Abstract
The competitiveness and profitability of the poultry industry in market conditions are hampered by growing problems with the safety and quality of poultry meat. The use of targeted microbial preparations can assist in resolving these problems. Numerous studies of the properties of bacteria of the genus Enterococcus have shown their effectiveness in the practice of poultry farming. The objectives of this study were to identify the effect of various doses of Enterococcus faecium ICIS 96 added to the diet of broiler chickens on their metabolism and to evaluate the productive qualities of the chickens when different doses are used. The experiment was carried out on 72 Cobb-500 cross broiler chickens, divided into 3 groups. Chickens in the first group received a suspension of E. faecium ICIS 96 containing 1 × 108 cells in 1 mL of sterile saline, at a dose of 0.1 mL per 1 kg of live weight. The second group of chickens received a double dose of enterococcus, that is 0.2 mL of the suspension per 1 kg of live weight per day. The results demonstrated that 0.1 mL of a 1 × 108 per mL enterococcus culture suspension in the poultry diet per 1 kg of live weight per day intensified metabolism and increased the live weight of chickens after 40 d of treatment.
Résumé
La compétitivité et la rentabilité de l’industrie de la volaille dans les conditions du marché sont désavantagées par les problèmes croissants de sécurité et de qualité de la viande de volaille. La solution à ce problème peut être trouvée grâce à l’utilisation de préparations microbiennes ciblées. De nombreuses études sur les propriétés des bactéries du genre Enterococcus suggèrent leur efficacité dans la pratique de l’aviculture. Le but de l’étude est d’évaluer l’effet de différentes doses d’E. faecium ICIS 96 sur le métabolisme et les qualités productives des poulets à griller. L’expérience a été réalisée sur 72 poulets de chair croisés Cobb-500, répartis en 3 groupes. Les poulets du premier groupe expérimental ont reçu une suspension de culture E. faecium ICIS 96, préparée à raison de 1 milliard de cellules microbiennes dans 1 mL de solution saline. Les poulets de chair du deuxième groupe expérimental ont reçu une dose doublée d’entérocoques, soit 0,2 mL d’une suspension de 1 milliard de cellules microbiennes pour 1 kg de poids vif par jour. Les résultats ont démontré que 0,1 mL d’une suspension de culture d’entérocoques dans l’alimentation des volailles pour 1 kg de poids vif par jour intensifiait le métabolisme et, par conséquent, augmentait le poids vif des poulets dans les 40 jours suivant l’ontogenèse post-incubation.
(Traduit par Docteur Serge Messier)
Introduction
The poultry industry is one of the most profitable and promising sectors of agriculture in many countries of the world (1,2) and provides high-quality dietary products, including meat (3,4). The intensive practices used in rearing broiler chickens have a negative impact on their health, productivity, and safety (5,6), however, which leads to large economic losses (7,8).
One of the ways to intensify production in the poultry industry, while providing the population with organic food, is the use of probiotics (9,10). Probiotic preparations consist of living bacterial cells that have a positive effect on the host organism (11–13). Most strains of microorganisms in probiotics are lactic acid producing microorganisms, one of which is enterococci (14–16).
Numerous researchers have used enterococci as a basis for probiotic preparations for poultry farming (17–19). This choice is influenced by the following biological characteristics of Enterococcus: immunomodulatory action, formation of vitamins, colonization of gastrointestinal mucosa, and antagonistic activity to pathogenic and conditionally pathogenic microorganisms (20–23).
A wide search for biotechnologically valuable microorganisms has resulted in selection and assessment of an avirulent strain of Enterococcus faecium ICIS 96 (24,25). Previous studies have shown that E. faecium ICIS 96 at a dose of 0.1 mL of a 1 × 108 suspension per 1 kg of live weight per day in the diet of broiler chickens activated their metabolism, which led to a natural increase in productivity (26). It remains unclear, however, whether there is a relationship between a higher daily dose of E. faecium ICIS 96 strain and its biological effect.
The objectives of this study were to obtain new experimental data on the effect of different doses of E. faecium ICIS 96 on the metabolism and to evaluate the performance of broiler chickens when different doses of E. faecium ICIS 96 were included in the diet.
Materials and methods
The experiment was carried out in the vivarium of the Federal State Budgetary Educational Institution of Higher Education “Orenburg State Agrarian University.” The experiment was conducted on 72 Cobb-500 cross broiler chickens, divided into 3 groups by the method of analogous pairs. The chickens were housed in battery cages in a controlled environment facility.
