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Original Articles

Effect of zilpaterol hydrochloride on animal performance and carcass characteristics in sheep: a meta-analysis

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Pages 104-112 | Received 27 Aug 2014, Accepted 17 Nov 2014, Published online: 19 Mar 2015

Abstract

The present study constitutes a meta-analysis of the use of zilpaterol hydrochloride (ZH) in sheep production (18 studies, n = 724 animals were evaluated), focused in its effects on productive performance and carcass characteristics in sheep who were given ZH in different doses (control 0, ≤0.50 and ≥0.54 mg/kg raised to the power 0.75 body weight (BW)). The analysis of the data assembled in the database was conducted by a statistical meta-analysis based on mixed model methodology. Results on weight gain were higher (P < 0.03) for the group supplemented with ≥0.54 mg vs. control treatment, feed conversion improved (P < 0.01) with the inclusion of ZH compared with the control group. Carcass yield and Longissimus dorsi area showed no differences (P > 0.05) between treatments, fat content in the carcass diminished in a linear effect (P = 0.02) with the inclusion of ZH. The results show a positive effect on improving animal performance, mainly in the characteristics on the fat deposition. The optimal dose varies depending on the variable to improve, ranged in 0.24 up to 1.21 mg ZH/kg BW0.75 to reduce fat and carcass get leaner or increase average daily gain, respectively.

1. Introduction

The livestock and meat industry is constantly looking for alternatives to promote fast and efficient growth of livestock, improve the carcass yield, i.e., increasing Longissimus dorsi muscle area (Beermann Citation2009; Etherton Citation2009) or diminishing the fat content in the carcass (Villalobos-Villalobos et al. Citation2014).

The study of products to improve growth rate and reduce days of fattening in sheep has been a constant in recent decades. In this sense, numerous studies have focused on the effects of metabolic modifiers, which improve the efficiency and profitability of livestock production by increasing the rate of growth, optimizing feed conversion (FC), and increasing carcass quality (Sillence Citation2004; Dikeman Citation2007; Johnson & Chung Citation2007).

The use of β-adrenergic agonists (β-AA) promotes rapid growth in farm animals, because it stimulates the development of muscle mass through an increase in protein synthesis and reduction in its degradation in the striated muscle, while in fat tissue reducing lipogenesis and increasing lipolysis (Mersmann Citation1998; Beermann Citation2009). Most of the physiological effects of catecholamines are due to specific interactions with β-adrenergic receptors (β-AR) (Abney et al. Citation2007). Therefore, the use of these substances has a number of advantages relating to the improvement of productivity (i.e., lean yield) and affects other quality factors negatively (i.e., tenderness), since the meat of animals treated with β-AA contains a greater proportion of lean tissue and less fat (Dominguez-Vara et al. Citation2010). One of the most widely used β-AA approved in the USA, Mexico, Canada, and South Africa is the zilpaterol hydrochloride (ZH), which has been used extensively in cattle, showing a positive impact on meat-producing beef cattle (Avendaño-Reyes et al. Citation2006; Montgomery et al. Citation2009). However, its use in sheep is limited, and when used, the general dose is that recommended for beef cattle (0.65–0.82 mg/kg BW0.75) (Canadian Food Inspection Agency Citation2014).

Therefore, it is important to determine issues such as optimal dose, schedule of administration, and its effects on performance and carcass composition in sheep (López-Carlos Citation2010). However, the determination of these issues is difficult because there is little information on its use in sheep and the results are contrasting (Salinas-Chavira et al. Citation2004; Moreno et al. Citation2010a; Rios-Rincón et al. Citation2010; Velazquez-Morales et al. Citation2010; Estrada-Angulo et al. Citation2011). The objective of this study was to perform a meta-analysis of studies done on the use of ZH in sheep and determines if there are differences in their use on performance and characteristics in the carcass.

2. Material and methods

2.1. Database development

Search information was focused on studies of feed supplementation ZH in sheep and their effects on performance and carcass quality. A database was conducted from experiments where both ZH and sheep were specified. This included publications that were obtained from the ISI Web Science database, Scopus, Redalyc, Routledge-Taylor and Francis Group, Springer Lynk using the words sheep, lamb, ZH, and/or carcass as a keywords.

In addition to ZH, related variables were also integrated in the database. These variables included at least a control group who had not received treatment and a ZH-treated group that, indicate the dose used, and the number of animals in each group. Then, we assessed the main production variables: initial live weight (LWi), final live weight (LWf), average daily gain (ADG), dry matter intake (DMI), FC (kg of DMI to gain a kg of live weight); and the main variables of carcass quality, including carcass yield (C. yield), hot carcass weight (HCW), cold carcass weight (CCW), thickness of subcutaneous fat (fat), and L. dorsi muscle area (L. dorsi). As for the diets used, these had to include the content of crude protein (CP) and metabolizable energy (ME), and the treatment time (days).

