values are the percentages of the total ion current normalized to the highest peak.

View larger version (31K): [in this window] [in a new window]   FIGURE 2 The total amount (A) and molar ratio (B) of fumonisin B1 (FB1) and hydrolyzed fumonisin B1 (HFB1) in each wash of the nixtamalized maize (A) and also in the lime water (B). Values are means ± SD in three successive washes (first, second, third) of the nixtamal. The values are normalized to the calculated grams of uncooked maize required to prepare the measured grams of nixtamal. Means without a common letter differ, P 0.05, n = 3. For the comparison of "lime water" to the "first wash," P = 0.0534.

View larger version (39K): [in this window] [in a new window]   FIGURE 3 The ability of acetonitrile/water (1:1) extracts of commercial masa flour (Clean Masa), clean maize, fumonisin B1–containing tortillas (FB-Tortillas) and the fumonisin B1–containing maize (FB-Maize) used to prepare the tortillas to disrupt sphingolipid metabolism based on the elevation in sphinganine in LLC-PK1 cells. The total FB1 plus hydrolyzed fumonisin B1 (HFB1) concentration in the final growth medium was <1.3, <1.3, 7.3 and 15.8 µmol/L, respectively. The inset is the sphinganine to sphingosine ratio. Means without a common letter differ, P 0.05, n = 4/treatment group).

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Regardless of the scale of the process, the initial cooking and steeping of maize under alkaline conditions is the most important step for converting FB₁ to HFB₁ and in reducing the total fumonisins in the cooked tortillas. In the commercial process, the cooking/steeping liquid was found to contain predominantly HFB₁ (7). Based on the data in Voss et al. (7), the ratio of HFB₁ to FB₁ in the cooking/steeping liquid was 45.5; in the pilot-scale study (6), the ratio was 20.2. These results are very similar to what was found with the process used by the Mayan communities in which there was 21 times more HFB₁ than FB₁ in the lime water after cooking and steeping overnight (Fig. 2B).

In the study of Meredith et al. (8), the tortillas from two Guatemalan Central Highland communities (Santa Maria de Jesus and Patzicia) contained high levels (>10 µg/g) of total fumonisins. The actual maize used to prepare the tortillas was not available for analysis; however, based on the results of the present study, the levels of FB₁ in the unprocessed maize would have had to be >20 µg (total fumonisins)/g maize to have 10 µg/g in the cooked tortillas. Levels of FB₁ of 20 µg/g in maize are uncommon in commercial maize (3); thus the fact that 66% of the tortillas from Santa Maria de Jesus contained 10 µg/g total fumonisins indicates that the quality of the maize used to prepare tortillas is at times exceedingly poor.

There are two results from the 1999 report (8) that cannot be explained easily in light of the findings of the present study. First, the tortillas from the 1999 study (8) contained predominantly HFB₁, whereas in the present study, the levels of HFB₁ and FB₁ (on a molar basis) in tortillas are approximately equivalent (Fig. 1). Second, the nixtamal in the earlier study (8) contained predominantly FB₁, whereas in the present study, the ratio of HFB₁ to FB₁ (on a molar basis) in the masa (1.04 ± 0.39) was similar to the ratio in the tortillas after cooking. It was suggested by Meredith et al. (8) that perhaps the conversion of FB₁ to HFB₁ occurred during cooking of the tortillas, but this contention is not supported by the results of the present study or other studies (6,7) where it is the boiling of the maize in lime water that appears to be responsible for the conversion of FB₁ to HFB₁. The only plausible explanations for the findings in the earlier study of Meredith et al. (8) are that the tortilla samples were mishandled before analysis (i.e., microbial decomposition during shipment or storage) or that the process of nixtamalization as practiced in Mayan communities can be highly variable, leading to highly variable results. Of the 50 household samples collected in 1995 (8), only frozen samples were analyzed. Thus, microbial activity during shipping or storage contributing to the high levels of HFB₁ is unlikely. In 1995, Santa Maria de Jesus experienced a water shortage that resulted in water rationing (8). If the amount of water used for alkaline treatment (boiling and steeping) had been reduced and washing steps omitted, then much higher levels of HFB₁ might be expected in the cooked tortillas.