Chickens in the first group (Group 1) received a suspension of E. faecium ICIS 96 culture, prepared at the rate of 1 × 108 microbial cells in 1 mL of saline solution, determined by comparison with the McFarland turbidity standard of 0.5 units. The probiotic supplement was prepared daily and added to the drinking water at a ratio of 0.1 mL per 1 kg of live weight. Chickens in the second group (Group 2) received a double dose of enterococcus daily, that is, 0.2 mL of probiotic culture per 1 kg of live weight. The live weight of each group was determined once every 10 d. Chickens in the control group did not get an enterococcus suspension and remained intact. The chickens were fed a dry balanced mixed fodder with nutritional values corresponding to the recommended standards of the All-Russian Scientific Research Institute of Technology for the Poultry Industry (VNITIP). The chickens had free access to feed and water. The experimental period was 40 d.
Blood was obtained from the axillary vein when the chickens were 30 and 40 d old. The resulting serum from the blood clot retraction was studied on a STAT FAX 1904 photometer (Awareness Technology, Palm City, Florida, USA). The following biochemical parameters were analyzed: total protein, albumin, urea, uric acid, pyruvic acid, glucose, triacylglycerols (TAG), total cholesterol, high-density lipoprotein (HDL) cholesterol, low-density lipoprotein (LDL) cholesterol, and activity of aspartate aminotransferase (AST) and alanine aminotransferase (ALT).
At 30 and 40 d of age, chickens in all 3 groups were weighed on a scale in the morning before feeding. The numerical findings were analyzed using the parametric method of estimating the confidence coefficient by the Fisher-Student’s t-test. Statistical data were processed using Microsoft Office Excel 2013 (Microsoft Corporation, Redmond, Washington, USA).
Results
The study showed that the dose of enterococcus given to chickens in Group 1 intensified protein metabolism. The period from 20 to 30 d in the life of broilers is characterized by an intensive weight gain. During this period, metabolites in the blood serum of chickens of Group 1 differed from chickens in the control group. Chickens in Group 1 had a 23.8% (P < 0.05) lower total protein content, 22.2% less urea, and a higher concentration of uric acid, which is the final product of protein metabolism in the body of poultry.
Machín et al (27) claim that more uric acid, which is an important antioxidant, in the blood can improve the antioxidant status of chickens. In our study, this trend continued until the age of 40 d, but was less pronounced. The marked changes demonstrated a more intensive consumption of nutrients that increased development of tissues in the growing bodies of chickens in Group 1.
Energy metabolism indicators demonstrated significant age-related changes when these chickens were 30 d old. Compared to chickens in the control group, those in Group 1 had a 17.8% lower concentration of total cholesterol and 34.7% less low-density lipoprotein (LDL) cholesterol, but 12.2% higher values of triacylglycerols and 24.4% more high-density lipoprotein (HDL) cholesterol in the blood serum.
Active cholesterol synthesis by the cell or intracellular hydrolysis of intracellular cholesterol esters is accompanied by a higher concentration of this substance and its intense excretion from the cell due to the capture of cholesterol molecules from cytoplasmic membranes by high-density lipoproteins and their predominant transportation to the liver.
Our data are consistent with those of Tayeri et al (28) who reported that when a probiotic based on lactic acid microorganisms is introduced into the diet of broiler chickens, HDL cholesterol in the blood serum increased and LDL cholesterol decreased. Zhang et al (29) also noted that when a probiotic containing E. faecium DSM 7134 was administered to chickens, the concentration of HDL cholesterol in the blood serum increased and LDL cholesterol decreased.
A similar result was reported by Capcarova et al (30), in which a decrease in the concentration of total cholesterol and lipids in blood plasma was noted after the probiotic strain E. faecium M 74 was introduced to poultry feed. By the age of 40 d, there was a general trend towards a decrease in the content of total cholesterol and an increase in the concentration of triacylglycerols (TAGs) in the blood of chickens in the treated groups.
After 30 d of treatment in our study, the concentration of glucose in the blood serum of chickens in Group 1 decreased by 19.7 to 32.5%. In addition, the content of this metabolite in the blood was 10.3% less than chickens in the control group (P < 0.05). The level of pyruvic acid and the activity of α-amylase in the chickens in Group 1 at the age of 30 d was higher than chickens in the control group (P < 0.05). This provides further evidence of intense metabolic activity in chickens, whose diet included enterococcus at a rate of 1 × 108 microbial cells in 1 mL of saline solution, given daily at a dose of 0.1 mL per 1 kg of live weight.
The noted changes in protein and carbohydrate-lipid metabolism in the chickens in Group 1 met the needs of their rapidly developing bodies and contributed to a 9.20% higher live weight compared to chickens in the control group by the age of 40 d (2796.6 g versus 2561.0 g, P < 0.05). Shehata et al (15) showed that the introduction of the probiotic strain E. faecalis-1 into the diet of broiler chickens contributed to a significant increase in body weight and feed conversion.
