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Nonionophore antibiotics do not affect the trans-18:1 and conjugated linoleic acid composition in beef adipose tissue¹

N. Aldai^*, M. E. R. Dugan^*,2, J. K. G. Kramer, P. S. Mir and T. A. McAllister

^* Agriculture and Agri-Food Canada, Lacombe Research Centre, 6000 C&E Trail, Lacombe, Alberta T4L 1W1, Canada; and Guelph Food Research Centre, 93 Stone Road West, Guelph, Ontario N1G 5C9, Canada; and Lethbridge Research Centre, 1st Avenue South 5403, PO Box 3000, Lethbridge, Alberta T1J 4B1, Canada

	Abstract

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The common practice in North American feedlot industries is to add antibiotics to the diet to prevent disease and improve both BW gain and feed efficiency. In this study, 240 crossbred steer calves were backgrounded on a 54% silage diet for 80 d and fed a finishing diet consisting of 81% barley grain, 10% barley silage, and 7.5% supplement (DM basis) with and without in-feed antibiotics for approximately 120 d. Calves were assigned to 1 of 5 treatments: a control with no antibiotics, 11 mg/kg of chlortetracycline, 44 mg/kg of chlortetracycline, 44 mg/kg of chlortetracycline plus 44 mg/kg of sulfamethazine, and 11 mg/ kg of tylosin phosphate. A combination of GLC and silver-ion HPLC methods was used to analyze the fatty acid composition of brisket adipose tissue, with emphasis on trans-18:1 and CLA isomers. The inclusion of nonionophore antibiotics in the diet had little effect on the fatty acid composition, except that feeding either 44 mg/kg of chlortetracycline or 11 mg/kg of tylosin caused small increases in 9c-14:1 and 16:0 relative to the control (0.26 and 0.9 g/100 g of total fatty acids, respectively). Likewise, profiles of trans-18:1 and CLA isomers were unchanged by antibiotics, but across treatments the predominant trans-18:1 isomer was 10t-18:1 (where t = trans; 3.22%) at 3 times the concentration of the second most abundant isomer (11t-18:1; vaccenic acid, 1.05%). Rumenic acid (9c,11t-18:2, where c = cis) was the major CLA isomer at 61% of total CLA, followed by 7t,9c-18:2 at 9%. Because no other effects on fatty acid composition were evident, data for trans-18:1 and CLA were pooled across treatments to investigate possible relationships among rumen PUFA metabolites. The total trans-18:1 content in brisket adipose tissue was positively correlated with 10t-18:1, but not with 11t-18:1, whereas the total CLA was positively correlated with 9c,11t-18:2, but not with 7t,9c-18:2. The 7t,9c-18:2 was, however, positively correlated with 10t-18:1 and 6t/7t/8t-18:1 but was negatively correlated with rumenic acid. These metabolic interrelationships suggest the presence of bacterial populations with distinct pathways for PUFA biohydrogenation in which either 10t-18:1 or 11t-18:1 predominate. Overall, the nonionophore antibiotics tested did not appreciably change adipose tissue composition and consequently could not be used to improve the trans-18:1 or CLA profile (i.e., increase vaccenic and rumenic acids at the expense of 10t-18:1).

Key Words: adipose tissue • antibiotic • beef • conjugated linoleic acid • trans-18:1

	INTRODUCTION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Antimicrobial agents have been used in beef cattle production since the 1950s for the prevention of disease and as growth promoters (Gustafson and Bowen, 1997; Witte, 1998). Some antimicrobials inhibit lipolysis (Van Nevel and Demeyer, 1995), whereas others inhibit the growth of certain bacteria (Russell and Strobel, 1989). The effects of only a few antimicrobials on beef fatty acid composition have, however, been investigated, despite the important role rumen microflora could play in defining lipid patterns (Cruz-Hernandez et al., 2006). Monensin appears to have been the most studied antimicrobial, and under in vitro conditions monensin increases total trans-18:1, specifically 10t-18:1 (where t is trans), and the main CLA isomer, 9c,11t-18:2 (where c is cis), in rumen fluid (Fellner et al., 1997; Jenkins et al., 2003; Wang et al., 2005). Adding monensin to the diets of steers (Marmer et al., 1985), sheep (Zhang et al., 2006), and dairy cows (Sauer et al., 1998; Eifert et al., 2006) also increased concentrations of total trans-18:1 and CLA in the rumen fluid, meat, plasma, and milk lipids, but only Eifert et al. (2006) reported a partial trans-18:1 isomer composition.

