J. Dairy Sci. 2007. 90:4718-4723. doi:10.3168/jds.2007-0286
© 2007 American Dairy Science Association ®
Effects of Corn Silage Derived from a Genetically Modified Variety Containing Two Transgenes on Feed Intake, Milk Production, and Composition, and the Absence of Detectable Transgenic Deoxyribonucleic Acid in Milk in Holstein Dairy Cows
S. Calsamiglia*,1,
B. Hernandez*,
G. F. Hartnell
and
R. Phipps
* Dpto. Ciència Animal i dels Aliments, Universitat Autónoma de Barcelona, 08193-Bellaterra, Spain
Monsanto Company, St. Louis, MO 63167
Centre for Dairy Research, School of Agriculture, Policy and Development, The University of Reading, RG6 6AR, UK
1 Corresponding author: Sergio.Calsamiglia{at}uab.es
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ABSTRACT
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The objectives were to compare the chemical composition, nutritive value, feed intake, milk production and composition, and presence in milk of transgenic DNA and the encoded protein Cry1Ab when corn silages containing 2 transgenes (2GM: herbicide tolerance: mepsps and insect resistance: cry1Ab) were fed as part of a standard total mixed ration (TMR) compared with a near isogenic corn silage (C) to 8 multiparous lactating Holstein dairy cows in a single reversal design study. Cows were fed a TMR ration ad libitum and milked twice daily. Diets contained [dry matter (DM) basis] 45% corn silage, 10% alfalfa hay, and 45% concentrate (1.66 Mcal of net energy for lactation/kg of DM, 15.8% crude protein, 35% neutral detergent fiber, and 4.1% fat). Each period was 28-d long. During the last 4 d of each period, feed intake and milk production data were recorded and milk samples taken for compositional analysis, including the presence of transgenic DNA and Cry1Ab protein. There was no significant difference in the chemical composition between C and 2GM silages, and both were within the expected range (37.6% DM, 1.51 Mcal of net energy for lactation/kg, 8.6% crude protein, 40% neutral detergent fiber, 19.6% acid detergent fiber, pH 3.76, and 62% in vitro DM digestibility). Cows fed the 2GM silage produced milk with slightly higher protein (3.09 vs. 3.00%), lactose (4.83 vs. 4.72%) and solids-not-fat (8.60 vs. 8.40%) compared with C. However, the yield (kg/d) of milk (36.5), 3.5% fat-corrected milk (34.4), fat (1.151), protein (1.106), lactose (1.738), and solids-not-fat (3.094), somatic cell count (log10: 2.11), change in body weight (+7.8 kg), and condition score (+0.09) were not affected by type of silage, indicating no overall production difference. All milk samples were negative for the presence of transgenic DNA from either trait or the Cry1Ab protein. Results indicate that the 2GM silage modified with 2 transgenes did not affect nutrient composition of the silages and had no effect on animal performance and milk composition. No transgenic DNA and Cry1Ab protein were detected in milk.
Key Words: genetically modified silage • stacked gene • milk production • DNA detection
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INTRODUCTION
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Since 1997, the agricultural area dedicated to genetically modified (GM) crops has increased from 4 to 102 million ha in 2006 (James, 2006). Soybeans, corn, cotton, and rapeseed have been modified for agronomic input traits such as herbicide tolerance or insect protection and are now widely used in livestock production systems as whole crop such as corn silage, or as specific crop components or coproducts such as corn grain or oilseed meals. Recently, crops containing stacked genes providing herbicide tolerance and insect protection in the same variety are becoming more widely used in crop production (James, 2006) and in livestock feeds (Taylor et al., 2005). The procedures for the safety and nutritional assessment of GM crops have been widely documented (EFSA, 2004) and extensively reviewed (Chesson, 2001; Kuiper et al., 2001; Cockburn, 2002). The starting point of the comparative assessment for their safety and nutritional assessment includes an agronomic, phenotypic, and compositional comparison with the near isogenic nonGM variety and a number of commercial varieties. However, hypothetical safety concerns, including the potential for introduced transgenic DNA, the protein encoded by the transgene, or both, to be transferred to animal-derived products intended for human consumption, need to be addressed. Although the World Health Organization (FAO/WHO, 1991) stated that, given the long history of safe consumption of DNA and the numerous studies with a wide range of livestock studies conducted to determine if fragments of transgenic DNA or their encoded protein were present in the digestive tract of livestock and in foods such as milk, meat, and eggs, the consumption of DNA from all sources—including GM plants—was safe and did not produce a risk to human health. These studies, which had been conducted using GM varieties modified for a single trait, have recently been reviewed (Flachowsky et al., 2005; Phipps et al., 2006). Whereas both authors concluded that the detection of DNA in milk, meat, and eggs is likely to be a function of the abundance of the gene, the size of the fragment of DNA being tested for, and the sensitivity of the analytical methods, food products derived from animals receiving GM crops were considered to be as safe as those derived from animals fed conventional feeds.