A double dose of E. faecium ICIS 96, as given to chickens in Group 2 in our study, did not affect their general clinical condition, although there were some metabolic changes. By the age of 30 d, the total protein content in the blood serum of chickens in Group 2 decreased by 9.76% to 29.7 g/L compared to 33.0 g/L in the control group. The same trend was observed in the content of albumin in the blood serum (6.52 difference), although the amount of total protein in the chickens in Groups 1 and 2 was 1.67% higher than in their peers in the control group.
The lower total protein in the blood serum of poultry of Group 2 is not the result of intensive consumption of albumin as a building material, as indicated by the low content of uric acid in the blood of chickens in Group 2 compared to those in the control group [70.3 mmol/L versus 178.9 mmol/L, respectively (P < 0.05)]. These findings echo those of Rozhkova et al (31) in which the probiotic supplement Profort, containing strains of E. faecium and Bacillus subtilis bacteria, in the diet of turkeys reduced albumin in their blood serum.
By the end of the study (at 40 d old), there was a general age-related tendency for total protein and albumin to decrease in the blood serum of all chickens. These changes occurred more intensively in the control group, which had 6.47% less total protein and 7.89% less albumin in their blood than chickens in Group 2. At the same time, in the experimental group, the concentration of uric acid was 28.56% higher than chickens in the control group (P < 0.05) (Table I).
Table I.
Hematological parameters of chickens in the control group and in Groups 1 and 2.
| Indicator | 30 d | 40 d | ||||
|---|---|---|---|---|---|---|
|
|
|
|||||
| Control | Group 1 | Group 2 | Control | Group 1 | Group 2 | |
| Total protein, g/L | 33.0 ± 1.99 | 25.1 ± 0.68* | 29.7 ± 0.43 | 24.5 ± 1.22 | 23.4 ± 1.32 | 26.1 ± 10.67 |
| Albumin, g/L | 15.3 ± 0.67 | 14.8 ± 0.73 | 14.3 ± 0.67 | 12.7 ± 0.33 | 13.2 ± 0.57 | 13.7 ± 5.59 |
| Uric acid, μmol/L | 178.9 ± 30.35 | 195.3 ± 15.26 | 70.3 ± 11.69* | 89.0 ± 14.95 | 97.4 ± 12.42 | 133.6 ± 5.25* |
| ALT, U/L | 8.8 ± 1.03 | 8.9 ± 0.87 | 8.8 ± 0.78 | 8.2 ± 0.27 | 8.3 ± 1.79 | 8.4 ± 3.53 |
| AST, U/L | 556.7 ± 31.86 | 1000.9 ± 268.31 | 439.3 ± 13.86* | 497.6 ± 59.70 | 647.9 ± 78.32 | 381.9 ± 162.78 |
| Glucose, mmol/L | 11.5 ± 0.56 | 10.3 ± 0.19 | 10.7 ± 0.29 | 10.5 ± 0.42 | 11.1 ± 0.67 | 11.5 ± 4.71 |
| Total cholesterol, mmol/L | 4.1 ± 0.21 | 3.4 ± 0.33 | 4.3 ± 0.20 | 2.5 ± 0.09 | 1.9 ± 0.53 | 2.8 ± 1.14 |
| TAG, mmol/L | 0.3 ± 0.03 | 0.3 ± 0.06 | 0.3 ± 0.07 | 0.5 ± 0.04 | 0.5 ± 0.12 | 0.5 ± 0.21 |
Statistical significance of biochemical parameters of chickens in the untreated control group and chickens in Groups 1 and 2 (P < 0.05).
ALT — Alanine aminotransferase; AST — Aspartate aminotransferase; TAG — Triacylglycerol.
Evaluation of the activity of the transamination enzyme in the blood of broilers when E. faecium ICIS 96 was introduced into the diet at different doses did not reveal significant changes in relation to alanine aminotransferase (ALT). The activity of blood ALT in chickens in Groups 1 and 2 at the age of 30 to 40 d was higher than chickens in the control group. There were changes, however, in the activity of aspartate aminotransferase (AST). At the age of 30 d, the activity of AST in the blood of chickens in Group 1 was 79.74% higher than chickens in the control group and 30.21% higher at 40 d. With the double dose of enterococcus (Group 2), the activity of AST decreased by 21.08% at 30 d (P < 0.05) and by 23.24% at 40 d. Analysis of indicators of carbohydrate-lipid metabolism in the blood of broiler chickens indicated that the dose of enterococcus strain did not significantly affect the glucose content. The low glucose content (7.19% to 10.31%) in the blood of chickens in Groups 1 and 2 at the age of 30 d increased by an additional 5.58 to 9.50% by the age of 40 d.