Biohydrogenation products of PUFA [i.e., rumenic acid (9c,11t-18:1) and its precursor, vaccenic acid (11t-18:1)] have been intensively investigated because of the finding that rumenic acid has purported roles in the prevention and possible treatment of several diseases, including diabetes, obesity, and some types of cancer (Belury, 2002; Ip et al., 2003). Some of the trans-18:1 isomers (notably 9t-18:1 and 10t-18:1) have, however, been shown to be associated with negative plasma lipid and lipoprotein profiles (Hodgson et al., 1996; Bauchart et al., 2007; Roy et al., 2007), and we recently reported that the predominant trans-18:1 isomer in subcutaneous fat from cattle fed a high barley grain diet was 10t-18:1 (Dugan et al., 2007). Because changes in rumen conditions can affect the composition and activity of rumen bacteria, the present work was undertaken to determine whether commonly used antimicrobials, other than monensin (i.e., chlortetracycline alone, chlortetracycline and sulfamethazine in combination, and tylosin) would alter the fatty acid composition of beef subcutaneous fat, with emphasis on the content or composition of individual trans-18:1 and CLA isomers.

	MATERIALS AND METHODS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
All animals involved in this study were cared for according to the guidelines set out by the Canadian Council of Animal Care (1993). Animals used in this work were part of a study investigating the nature of nonionophore antibiotic resistance throughout the farm to food continuum.

Animals and Treatments

A total of 240 crossbred steer calves (198 ± 20 kg of initial BW) were used in this study, conducted at the Lethbridge Research Centre experimental feedlot in 24 feedlot pens. Calves originated from the same ranch and did not receive any dietary antimicrobials before the initiation of the experiment. The calves were randomly assigned to 1 of 5 treatments: 1) control, 2) A11 (11 mg/kg of chlortetracycline from Aureomycin-100 G; Alpharma Inc., Mississagua, Ontario, Canada), 3) A44 (44 mg/kg of chlortetracycline), 4) AS700 (44 mg/kg of chlortetracycline and 44 mg/kg of sulfamethazine from Aureo S-700; Alpharma Inc.), and 5) T11 (11 mg/kg of tylosin phosphate from Tylan; Elanco Animal Health, Guelph, Ontario, Canada). For each treatment, there were 5 pens of 10 animals, except for A44, which had 4 pens.

Antibiotics were fed throughout the feeding period and withdrawn 21 d before slaughter, exceeding current Canadian regulations (18 d for chlorotetracycline, 10 d for chlorotetracycline plus sulfamethazine, and no requirement for tylosin). A barley silage-based grower total mixed ration was fed for 80 d (Table 1), and cattle were subsequently adapted from the silage-based diet to a grain-based finishing diet by using 4 transition diets over a 21-d period. Steers were finished for 120 d on a barley grain-based total mixed ration (Table 1) typical of that used in the Western Canadian feedlot industry. Cattle were fed once daily to appetite to ensure that all feed provided each day was consumed. Antibiotics were mixed into barley-based premixes and were top-dressed by hand onto the rations daily and mixed in with a pitchfork to achieve the targeted concentrations and to avoid cross-contamination among diets. Animals in each pen were group fed and were capable of feeding at the feed trough at the same time. Cattle assigned to the control treatment were provided with premix that contained no antimicrobial agents.

All animals examined for fatty acid profiles were slaughtered within 48 h in a commercial abattoir at market BW (580 ± 34 kg). For each carcass, a sample of brisket adipose tissue was collected, placed in a plastic bag, frozen on dry ice, transported to the laboratory, and stored at –80°C until analyzed. Feed samples from the finishing diet were collected weekly for each treatment, pooled by month, frozen at –80°C, and monthly samples were pooled before fatty acid determinations.