Although published literature has so far focused on GM varieties containing a single transgene, a very recent publication by Singhal et al. (2006) compared the composition and subsequent performance of crossbred dairy cattle in India when they received, as part of their diet, cotton seed derived from a conventional variety with a GM variety containing 2 transgenes (Cry1Ac and Cry2Ab). The authors established that the composition of the cotton seeds was similar and that there was no significant difference in feed intake and milk production of the crossbred dairy cows, and that the protein encoded by the 2 transgenes could not be detected in blood or milk. With the exception of this very recent publication, no comparable studies to those conducted with GM varieties modified with a single gene have been published in which high-yielding Holstein cows received diets containing a GM variety modified with 2 transgenes.
The objective of the current study was to compare the chemical composition, nutritive value, feed intake, and milk production and composition of high yielding Holstein dairy cows fed a TMR containing corn silage derived from a GM variety modified with 2 transgenes (herbicide tolerance: mepsps and insect resistance: cry1Ab) to that obtained with its near-isogenic non-GM counterpart, and to determine if transgenic DNA from either transgene or the encoded protein (Cry 1Ab) could be detected in milk. The transgenic mepsps protein is difficult to differentiate from the endogenous mepsps found in corn, and therefore it was not part of the objective.
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MATERIALS AND METHODS
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Crop and Silage Production
Corn crop from nongenetically modified (corn variety DK 493, lot 1760R4F) and genetically modified (2GM: DK493RR/Bty, lot 1746AIIX) corn was planted in Lleida, Spain. The crops were harvested, processed, and transported in different trucks from the field to the Animal Experimental Service of the Universitat Autonoma de Barcelona (Barcelona, Spain). Upon arrival, a 1.5-kg representative sample of each crop was obtained as the truck was being unloaded and analyzed for nutrient composition (Dairy One, Ithaca, NY) and for positive confirmation of the control and the GM product using lateral flow strips for the Cry1Ab protein (Strategic Diagnostics, Newark, NJ). The freshly chopped corn was packed in 2 different AgBags the same day of harvesting using a Rotopress bagger (Rotopress, Sioux Center, IA). Appropriate measures were taken during harvest, processing, and storage of silages to avoid potential cross contamination. On opening the silage bags, a 1-kg representative sample was taken from each silo for mycotoxin and nutrient analysis. Samples of corn silage were taken daily during the lactation trial, composited within period and treatment, and frozen until analysis. Samples were analyzed for nutrient content (DM, NDF, ADF, acid detergent lignin (ADL), CP, fat, ash, Ca, P, Na, K, and Mg), in vitro digestibility, gas production, pH, ammonia N, and soluble N.
Lactation Trial
The lactation trial was conducted at the Field and Animal Experimental Service of the Universidad Autonoma de Barcelona (Bellaterra, Spain). The dairy barn unit is a 9 tie-stall barn with individual feedbunks. The study included 8 midlactation Holstein dairy cattle in their second or greater lactation with an average of 126 d in milk, 647 kg of BW, and 2.79 BCS (1 to 5 scale) at the start of the trial. All cows were in good health. Cows were fed total mixed diets containing corn silage formulated to meet or exceed the US National Research Council current requirements for lactating dairy cattle (NRC, 2001). In the second period, an additional 100 g/head per day of sodium bicarbonate and 50 g/head per day of magnesium oxide were added to the ration to prevent potential subclinical acidosis. Diets were formulated to contain the same amount of corn silage DM in both treatments. Feed and water was offered ad libitum. Cattle were turned out for exercise in a dry lot for about 2 h/d where they had access to water but not feed. Animals were milked twice daily (0800 and 1900 h) and observed daily for any health-related incidences.
The study was a single reversal design with 8 lactating multiparous Holstein-Friesian cows and 2 treatments. Each square was replicated 4 times, so a total of 8 animals were used. Cows were blocked into 4 groups based on DIM and mean daily milk yield recorded in d –4 to –2 prior to the initiation of the experiment. Each block of 2 cows was assigned to a square. Cows in each square were randomly assigned to treatments for the first period the day prior to the initiation of the trial and then switched to the other treatment in period 2. Each of the 2 periods was 28 d in duration. The first 24 d of each period were used for adaptation to treatments, and d 24 to 28 were used to collect data and samples.
During d 1 to 24 of each period the quantity of feed offered and refused was recorded daily from Monday through Friday. During d 25 to 28 of each period, the quantity of feed offered and refused was recorded daily. Corn silage samples were collected weekly for DM determination and rations adjusted weekly to accommodate any variation. Corn silage, the mixture of remaining dietary ingredients, and the TMR were sampled on a daily basis and composited within period and treatment of nutrient content analysis (DM, NDF, ADF, ADL, CP, fat, ash, Ca, P, Na, K, and Mg).