Our results on the content of glucose, ALT, and AST in the blood of chickens echo the results of Demeterová et al (32) in which the probiotic strain E. faecium DSM 7134 was introduced into the diet of broiler chickens.
Lipids are transported in the blood without oxidizing or breaking down and the blood lipid pattern demonstrates the state of lipid metabolism. In this regard, the study of the total cholesterol content becomes of great interest. Cholesterol is a part of cell membrane structure and the basis for the biosynthesis of bile acids and hormones. Our study revealed a 4.65% higher total cholesterol content in chickens in Group 2 at the age of 30 d, both in relation to the control group and Group 1 (4.3 mmol/L versus 3.4 mmol/L). By the age of 40 d, the total cholesterol content in the blood generally tended to decrease. Nevertheless, its concentration in chickens in Group 2 was 12% higher than that in the control group.
The content of triacylglycerols (TAGs) in the blood of chickens in Group 2 was 11.11% higher than in control birds at 30 d and 1.96% lower than controls at 40 days.
These metabolic processes affected the growth rate of the chickens. Throughout the study period, a higher dose of E. faecium ICIS 96 resulted in a 1.17 to 13.91% lower average live weight of chickens in Group 2 than that of chickens in the control group. By the end of rearing, chickens in Group 2 weighed 12.13% less than their peers in the control group (2250.3 g versus 2561.0 g, P < 0.05) (Figure 1).
Figure 1.
Live weight of chickens in the untreated control group and chickens in both Groups 1 and 2.
* Statistically significant difference in live weight of chickens in the control group and chickens treated with standard (0.1 mL of 108 CFU/mL per kg of live weight) or a double dose of E. faecium ICIS 96 (P < 0.05).
Evaluating the biochemical parameters of the blood and the productive qualities of the chickens in Groups 1 and 2, we concluded that there is no direct relationship between the productivity of the chickens and the introduction of high doses of probiotic supplements into the diet. However, by the age of 40 d in chickens in Group 1, which received a lower dose of enterococcus, changes in protein and carbohydrate-lipid metabolism were noted that contributed to a 9.20% increase in live weight compared to the control group.
By the end of the experimental period, chickens in Group 2 that received a double dose of enterococcus weighed 12.13% less than chickens in the control group. Therefore, we conclude that the lower dose of 0.1 mL per 1 kg of live weight per day of E. faecium ICIS 96 is the most effective.
Discussion
According to the literature, there is no direct relationship between poultry productivity and higher doses of probiotic supplements in the diet, which is consistent with the results of our study. Mountzouris et al (33) reported that a 5-component probiotic preparation with 2 strains of Lactobacillus bacteria and 1 culture of Bifidobacterium sp., Enterococcus, and Pediococcus sp. microorganisms provided the best growth rates in the group of broilers with the lowest concentration of probiotics (108 CFU/kg of the diet). Apata (34) reported that a low dose of Lactobacillus bulgaricus (2.4 × 109 and 6 × 109 CFU/kg of ration) introduced into the diet of broiler chickens proved to be more effective than a high dose of the preparation (8 × 109 CFU/kg of ration).
On the other hand, Zou et al (35) showed that a probiotic supplement consisting of B. subtilis (2 × 108 CFU/g), C. butyricum (2 × 106 CFU/g), and E. faecalis (1 × 106 CFU/g) added to the diet of broiler chickens contributed to an increase in the productive qualities of chickens, although the best indicators were noted in the group of broilers that received a double dose of the probiotic complex. Some studies have claimed that the most efficient use of probiotics in animals is by including a daily dose of 1 × 107 to 1 × 109 of microbial cells (36–38).
The results of this study have shown that a daily dose of 1 × 108 E. faecium ICIS 96 per mL, given at a dose of 0.1 mL/1 kg of live weight of in the diet intensifies metabolism and increases the live weight of chickens within the first 40 d of life. These findings broaden our understanding of the biological effects of probiotic strains of enterococci in vivo and make it possible to recommend this daily dose as effective in raising broiler chickens.
The effects of the action of the Enterococcus culture on the poultry organism shown in this study will assist the poultry industry to choose the most effective means of improving the quality and safety of their products. Our further research will be aimed at selecting the dosage of the drug that ensures the successful survival of the probiotic strain in the body of chickens and determining its potency and viability after long-term storage in production facilities.
Acknowledgment
This study was conducted with the financial support of the Federal State Budgetary Institution’s Fund for the Promotion of the Development of Small Businesses in the Sphere of Science and Technology under the grant program UMNIK-2019.
Funding Statement
This study was conducted with the financial support of the Federal State Budgetary Institution’s Fund for the Promotion of the Development of Small Businesses in the Sphere of Science and Technology under the grant program UMNIK-2019.
Footnotes
Data from this study are available from the authors upon request.
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