Feed Fatty Acid Analysis

Fatty acid methyl esters (FAME) from the finishing diet were prepared according to Sukhija and Palmquist (1988) and analyzed by using the chromatographic conditions reported in Dugan et al. (2007).

Adipose Tissue Analysis

Brisket adipose tissue from each animal was freeze-dried and directly methylated with sodium methoxide individually, and the FAME were analyzed by using the GLC and silver-ion HPLC equipment and methods outlined by Cruz-Hernandez et al. (2004). The trans-18:1 isomers were, however, analyzed by using 2 complementary GLC temperature programs instead of a preparatory silver-ion TLC separation combined with GLC analyses at 120°C (Dugan et al., 2007; Kramer et al., 2008).

For the identification of FAME by GLC, reference standard 463 from Nu-Chek Prep Inc. (Elysian, MN) was used. Branched-chain FAME were identified by using GLC reference standard BC-Mix1, purchased from Applied Science (State College, PA). The CLA isomer mixture UC-59M, which was obtained from Nu-Chek Prep Inc., contained the 9c,11t, 8t,10c, 11c,13t, 10t,12c, 8c,10c, 9c,11c, 10c,12c, 11c,13c, 11t,13t, 10t,12t, 9t,11t, and 8t,10t isomers. The trans-18:1 and CLA isomers not included in the standard mixtures were identified by their retention times and elution orders as reported previously (Cruz-Hernandez et al., 2004, 2006; Kramer et al., 2008).

Statistical Analysis

Statistical analysis of fatty acid were performed by using PROC MIXED (SAS Inst. Inc., Cary, NC), with antimicrobial treatment included as the main effect and pen as a random factor. For those fatty acids having a significant (P < 0.05) random effect of pen within treatment, pen was used as the experimental unit. Individual animals were used as the experimental unit for those fatty acids in which the effect of pen within treatment was not significant (P > 0.05). The LSMEANS and PDIFF options were used for generating least squares means and comparison of treatments was by F-test protected LSD. Polynomial regressions incorporating linear and quadratic coefficients were also conducted by using the GLM procedure of SAS to evaluate the relationship between selected biohydrogenation products of PUFA. For instances in which the quadratic effects were not significant (P > 0.05), models were then reprocessed with only the linear effect. At slaughter, some animals were held back for additional antimicrobial resistance testing [A11 (n = 1); A44 (n = 3); AS700 (n = 1); T11 (n = 1)], and adipose tissue from these animals was not collected or analyzed.

	RESULTS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Diet compositions for the grower and finisher diets are given in Table 1. For the finishing diet, fatty acids present in concentrations of >0.3 g/100 g of FAME represented 98% of fatty acids. The dietary fatty acid composition was typical for a high-concentrate, barley-containing diet and consisted primarily of linoleic acid (18:2n-6), a 10:1 ratio of linoleic acid to linolenic acid (18:3n-3), and relatively high concentrations of 9c-18:1 and 16:0.

Concentrations of brisket adipose tissue fatty acids are reported for fatty acids with concentrations >0.1 g/100 g of total FAME (Table 2). For straight-chain SFA, 16:0, 18:0, and 14:0 were the predominant fatty acids, whereas in the branched-chain group, anteiso-17:0 and iso-17:0 were the most abundant. In general, dietary antibiotics did not affect concentrations of SFA, except for 16:0, which was greater (P = 0.02) in the A44 and T11 treatments, intermediate in the A11 treatment, and least in the control and AS700 treatments. However, the range in 16:0 was only 25.1 to 26 g/100 g of total FAME. On the other hand, 18:0 was numerically decreased for A44 and T11 treatments when expressed as grams per 100 g of total FAME, and this difference was significant when expressed as grams per 100 g of total SFA (P = 0.01, data not shown). Concentrations of total SFA and both individual and total branched-chain fatty acids were not affected by the different antibiotic treatments.

View larger version (11K): [in this window] [in a new window]   Figure 1. Individual trans-18:1 isomers as a percentage of total trans-18:1 in adipose tissue from beef brisket across antibiotic treatments (grand means; error bars = SEM; n = 234).

