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Poult Sci 2006. 85:1795-1797
© 2006 Poultry Science Association
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PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION: Research Notes

Evaluation of Corn Furan Fatty Acid Putative Endocrine Disruptors on Reproductive Performance in Adult Female Chickens

K. W. Wilhelms*,{dagger}, G. A. Kraus*,§, J. D. Schroeder§, J. W. Kim§, S. A. Cutler{dagger}, M. A. Rasmussen||, L. L. Anderson{dagger},{ddagger},1 and C. G. Scanes*,{dagger},{ddagger}

* Interdepartmental Toxicology Program, {dagger} Department of Animal Science, {ddagger} Department of Biomedical Sciences, and § Department of Chemistry, Iowa State University, Ames 50011; and || National Animal Disease Center, USDA-ARS, Ames, IA 50010

1 Corresponding author: llanders{at}iastate.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Based on evidence from rodent models, it was hypothesized that furan fatty acids found in corn would inhibit reproduction in the laying hen. An isomeric mixture of furan fatty acids [9, (12)-oxy-10,13-dihydroxystearic acid and 10, (13)-oxy-9,12-dihydroxystearic acid] was administered for a period of 3 wk via the diet (1 and 3 ppm) at levels greater than those in corn to 20-wk-old pullets. There were no overt indications of acute or chronic toxicity (no effects on mortality, feed intake, or average daily gain). Similarly, there was no dose-dependent effect on reproductive parameters [egg production, egg weight, shell thickness, ovarian weight, number or weight of large yolky preovulatory follicles, and number of small yellow follicles (4–8 mm in diameter)]. The present data do not suggest that furan fatty acids are a cause of concern to the poultry industry.

Key Words: corn furan fatty acid • endocrine disruptor • egg production • chicken


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
For over the past decade, there has been increasing attention focused on endocrine disruption. A wide range of chemicals has been classified as putative endocrine disruptors, natural or synthetic compounds that mimic, enhance, or inhibit endogenous hormones (Boorgeest et al., 2002). These include the soy isoflavones and other plant compounds (Kurzer and Xu, 1997), many pesticides (Cooper et al., 1999), and industrial plasticizers (Casajuana and Lacorte, 2004), among others.

For many years, there has been evidence that corn-based products possess compounds with the ability to alter growth and reproductive states (Dam et al., 1959; Booth et al., 1960). Recently, putative endocrine disruptors derived from linoleic acid were discovered in corncob animal beddings (Markaverich et al., 2002a,b). These chemicals have been identified as an isomeric mixture of 9, (12)-oxy-10,13-dihydroxystearic acid and 10, (13)-oxy-9,12-dihydroxystearic acid furan fatty acids. These chemicals possess mitogenic activity in treated MCF-7 human breast cancer cells (Markaverich et al., 2002a). Furthermore, they have the ability to block progression of the estrous cycle (Markaverich et al., 2002a,b), to initiate persistent metestrus, and to reduce mating behavior in Sprague-Dawley rats (Schettler, 2003). However, they possess no detectable estrogenic or antiestrogenic activities (Markaverich et al., 2002a,b).

There is newfound concern about the putative endocrine disruptor effect of these compounds on reproduction, as corn-based products are a staple of many human, livestock, and experimental animal diets (Schettler, 2003). The present study examined the ability of furan fatty acids to inhibit reproductive development, egg production, and ovarian functioning in the hen.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Birds
All procedures were approved by the Iowa State University Committee on Animal Care (protocol 8-03-5498-G). White Leghorn pullets (19 wk old) from Sparboe Farms (Litchfield, MN) that had previously been on a short photoperiod of 10 h of light per day were used. The treatments were initiated 1 wk after the birds arrived at Iowa State University. At that time, they were on a light period of 14 h per day. By the beginning of the feeding trial, all birds were in lay. Birds were weighed and randomly placed individually into cages (30.5 x 40.5 x 44 cm) with a feeder supplying feed to 3 adjacent cages. The basal diet (ground corn, 566.7 g/kg; soybean meal (48% CP), 265.0 g/kg; animal and vegetable fat blend, 36.5 g/ kg; DL-Met, 2.5 g/kg; dicalcium phosphate, 22.3 g/kg; limestone, 81.0 g/kg; oyster shell, ground 15.0 g/kg; NaCl (iodized), 5.0 g/kg; trace mineral premix, 3.0 g/kg; vitamin premix, 3.0 g/kg) was formulated to meet NRC requirements (NRC, 1994) and mixed at the Iowa State University Poultry Research Center. The concentrations of Ca and nonphytate P were, respectively, 4.22 and 0.52%. All ingredients were obtained from Archer-Daniels-Midland Co. (Decatur, IL) or local suppliers. Feed and water were available ad libitum. A long day length (14L:10D) was imposed to bring the birds into full reproduction.