Initially, by using the above-mentioned keywords, a total of 24 articles were found. After abstract evaluations, there were 18 potential articles to be included in the database. Full texts of these articles were then evaluated, and as a result, a total of 26 studies from 18 articles met the respective criteria (), comprising 724 animals and different ZH doses were performed into the database. The studies that there were excluded from the database were because they worked with females under heat stress (Avendaño-Reyes et al. Citation2010, Citation2011; Macias Cruz et al. Citation2010, Citation2013; Velazquez-Morales et al. Citation2010) and the study of Salinas-Chavira et al. (Citation2006) considered grazing lambs.

Table 1. Effect of the addition of ZH on the productive performance and carcass characteristics in fattening lambs.

2.2. Setting the data and statistical analysis

Variables being dependent on body weight (BW) were standardized by relating them to metabolic body weight (BW0.75) to counterbalance the associated variation among and within animals. All data reported were transformed into the same units of measurements so that administration of the daily dose of ZH is expressed in mg ZH/kg BW0.75. The LWi and LWf were calculated in Kg BW0.75. DMI was adjusted in g/kg BW0.75. ME was obtained in MJ/kg DM and CP in g/kg DM of the diet. FC was calculated based on kg DMI to gain 1.0 kg BW (Shimada-Miyasaka Citation2003). The parameters for carcass evaluation were: carcass yield (%), HCW (kg), CCW (kg), subcutaneous fat thickness (cm), and L. dorsi muscle area (cm2). The analysis of the data assembled in the database was conducted by a statistical meta-analysis based on mixed model methodology (St-Pierre Citation2001; Sauvant et al. Citation2008). The data of the variables obtained were initially subjected to an exploratory analysis of tests for normality and multiple correlations to determine the feasibility of the data (Hair et al. Citation1998). The variables considered for the principal component analysis (PCA) were ADG (g/kg BW0.75), FC (kg/kg BW), subcutaneous fat thickness (Fat, cm), carcass yield (C. yield, %), HCW (kg), and CCW (kg).

Once the data matrix was analyzed using two multivariate techniques: (1) PCA and (2) hierarchical cluster analysis (CA), the first multivariate technique was to reduce the information and generate major factors.

PCA were rotated with varimax, which allowed to choose those that explanation of the variables presented (Garcia Citation2008), with CA the cases were grouped according to the similarity and differences between cases, that is internally homogeneous and externally heterogeneous (Guisande et al. Citation2006). For CA only used the rotated factors with eigenvalue higher than 0.5 (Hair et al. Citation1998), the clustering method was Ward's, the measure was the Euclidean distance squared. The PCA was performed using the statistical program Statistical Package for Social Sciences (SPSS, version 15.0, November Citation2006), and CA was performed with the statistical software STATISTICA version 7.0 March Citation2013).

Productive parameters and carcass characteristics were analyzed using the General Linear Model procedure of SAS (Citation1999). Using a completely randomized design, Yij = μ + Ti + Eij, where Yij = response variable in level i of treatment (T), μ = general mean, Ti = effect of treatment factor level I, and Eij = random error.

Furthermore, the linear and quadratic effects were evaluated and a correlation between the variables was made. Also, the equation of the second derivative was determined to obtain the optimum inclusion level (SAS Citation1999) of ZH.

(1)
where Y = response variable (ADG, DMI, FC, Fat, and L. dorsi), “a” is the intercept and “b” is the slope, x is expressed in mg ZH/kg BW0.75.

3. Results and discussion

The PCA results are presented in obtaining four factors (F), which were assigned a name to describe them, F1 refers to C. yield, HCW, and CCW, and it was named carcass performance. The F2 was related to FC, indicating that when ZH is included, FC increases, explains the effect of ZH on the metabolism of the digested feed, named effect of ZH on the metabolism of the digested feed. F3 refers to the ADG, named growth response. F4 makes reference to subcutaneous fat thickness and the presence of ZH, showing that the absence of ZH favors the presence of subcutaneous fat thickness; it was named effect on fat deposition. These factors accounted for 92% of the total variation.

Table 2. Correlation coefficients of variables and total variance of the rotated factors (F1, carcass performance; F2, effect of ZH on the metabolism of the digested feed; F3, growth response; F4, effect of ZH on the fat deposition) identified in the PCA.

responds to the characteristics for different studies of ZH in fattening lambs, showing heterogeneity in the data, where the ZH shows a response on the animal and no effect attributable to the administration of ZH. Similar situation was presented to analyze the forest plot () showing that the highest percentage of studies are outside of the confidence limits (P > 0.05), but are grouped at a confidence level of 0.1, indicating that while the study is not completely homogeneous, presents sufficient basis for analysis, using models that consider the variability of these data.