View larger version (8K): [in this window] [in a new window]   Figure 2. Major individual CLA isomers as a percentage of total CLA in adipose tissue from beef brisket across antibiotic treatments (grand means; error bars = SEM; n = 234).

View larger version (18K): [in this window] [in a new window]   Figure 3. Linear and quadratic regressions between the total trans-18:1 and individual major trans-18:1 isomers (a) and the minor trans-18:1 isomers (b, c; n = 234).

View larger version (26K): [in this window] [in a new window]   Figure 4. Linear regressions between the total CLA and individual major CLA isomers (a) and minor CLA isomers (b; n = 234).

View larger version (27K): [in this window] [in a new window]   Figure 5. Linear and quadratic regressions between 11t-18:1 and major CLA isomers (a), and 10t-18:1 and major CLA isomers (b; n = 234).

View larger version (14K): [in this window] [in a new window]   Figure 6. Linear regression between 6t/7t/8t-18:1 and 7t,9c-18:2 isomers (n = 234).

	DISCUSSION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Given the potential negative effects of monensin on ruminal biohydrogenation of PUFA, it was of interest to determine to what extent nonionophore antibiotics could influence beef fatty acid composition. In the present study, the effects of 3 nonionophore antibiotics (i.e., chlorotetracycline, tylosine, sulfamethazine) used in beef cattle production in North America on fatty acid profiles in brisket adipose tissue were investigated. Tylosin is a macrolide that inhibits protein synthesis by reversibly binding to the 50S subunits of the ribosome, causing premature detachment of incomplete polypeptide chains (Karahalios et al., 2006). Chlortetracycline also inhibits protein synthesis by preventing the association of aminoacyl-transfer RNA with the bacterial ribosome (Chopra and Roberts, 2001). On the other hand, sulfamethazine acts by competitively preventing the uptake of p-aminobenzoic acid in susceptible microorganisms, resulting in inhibition of the biosynthesis of folic acid (Giguère et al., 2006). Sulfonamides are generally used in combination with chlortetracycline in feedlot beef to improve performance and prevent coccidiosis (Pritchard et al., 1993). To date, only a few studies have investigated the effect of nonionophores on overall rumen fermentation (Van Nevel and Demeyer, 1995; Marounek et al., 1998), and their inhibitory effect on soybean oil hydrolysis was found to be slightly less than that produced by ionophores (Van Nevel and Demeyer, 1995). The extension of this line of investigation to determine whether nonionophore antibiotics could influence the fatty acid profile of beef was therefore considered of both scientific and practical interest.

Dietary Effects on Brisket Fatty Acid Composition

In general, there were very few treatment effects on the composition of brisket adipose tissue fatty acids. Despite the large number of animals per treatment, only slight increases were observed in 16:0 and 9c-14:1 for the A44 and T11 treatments. The reason for these differences is not apparent. The results suggest a slight increase in endogenous fat synthesis, but this could also be because of either small differences in feed intake, slight shifts in microbial or possibly animal metabolism, or both. Differences in backfat depths, however, were not detected (P = 0.95; data not presented).

Although differences in trans-18:1 and CLA isomers were not found, the characteristic distributions of the trans-18:1 and CLA isomers across diets were as might be expected when feeding a highly fermentable source of carbohydrate (i.e., feeding 85% barley; Dugan et al., 2007). Interestingly, barley contains less starch (57 to 58%) compared with other grains such as corn (72%; Huntington, 1997), but the fermentation rate of starch in barley is greater (Herrera-Saldaña et al., 1990). Barley (18.3 mg of FAME/g of DM) is also a good source of both 18:2n-6 (50%) and 18:3 (6%), which serve as substrates for biohydrogenation by rumen bacteria. The end result of feeding this high-concentrate diet was beef adipose tissue that contained 1.5 times more 10t-18:1 than 11t-18:1, irrespective of the antibiotic treatment. The trans-18:1 isomer distribution was similar to that observed by others when high-concentrate diets were fed to beef or dairy cattle (beef fat: Daniel et al., 2004; Hristov et al., 2005; Dugan et al., 2007; milk fat: Piperova et al., 2002; Roy et al., 2006; abomasal digesta: Duckett et al., 2002; Sackmann et al., 2003). This trans-18:1 isomer profile stands in marked contrast to that found in pasture-fed cattle, for which 11t-18:1 is the prominent trans-18:1 isomer in milk (Kraft et al., 2003; Loor et al., 2003; Cruz-Hernandez et al., 2004, 2006) and meat fat (Dannenberger et al., 2004; Dugan et al., 2007).