Experimental Design and Treatments
It was hypothesized that furan fatty acids would inhibit reproductive development in female poultry. There were 3 treatments of furan fatty acid in the diet added at the following concentrations: 0, 1, or 3 ppm. The highest dose was estimated to meet the concentration reported as having reproductive effects in rats (Casajuana and Lacorte, 2004). Blocks of 3 cages each containing 1 pullet were randomly assigned to 1 of 3 treatments, with 9 replicate cages/birds per treatment or 3 replicate blocks of cages/ treatment. The furan fatty acid mixture was added directly into the basal diet using 0.12 mL/kg of ethanol as a vehicle. The diets were mixed for 20 min and then stored at room temperature throughout the experiment.

Fatty Acid Furan Synthesis
An isomeric mixture of furan fatty acids [9, (12)-oxy-10,13-dihydroxystearic acid and 10, (13)-oxy-9,12-dihydroxystearic acid] was prepared as follows (Moghaddam et al., 1996; Markaverich et al., 2002a). The purity of the synthesized compound was evidenced by proton NMR, by high-resolution mass spectrometry, and by thin-layer chromatography. Results of these analyses are NMR (CDCl3) 0.87 (br t, J = 6 Hz, 3 H), 1.15 to 1.70 (m, 22 H), 1.78 to 2.21 (m, 2 H), 2.29 to 2.34 (m, 2 H), 3.32 to 3.48 (m, 1 H), 3.68 to 3.80 (m, 1 H), 3.95 to 4.12 (m, 1 H), and 4.20 to 4.32 (m, 1 H). The high-resolution mass spectrometry mass-to-charge ratio for C18H34O5, calculated 330.2406; found 330.2411. Bisepoxide linoleic acids were prepared directly from linoleic acid by epoxidation with metachloroperbenzoic acid in methylene chloride at 0°C. The bisepoxide was purified by column chromatography and then converted into a mixture of dihydroxycarboxylic acids by treatment with an aqueous solution of 70% perchloric acid. The resulting mixture was used in the studies.

Experimental Protocol
At the start of the study, BW were recorded. The chickens were then fed treatment diets ad libitum for 21 d. During this period, feed intake, number of eggs laid, egg weight, and any overt abnormalities were recorded. Shell thickness was also determined (measured at 4 sites on the egg and the mean used in analysis).

On d 21, the hens were weighed and killed by decapitation. Ovary and oviduct weights were determined, as were any reproductive overt abnormalities (atretic follicles, internal eggs). The ovarian follicles were collected. The weight of the F1 to F5 largest follicles were determined, as were the number of large yolky follicles (>8.0 mm in diameter) and the number of small yellow follicles (4 to 8 mm in diameter).

Statistics
The study was analyzed as a randomized design with subsampling. All data were analyzed using PROC MIXED in SAS Version 8.2 (SAS Institute Inc., Cary, NC), with the exception of egg lay. Egg lay was analyzed by binomial and multinomial logistic regression. Values found different were separated using Dunnett’s method. Significance was determined at P ≤ 0.05.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
The study examined the effect of furan fatty acids [an isomeric mixture of 9, (12)-oxy-10,13-dihydroxystearic acid and 10, (13)-oxy-9,12-dihydroxystearic acid present in corn] on reproduction in hens. The furan fatty acids exhibited no acute toxicity, as indicated by the absence of any mortality (0/9 in birds on 0, 1, and 3 ppm furan fatty acids). Similarly, there was no evidence for chronic toxicity, as neither feed intake nor BW gain were affected by the presence of furan fatty acids in the feed (Table 1Go).