Regardless of the reason for the high levels of HFB₁ in tortillas in the earlier study, the results of the present study show clearly that the process of nixtamalization as practiced by Mayan communities under optimal conditions (adequate water) can effectively reduce the level of total fumonisins in cooked tortillas to a degree similar to that seen in studies using commercial or pilot-scale processes. In addition, the biological activity of the acetonitrile/water extract of the cooked tortillas was reduced relative to extracts of the uncooked maize based on the elevation in sphinganine, which is closely correlated with fumonisin toxicity in vitro (13) and in vivo (1). Furthermore, boiled maize foods such as porridge (Africa) or polenta (Italy) have been shown to reduce FB₁ by 23 and 8%, respectively (14), whereas boiling plus alkali treatment in this study reduced the total fumonisins by 50%, and 50% of the total fumonisins in the tortillas was present as hydrolyzed fumonisins. In other studies, even greater reductions in total fumonisins were reported (6,7). Given greater reduction in total fumonisins through alkali treatment and the fact that hydrolyzed fumonisins are less toxic in both rats (15) and mice (16) than the parent compounds, we hypothesize that at a given level of FB₁ contamination of maize, nixtamalized tortillas will be (on a gram for gram basis) a safer product than boiled maize products prepared from the same contaminated maize. This finding is important because fumonisins, including hydrolyzed fumonisins, have been suggested to be potential risk factors for neural tube defects in humans in areas in which consumption of maize products, including tortillas, is high.⁴ Therefore, minimizing fumonisin exposure through appropriate processing at the household level in these areas is an important management strategy for reducing the number of consumers who potentially exceed the recommended PMTDI.

	ACKNOWLEDGMENTS

 
We thank Jency Showker for excellent technical assistance and Faustina de Leiva for hard work and dedication in preparation and cooking of the tortillas.

	FOOTNOTES

 
¹ Presented in abstract form at Society of Toxicology, March 2003, Salt Lake City, UT [Riley, R., Palencia, E., Torres, O., Hagler, W., Meredith, F. & Williams, L. (2003) Fate of fumonisin in maize during nixtamalization and tortilla production by Mayan communities in Guatemala. Toxicol. Sci. 72: 252 (abs.)].

² Supported by U.S. Department of Agriculture Foreign Agricultural Service grant X01–4510-62–751071–4 and a grant from the International Life Sciences Institute of North America.

⁴ Abbreviations used: FB, fumonisin B; HFB, hydrolyzed fumonisin B; NOEL, no observable effect level; OPA, ortho-phthaldialdehyde; PMTDI, provisional maximum tolerable daily intake.

⁵ Workshop on the Role of Fumonisins in Neural Tube Defects, January 2003, Atlanta, Georgia (Marasas, W.F.O., Riley, R. T., Hendricks, K. A., Stevens, V. L., Sadler, T. W., Gelineau-van Waes, J., Missmer, S. A, Cabrera Valverde, J., Torres, O. L., Gelderblom, W.C.A., Allegood, J., Martínez de Figueroa, A. C., Maddox, J., Miller, J. D., Starr, L., Sullards, C., Roman Trigo, A. V., Voss, K. A., Wang, E. & Merrill, A. H., Jr. Fumonisins disrupt sphingolipid metabolism, folate transport, and development of neural crest cells in embryo culture and in vivo: A potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize).

Manuscript received 11 June 2003. Initial review completed 18 June 2003. Revision accepted 5 July 2003.

	LITERATURE CITED

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

1. Marasas, W.F.O., Miller, J. D., Riley, R. T. & Visconti, A. (2000) Environmental Health Criteria 219: Fumonisin B₁, International Programme on Chemical Safety 2000 United Nations Environmental Programme, the International Labour Organization and the World Health Organization Geneva, Switzerland.