At initiation of the study and on d 28 of each period, animals were weighed and condition scored using the 5-point system (Edmonson et al., 1989). Body condition scoring was done independently by the same 2 people over the course of the study. Individual milk yields were hand-recorded after each milking throughout the experiment. Milk samples were obtained from a proportional automatic sampler. Consecutive p.m. and a.m. milk samples were collected during d 24 to 28 of each period and were analyzed for fat, protein, SNF, lactose, and SCC. In addition, 32 samples (2 milk samples from each period per cow taken during the p.m. milking of d 24 and the a.m. milking of d 25 of each period) were taken aseptically for the analysis of the transgenic DNA and Cry1Ab-protein, and stored frozen until analysis.
Chemical Analyses
Dry matter of silages was determined by drying samples at 65°C for 48 h. The NDF, ADF, and ADL were analyzed sequentially by the Van Soest et al. (1991) method using heat-resistant amylase and sodium sulfite. Crude protein, ether extract, and ash were determined following AOAC procedures (2000). Aflatoxin content was determined by thin layer chromatography (AOAC, 2000). Mineral content of silages, the concentrate mix, and TMR were determined by atomic absorption spectrophotometry. Rumen DM digestibility and gas production of silages were determined in vitro (Theodorou et al., 1994). Milk analysis was carried out with a Milkoscan (Milkoscan model 4000, Foss Electric, Hillerød, Denmark). Energy content of feeds was calculated with the NRC (2001) computer model at the actual milk production and DM intake level.
Milk samples for DNA and Cry1Ab-protein were processed in duplicate by GeneScan (Freiburg, Germany). The DNA was extracted and tested using p35S and MON 810 PCR specific assays (Nemeth et al., 2004). Milk samples for the Cry1Ab-protein were thawed in a 50°C water bath and heated to 40°C. The samples were vortexed and then centrifuged at ambient temperature (sample temperature 
40°C) at 3,000 x g for 10 min. After centrifugation, the tubes were cooled in ice water for 10 min. The solidified fatty top layer was pierced, and an aliquot of the skim milk was transferred to a fresh tube or microtiter/deepwell plate. The 6 Bt Maize Test Kit (Strategic Diagnostics Inc., Newark, DE) was used according to the manufacturers instruction (Bt Maize Kit User’s Guide Reference 3099983).
Statistical Analyses
Data for BW and condition scores were analyzed using the Proc GLM of SAS (Version 8.00, SAS Inst. Inc., Cary, NC). The rest of production data were analyzed using a mixed model for repeated measures of SAS using the compound symmetric structure of variance. Treatment, period, and day were considered fixed factors, and the cow random factor. The model was
Treatment means are reported as least squares means with the associated standard error of the difference between treatments. Significant differences were declared at P < 0.05.
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RESULTS AND DISCUSSION
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Nutrient Composition of Corn Plant and Silages
Analysis of samples of the fresh crop plant confirmed that the control silage was negative for the presence of Cry1Ab protein, and the 2GM fresh crop plant was positive to the presence of Cry1Ab protein, and no cross contamination occurred. Chemical composition of the fresh corn crops, corn silages, and TMR (Tables 1
and 2) were within expected ranges and similar between treatments. The test for aflatoxins B1, B2, G1, and G2 were all negative at the opening of control and 2GM silos. In vitro DM digestion, gas production, ammonia, and total soluble N were similar between silage types and within normal ranges (Table 1). Sidhu et al. (2000) compared chemical composition of 5 comercial glyphosate-tolerant corn hybrids and concluded that, except for few small differences with no biological significance, nutrient content was similar to nonglyphosate tolerant corn. Faust (1999) and Faust and Spangler (2000) compared nutrient composition, important feeding-related characteristics, and in vitro digestion of DM of insect-resistant (Bt) corn compared with near-isogenic hybrids and concluded that both had similar feeding values. Similar results have been observed by other reports on glyphosate-tolerant corn (Petty et al., 2001; Donkin et al., 2003) and Bt corn (Barriere et al., 2001; Donkin et al., 2003). Although the combined modification 2GM has not been tested previously in dairy cows, results from the present study agree with previous observations with the single trait modifications and indicate that the 2GM silage had similar chemical composition and nutritional value as compared with the near-isogenic corn silage.