Figure 1. Characteristics for different studies of ZH. Obtained from the Heterogenety Dersimonian and Laird´s test.
Figure 1. Characteristics for different studies of ZH. Obtained from the Heterogenety Dersimonian and Laird´s test.
Figure 2. Characteristics for different studies of ZH in fattening lambs obtained from the forest plot test.
Figure 2. Characteristics for different studies of ZH in fattening lambs obtained from the forest plot test.

CA was determined with the coordinates of the rotated factors (), which show the presence of three groups. The characteristics of each group with respect to its variables are presented in . It is noted that the main grouping variable is the dose of ZH used, so the groups (G) were Group 1 (high doses), higher than 0.54 mg/kg BW0.75; Group 2 (low doses), less than 0.50 and higher than 0.23; and Group 3 control group, without the addition of ZH.

Figure 3. Dendrogram to 26 cases of ZH administration (mg ZH/kg BW0.75) in fattening lambs; G1, Group 1, higher than 0.54 mg/kg BW0.75; G2, Group 2, low-dose group less than 0.50 mg/kg BW0.75; G3, Group 3, control group without ZH.
Figure 3. Dendrogram to 26 cases of ZH administration (mg ZH/kg BW0.75) in fattening lambs; G1, Group 1, higher than 0.54 mg/kg BW0.75; G2, Group 2, low-dose group less than 0.50 mg/kg BW0.75; G3, Group 3, control group without ZH.

Table 3. Characteristics of the groups obtained from CA for different dose of ZH in fattening lambs.

The control group was characterized by lower ADG and more back fat present in the carcass. The low-dose group (≤0.50 mg/kg BW0.75) had the lowest FC, the best carcass features and the highest HCW and CCW; this effect could be done because the animals start with a heavy weight than the rest of the treatments. The high-dose group (>0.54 mg/kg BW0.75) showed a linear reduction in subcutaneous fat thickness (P = 0.025) which coincides with Mersmann (Citation1998) and Beermann (Citation2009).

shows the day of the trials analyzed, the characteristics of the diet as well as initial and final weights of the lambs. There were no differences (P > 0.05) in any of the variables analyzed. The ME and protein levels of these studies are consistent with those recommended by the NRC (Citation2007), which was reflected in the good condition of the animals, since the amount of these nutrients is the main factor determining the productivity thereof.

Table 4. Effect of ZH dose (mg ZH/kg BW0.75) on the main parameters of fattening lambs.

The growth response to ZH administration commonly is often reduced over time (Dunshea Citation1993; Moody et al. Citation2000; Abney et al. Citation2007; Aguilera-Soto et al. Citation2008), which is possibly a result of desensitization of the β-AR after chronic exposure to the β-AA (Dunshea et al. Citation1998). Similarly in cattle, Dikeman (Citation2007) analyzing several studies using ZH, its administration is recommended for a period not exceeding 30 days, which is within the range of days of supply used in this study.

According to Estrada-Angulo et al. (Citation2011), when comparing 20-, 30-, and 40-day supply of ZH, the rate response tends to remain constant or even decrease with increase in treatment days, revealing why the best balance between cost and benefit is between 20 and 30 days of treatment. The same effect was observed by López-Carlos et al. (Citation2010, Citation2011) who found that the supply of ZH for more days, the HCW decreases linearly, the opposite phenomenon occurring with the subcutaneous fat thickness.

With the major productive characteristics of lambs treated with ZH (), the doses ≥0.54 mg ZH/kg BW0.75 showed a higher ADG (P = 0.039) compared to the control group.

DMI were not different (P = 0.662) between treatments. ADG increased by 20% and 32% when administered ≤0.50 and ≥0.54 mg ZH/kg BW0.7, respectively, compared with the control group. Estrada-Angulo, Barreras-Serrano, et al. (Citation2008) founded a trend (P = 0.07) in the increase of ADG compared with the control group, and López-Carlos et al. (Citation2011) reported an increase of 24.4% in ADG. Similarly, López-Carlos et al. (Citation2010) evaluated the effect of ractopamine hydrochloride (RH) (0.35, 0.70, and 1.05 mg/kg BW) and ZH (0.10, 0.20, and 0.30 mg/kg BW) on growth performance of Dorper × Katahdin sheep for 42 days reported a linear increase in the ADG with increased levels of both β-AA, without adversely affecting feed efficiency.