2. IARC (2002) Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. IARC Monographs on the Evaluation of Carcinogenic Risks of Chemicals to Humans 82:275-366 IARC Press Lyon, France.

3. Bolger, M., Coker, R. D., Dinovi, M., Gaylor, D., Gelderblom, W.F.O., Paster, N., Riley, R. T., Shephard, G. & Speijers, G. A. (2001) Fumonisins. Safety Evaluation of Certain Mycotoxins in Food. Food and Agriculture Organization of the United Nations, paper 74. 2001:103-279 World Health Organization Food Additives Series 47.

4. Bressani, R. (1990) Chemistry, technology, and nutritive value of maize tortillas. Food Rev. Int. 6:225-264.

5. Saunders, S. D., Meredith, F. I. & Voss, K. A. (2001) Control of fumonisin: effects of processing. Environ. Health Perspect. 109:333-336.

6. Dombrink-Kurtzman, M. A., Dvorak, T. J., Barron, M. E. & Rooney, L. W. (2000) Effect of nixtamalization (alkaline cooking) on fumonisin-contaminated corn for production of masa and tortillas. J. Agric. Food Chem. 48:5781-5786.[Medline]

7. Voss, K. A., Poling, S. M., Meredith, F. I., Bacon, C. W. & Saunders, D. S. (2001) Fate of fumonisins during the production of fried tortilla chips. J. Agric. Food Chem. 49:3120-3126.[Medline]

8. Meredith, F. I., Torres, O. R., Riley, R. T. & Merrill, A. H., Jr (1999) Fumonisin B₁ and hydrolyzed fumonisin B₁ levels in nixtamalized maize (Zea mays L.) and tortillas from two different geographical locations in Guatemala. J. Food Prot. 62:1218-1222.[Medline]

9. Meredith, F. I., Bacon, C. W., Plattner, R. D. & Norred, W. P. (1996) Preparative LC isolation and purification of fumonisin B₁ from rice culture. J. Agric. Food Chem. 44:195-198.

10. Plattner, R. D. & Branham, B. E. (1994) Labeled fumonisin: production and use of fumonisin B₁ containing stable isotopes. J. Assoc. Off. Anal. Chem. Int. 77:525-532.

11. Poling, S. M. & Plattner, R. D. (1999) Rapid purification of fumonisins B₁, B₂, B₃, and their hydrolyzed products with solid-phase extraction columns. J. Agric. Food Chem. 47:2344-2349.[Medline]

12. Riley, R. T., Norred, W. P., Wang, E. & Merrill, A. H., Jr (1999) Alteration in sphingolipid metabolism: bioassay for fumonisin- and ISP-I-like activity in tissues, cells, and other matrices. Nat. Toxins 7:407-414.[Medline]

13. Yoo, H.-S., Norred, W. P., Showker, J. L. & Riley, R. T. (1996) Elevated sphingoid bases and complex sphingolipid depletion as contributing factors in fumonisin-induced cytotoxicity. Toxicol. Appl. Pharmacol. 138:211-218.[Medline]

14. Shephard, G. S., Leggott, N. L., Stockenstrom, S., Somdyala, N.I.M. & Marasas, W.F.O. (2002) Preparation of South African maize porridge: effect on fumonisin mycotoxin levels. South African J. Sci. 98:393-396.

15. Voss, K. A., Riley, R. T., Bacon, C. W., Meredith, F. I. & Norred, W. P. (1998) Toxicity and sphinganine levels are correlated in rats fed fumonisin B₁ or hydrolyzed FB₁. Environ. Toxicol. Pharmacol. 5:101-104.

16. Howard, P. C., Couch, L. H., Patton, R. E., Eppley, R. M., Doerge, D. R., Churchwell, M. I., Matilde Marques, M. & Okerberg, C. V. (2002) Comparison of the toxicity of several fumonisin derivatives in a 28-day feeding study with female B6C3F₁ mice. Toxicol. Appl. Pharmacol. 185:153-165.[Medline]

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