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Table 1. Chemical composition (% of DM) of the fresh chopped corn and chemical composition and fermentation profiles of control and genetically modified (2GM) silages
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Lactational Performance
The effects of silage type on production performance are presented in Table 3. Silage type did not affect (P > 0.05) DMI (average of 22.1 kg/d). Cows fed the 2GM produced milk with higher (P < 0.05) milk protein (3.00 vs. 3.09%), lactose (4.72 vs. 4.83%), and SNF (8.40 vs. 8.60%) content when compared with control. However, the total yield (kg/d) of milk (average of 36.5), 3.5% FCM (average of 34.4), fat (average of 1.151), protein (average of 1.106), lactose (average of 1.738), and SNF (average of 3.093), as well as SCC (average of 2.11 log SCC) were not affected by type of silage. Treatments did not affect the change in BW (average of +7.8 kg) and condition score (average of +0.09 units). A number of studies have now been conducted comparing GM crops, which have been modified though the insertion of one transgene with appropriate counterparts. For example, Faust and Miller (1997) and Folmer et al. (2000) found no differences in feed intake, milk production, milk composition, and milk component yields between cows fed Bt corn and non-Bt near-isogenic hybrids. Similar results were reported by Grant et al. (2003) when a different Bt protein (Cry3Bb1) was fed. Barriere et al. (2001) compared Bt corn vs. non-Bt near-isogenic corn in lactating dairy cattle and observed that cows fed the Bt corn had higher DM intake, but milk production and composition were not affected. Donkin et al. (2003) reported no effect of glyphosate-tolerant corn vs. near-isogenic hybrids on DMI or milk production and composition. Similar results were reported by Ipharraguerre et al. (2003) and Grant et al. (2003). In the current study, there are no obvious nutritional reasons that justify the higher protein, lactose, and SNF concentrations. However, because milk production was numerically lower, and milk component yields were similar between treatments, the increased milk component concentrations may be attributed to the inverse relationship between milk yield and milk component concentration (Brun-Bellut et al., 1984).
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Table 3. Dry matter intake, milk production, and composition and BW change in dairy cows fed control and genetically modified (2GM) corn silage
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The results from the current study are the first on the use of a GM corn modified with 2 stacked genes in lactating dairy cattle. However, the results from the chemical composition and production responses indicate that the use of the 2GM silage did not adversely affect animal performance and are indeed similar to the studies using GM crops modified with only one transgene.
The milk DNA was successfully extracted from all samples submitted for analysis, and all were found to be negative for the CaMV 35S promoter and the MON 810 (cry1Ab) genes. Thus, the transgenic DNA or fragments thereof were not detected in the milk of cows fed the silage containing the mepsps and cry1Ab genes. In previous studies in which transgenic Bt corn was fed to different animals, transgenic Bt DNA was not detected in meat from pigs (Weber and Richert, 2001), in blood, liver, and muscle from broilers (Anonymous, 2001; Deaville and Maddison, 2005), in milk samples from dairy cows (Phipps et al., 2001, 2002, 2003), or in beef or dairy organs (Jennings et al., 2003). Using the p35S PCR assay, Nemeth et al. (2004) also reported no detection of transgenic DNA fragments in muscles samples from steers, broiler chickens, and swine or in milk from dairy cows.
The test for the presence of the Cry1Ab-protein encoded in the GM modified corn had a limit of detection of 0.1 ng/mL. All milk samples were negative to the presence of the Cry1Ab-protein. Transgenic proteins have not been detected in animal products from animals fed transgenic corn (Anonymous, 2001; Weber and Richert, 2001; Ash et al., 2003).
When Clark and Ipharraguerre (2001) reviewed published data, they concluded that once the comparative assessment had established that the composition of the GM variety was comparable with that of the appropriate counterparts, then nutritional comparability could be assumed. Flachowsky and Aulrich (2001) concluded that, under these circumstances, feeding trials with livestock animals added little to the overall safety and nutritional evaluation of GM crops with agronomic input traits. A series of studies conducted by Taylor et al. (2003a,b,c, 2004a,b,c, 2005) with GM corn varieties with stacked traits fed to broiler chicken, and results from the present experiment would strongly suggest that the same conclusion can be applied to stacked genes.
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CONCLUSIONS
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The nutrient composition of 2GM fresh corn plants, and nutrient composition and in vitro fermentation of the 2GM corn silage, were not different from the near isogenic control. Feeding the 2GM corn silage to lactating dairy cattle did not affect milk fat concentration and SCC but increased the content of milk protein, lactose, and SNF. Feeding the 2GM corn silage to lactating dairy cattle did not affect DM intake, and the yield of milk, FCM, fat, protein, lactose, and SNF. Transgenic DNA from corn containing mepsps and cry1Ab genes, or the Cry1Ab-protein encoded in the 2GM corn silage were not detected in milk from cows fed the GM corn silage.
Received for publication April 16, 2007.
Accepted for publication May 4, 2007.
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ABSTRACT
INTRODUCTION