Effect of Antibiotics on Rumen Fatty Acid Metabolites in Adipose Tissue

It is clear from the adipose tissue composition that the antibiotics tested in this study did not significantly alter the biochemical processes involved in the biohydrogenation of PUFA or the desaturation of the trans-18:1 isomer products. Therefore, these nonionophore antibiotics did not selectively inhibit either the 11t- or 10t-18:1-producing strains of bacteria, which in turn would have altered the relative abundance of these 2 primary metabolites of PUFA biohydrogenation. Finding little or no selectivity in the rumen population assessed by the 11t- and 10t-18:1 contents after treatment with chlortetracycline could be considered reasonable, because chlortetracycline is a broad-spectrum antibiotic with activity against both gram-positive and gram-negative aerobic and anaerobic bacteria (Giguère et al., 2006). On the other hand, tylosin, which acts mostly against gram-positive bacteria inhibiting protein synthesis (Karahalios et al., 2006), could have caused a change in the trans-18:1 profile because B. fibrisolvens, the main producer of 11t-18:1, has been reported to be sensitive to tylosin (Marounek and Savka, 1994). The reason tylosin did not alter 10t-18:1 may be because an additional source of available dietary PUFA was not provided to the rumen bacteria. Butyrivibrio fibrisolvens is known to be sensitive to monensin, but there appears to be no shift toward 10t-18:1 production in milk fat when dairy cows are fed a basal diet without an added source of PUFA (Mutzvanga et al., 2003; unpublished data from that study: 11t-18:1 content in control and monensin-treated cows was 1.33 and 1.19%, respectively; 10t-18:1 content in control and monensin-treated cows was 0.71 and 0.71%, respectively). However, when an available source of PUFA was provided (i.e., soybean oil), a significant 10t-18:1 shift was evident in the monensin-treated cows (Eifert et al., 2006). This agrees with the in vitro results by Jenkins et al. (2003), who demonstrated a 10t-18:1 shift when rumen digesta were provided with both monensin and soybean oil in an artificial rumen. It is important to note that the added PUFA also need to be available to the rumen bacteria, as demonstrated by Duckett et al. (2002), who showed a 10t-18:1 shift in duodenal contents of steers when feeding corn oil as opposed to an equivalent oil concentration in the form of high-oil corn grain. Therefore, the lack of change observed with tylosin may well be because no source of readily available PUFA was added to the diet in the present study; consequently, there would not be enough precursor (18:2n-6 and 18:3n-3) available for the biohydrogenation process. This possibility was not explored in the present work because supplemental sources of PUFA are not commonly used in Canadian feedlot diets, but this is an obvious area for future research.

Metabolic Interrelationships of trans-18:1 and CLA Isomers

Naturally high levels of variation among animals within the same herd and fed the same diet are well recognized for both vaccenic and rumenic acid concentrations in milk (Jahreis et al., 1997; Kelly et al., 1998; Lawless et al., 1999; Peterson et al., 2002) and beef fat (Dugan et al., 2007). The concentrations of these fatty acids are characteristic of individual animals, as demonstrated in dairy cows when fed 2 widely different diets while maintaining their hierarchical position (Peterson et al., 2002). Consequently, because of the high variation in concentrations of trans-18:1 and CLA isomers, the lack of any treatment effects, and the large number of cattle investigated in this study (n = 234), this presented an ideal opportunity to further investigate possible correlations or interrelationships among these fatty acid metabolites.