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  		Table 1. Effects of dietary furan fatty acids [an isomeric mixture of 9, (12)-oxy-10,13-dihydroxystearic acid and 10, (13)-oxy-9,12-dihydroxystearic acid] on growth and reproductive parameters in laying hens1
 
These furan fatty acids exhibit marked inhibitory effects on reproduction in rodent models when exposed to concentrated extracts and synthesized compounds at a dose of ~0.32 mg/kg per day (Markaverich et al., 2002a; Moghaddam et al., 1996). In contrast, the furan fatty acids had little effect on reproduction in the hen with daily doses of 0.096 and 0.28 mg/kg per day (at 1 and 3 ppm, respectively). For instance, treatment with either 1.0 or 3.0 ppm furan fatty acids did not influence (P > 0.05) any of the following parameters: weights of oviduct, ovary, or large yolky follicles (F1 to F5); number of large yellow follicles (>8.0 mm in diameter); and number of small yellow follicles (4 to 8 mm in diameter; Table 1Go). Moreover, furan fatty acids had no effect on egg production or quality (as indicated by number of yolks and shell thickness) in all weeks of treatment. There were, however, changes in 2 reproductive parameters. As might be expected, there was a decrease (P < 0.05) in shell thickness between the first and second and between the second and third week of lay, irrespective of furan fatty acid treatment.

In summary, furan fatty acids at concentrations above those found in corn (Markaverich et al., 2002a) have no overt toxicity and little acute effect on reproduction in the layer hen. It is unclear whether effects may be observed if administered over a longer period or at higher doses.


   ACKNOWLEDGMENTS
 
This study was supported by Iowa Agricultural and Home Economics Experiment Station and by a Cooperative Agreement from the USDA Agricultural Research Service (no. 58-3625-4147). We gratefully acknowledge the statistical advice from David F. Cox and Cory Heilmann (Iowa State University, Department of Statistics).

Received for publication March 13, 2006. Accepted for publication May 25, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Boorgeest, C., C. Greenfield, D. Tomic, and J. Flaws. 2002. The effects of endocrine disrupting chemicals on the ovary. Front. Biosci. 7:d1941–d1948.[ISI][Medline]

Booth, A., E. Bickoff, and G. Kohler. 1960. Estrogen-like activity in vegetable oils and mill by-products. Science 131:1807–1808.[Abstract/Free Full Text]

Casajuana, N., and S. Lacorte. 2004. New methodology for the determination of phthalate esters, bisphenol A, bisphenol A diglycidyl ether, and nonylphenol in commercial whole milk samples. J. Agric. Food Chem. 52:3702–3707.[ISI][Medline]

Cooper, R., J. Goldman, and T. Stoker. 1999. Neuroendocrine and reproductive effects of contemporary-use pesticides. Toxicol. Ind. Health 15:26–36.[Abstract/Free Full Text]

Dam, R., R. Leach Jr., T. Nelson, L. Norris, and F. Hill. 1959. Studies on the effect of quantity and type of fat on chick growth. J. Nutr. 68:615–632.[Abstract/Free Full Text]

Kurzer, M., and X. Xu. 1997. Dietary phytoestrogens. Annu. Rev. Nutr. 17:353–381.[ISI][Medline]

Markaverich, B., M. Alejandro, D. Markaverich, L. Zitzow, N. Casajuna, N. Camarao, J. Hill, K. Bhirdo, R. Faith, J. Turk, and R. Jan. 2002a. Identification of an endocrine disrupting agent from corn with mitogenic activity. Biochem. Biophys. Res. Commun. 291:692–700.[ISI][Medline]

Markaverich, B., S. Mani, M. Alejandro, A. Mitchell, D. Markaverich, T. Brown, C. Velez-Trippe, C. Murchison, B. O’Malley, and R. Faith. 2002b. A novel endocrine-disrupting agent in corn with mitogenic activity in human breast and prostatic cancer cells. Environ. Health Perspect. 110:169–177.[ISI][Medline]

Moghaddam, M., K. Motoba, B. Borhan, F. Pinot, and B. Hammock. 1996. Novel metabolic pathways for linoleic and ara-chidonic acid metabolism. Biochim. Biophys. Acta 1290:327–339.[Medline]

National Research Council. 1994. Nutrient Requirements of Poultry. 9th ed. Natl. Acad. Press, Washington, DC.

Schettler, T. 2003. Corn and corn-derived products: Sources of endocrine disruptors. Environ. Health Perspect. 111:A691. (Abstr.)[ISI][Medline]





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