FC was significantly better (P = 0.017) for the ZH group than the control group. The FC improved by 23% and 22% with the addition of ZH (≤0.50 and ≥0.54 mg ZH/kg BW0.75, respectively) with respect to the control group. These results are similar to those reported by López-Carlos et al. (Citation2011), who use Dorper × Katahdin sheep with ZH (6 mg/kg DM) or RH (20 mg/kg DM), and reported similar effects of the two β-agonists, but with a higher final weight (9.6%), better ADG (24.4%) and FC (28.2%) compared with the control group. Similarly, Rios-Rincón et al. (Citation2010) evaluated the influence of treatment with ZH (0.12 or 0.18 mg/kg of BW) on performance and carcass characteristics, using Pelibuey × Katahdin during the last 35 days on feed, reporting that the use of ZH increased ADG by 40%.

By showing differences in ADG and FC when ZH is provided, it appears that in addition to higher gains in muscle tissue, there was a better efficiency of utilization of ingested nutrients. This can be explained because one of the effects of the administration of β-AA is the increase in blood flow to the periphery of the body, resulting in a greater flow of nutrients into the muscles and, therefore, more substrates for the protein synthesis (Mersmann Citation2002) so that the gain of muscle mass could be explained by an increase in protein synthesis and/or a decrease in the proteolysis (Bell et al. Citation1998).

As for the main characteristics of the carcass (), there were not significant differences (P > 0.05) for any variable, showing a linear effect (P = 0.025) to decrease the thickness of subcutaneous fat as increased the dose of ZH. This is because the β-AA increases the degradative metabolism of lipids in the adipocytes. Activating the catabolism of lipids through the activation of hormone-sensitive lipase, which is activated by the protein kinase A leads to a degradation of triglycerides into glycerol and fatty acids (Mersmann Citation2002), which are provided by the adipocyte to be used as sources by other oxidative tissues. At the same time, the synthesis and esterification of fatty acids within the triacylglycerol is inhibited by β-AA (Dominguez-Vara et al. Citation2010) so that the increase in the catabolism (lipolysis) and the decrease in anabolism (fat generation) resulting in a lower fat deposition (Mersmann Citation2002). This is important because it has been observed that the accumulation of fat in animals reduces production efficiency, therefore, when using β-AA productivity is improved (Salinas-Chavira et al. Citation2004).

Table 5. Effect of ZH dose (mg ZH/kg BW0.75) on the main carcass characteristics in fattening lambs.

Although this study only showed a linear effect (P = 0.025) to the decrease of subcutaneous fat when administered ≤0.50 and ≥0.54 mg ZH/kg BW0.75 (18% and 29%, respectively), this reduction in the amount of fat is similar to that reported by Mondragon et al. (Citation2010) and López-Carlos et al. (Citation2010), this studies reported a linear reduction in back fat thickness with increasing the dose of ZH.

In , there is a correlation between the dose of ZH and the variables studied, being positive in the LWf (P = 0.0126) and negative in FC (P = 0.005) and fat (P = 0.028) and a positive trend in ADG (P = 0.080), which indicates that a higher ZH dose increases LWf and improve FC and reduce fat with a tendency to increase the ADG, making the sheep more efficient.

Table 6. Correlation between the carcass characteristics of fattening lambs supplemented with ZH and its main productive parameters, the upper part shows the degree of significance (P value) and lower absolute values.

shows the calculation of the second derivative, which was used to obtain the optimal dose of ZH (mg/kg BW0.75) in fattening lambs nearing slaughter. It is observed that the optimal dose varies depending on the variable you want to improve, using amounts up to 1.21 mg ZH/kg BW0.75 to increase ADG or 0.24 mg ZH/kg BW0.75 in order to reduce fat and carcass get leaner (). As an average, the optimal ZH dose for fattening lambs ranged in 0.40 as a lower dose up to 0.60 mg ZH/ kg BW0.75 depending on the response to improve, which is lower than the recommended in other studies.

Table 7. Calculating the second derivative equation (y = a + bx + bx2) to estimate the optimal dose of ZH (mg ZH/kg BW0.75) in fattening lambs.

Although on fattening lambs, the results of this study are consistent with Dikeman (Citation2007), using ZH during the last 30 days (fattening period), increasing ADG, improved FC and also has a tendency to decrease in carcass fat. The main effect of ZH that has been determined is a lower total fat, and an increase in the percentage of muscle and increase in the L. dorsi muscle area.

4. Conclusion

The ZH supplementation improved daily gain and FC in fattening lambs and a trend toward decreased subcutaneous fat with increasing dose. The ZH has significant positive correlation to the LWf and FC, and a negative correlation with a decrease in carcass fat. More studies are necessary to elucidate the optimal ZH dose in fattening growing lambs.

Acknowledgments

Dr Arturo Ortiz was granted for a CONACyT fellowship during his studies in the PCARN at the University Autonomous State of Mexico, Mr. Martín Barbosa was granted for a CONACyT fellowship during his studies in the University Autonomous State of Mexico, as a specialist in sheep production program. We also thank Miss. Liz Hooper, LTC-University of North Texas for the critical review of the present manuscript.

References

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