The total trans-18:1 content in brisket adipose tissue of all 234 beef animals ranged from 1.1 to 4.8% of total fatty acids, and this content was positively and significantly related to 10t-18:1, but not 11t-18:1. Likewise, the total CLA content of the samples collected ranged from 0.4 to 1.1% of total fatty acids, and 9c,11t-18:2 was correlated with total CLA.

Several conclusions can be drawn from these results. Greater concentrations of total trans-18:1 content in beef are not necessarily related to a greater concentration of vaccenic acid (11t-18:1). As shown here, a greater percentage of the trans-18:1 content was associated with 10t-18:1 (range 0.2 to 3.4%), and not 11t-18:1 (range 0.2 to 1.2%). On the other hand, increased concentrations of total CLA are more likely to be associated with the desired rumenic acid (9c,11t-18:2). It should be noted that the GLC peak often labeled "9c,11t-18:2" consisted of several coeluting CLA isomers, particularly the 7t,9c-18:2 isomer, and can be resolved by using silver-ion HPLC (Yurawecz et al., 1998; Cruz-Hernandez et al., 2004).

The results of this study also showed that several trans-18:1 and CLA isomers appear to be metabolically interrelated. For instance, the well-known precursor-product relationship of 11t-18:1 and 9c,11t-18:2 via the ⁹-desaturase enzyme (Griinari et al., 2000) also showed a correlation in this study. Also of interest is the observation that the precursor-product relationship of 6t/7t/8t-18:1 and 7t,9c-18:2 was significant, supporting the previous findings of Corl et al. (2002), who found that 7t-18:1 was converted to 7t,9c-18:2 by the ⁹-desaturase enzyme. This is surprising because 7t-18:1 is only 1 of the 3 trans-18:1 isomers in this peak. Furthermore, both 10t- and 6t/7t/8t-18:1 peaks showed strong correlations with total trans-18:1.

At present, knowledge is lacking on the biochemical processes linking trans-18:1 isomers, other than by the random isomerization process proposed by Mosley et al. (2002). However, an isomerization hypothesis in which all trans-18:1 isomers originate from other 18:1 precursors fails to explain in the present experiment the intermediate concentration of 11t-18:1, the greater concentration of 10t-18:1, and their apparent lack of relationship. An alternative explanation is that the rumen population consists of bacteria with 2 distinctly different metabolic pathways of PUFA metabolism, forming either the 11t-18:1 or 10t-18:1 end products (Kramer et al., 2004), with other trans-18:1 isomers being generated by subsequent reactions within these major rumen metabolic pathways.

The feed additive antibiotics examined in the present study appeared to have no unique or selective effects on the fatty acid composition of trans-18:1 and CLA isomers. This suggests that these antibiotics did not additionally alter the biohydrogenation activity of rumen bacteria or that these populations adapted to the presence of these antibiotics during the feeding period. The consistent fatty acid profiles across treatments were apparently the result of an overriding influence of the high-grain (in this instance, barley) diet fed during the finishing period. It is quite likely that antibiotics such as ionophores that target primarily gram-positive bacteria may have a greater impact on the fatty acid profile of beef than do antibiotics such as chlortetracycline and sulfamethazine, which have a more broad-spectrum antimicrobial activity. Overall, when feeding a high-barley diet, the concentration of total trans-18:1 in brisket adipose tissue was quite variable and greater concentrations were related to 10t-18:1, and not 11t-18:1. In addition, none of the antibiotics used in this study was found to increase the amounts of desirable fatty acids (i.e., vaccenic and rumenic acids) in beef fat from cattle fed the barley-based finishing diet. Investigation into the use of antibiotics specifically targeting bacteria producing 10t-18:1 that would either enhance, or at least not interfere with, bacteria producing 11t-18:1 would be an important next step.

	Footnotes

 
¹ We thank David Rolland and Fred Van Herk for their technical assistance. The Education, University, and Research Department of the Basque Government (Vitoria-Gasteiz, Basque Country, Spain) is also acknowledged for the support of Noelia Aldai through a postdoctoral fellowship.

² Corresponding author: duganm{at}agr.gc.ca

Received for publication February 11, 2008. Accepted for publication August 1, 2008.

	LITERATURE CITED

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 


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