Keywords
Antibiotics alternative, Average daily gain, Goats, Natural feed additives, Protozoa, Secondary metabolites, Sheep.
Antibiotics alternative, Average daily gain, Goats, Natural feed additives, Protozoa, Secondary metabolites, Sheep.
The manuscript was revised according to the comments from reviewers with the following details:
1. Indicated original words before using abbreviations.
2. Deleted the statement regarding the authors’ duties in study selection and data extraction.
3. Added data about the type of ration and experimental design in Table 3.
4.Included the discussion about why essential oils can be used as a growth promoter for small ruminants
See the authors' detailed response to the review by Liang Chou Hsia
See the authors' detailed response to the review by C.J. Linde du Toit
In animal nutrition, antibiotics become the first choice of feed additive due to their substantial benefit toward health and productivity. However, the routine use of this chemical additive yields residues in livestock products, and is also responsible for the development of microbial antibiotic resistance1,2. These factors represent a dangerous risk to human health, which has led to the global drive to reduce antibiotic use in the livestock sector. As a result, several natural products have been proposed to be used as antibiotic alternatives3,4.
Among natural feed additives, essential oils have a unique mechanism of action in livestock production. They can manipulate rumen fermentation characteristics5,6 and subsequently improve growth rate7,8. However, other findings showed no meaningful effect of this feed additive on productive performance9,10, while another study showed a negative impact11. The inconsistent results among studies requires an appropriate tool to quantify the overall effect. Therefore, this study was conducted to measure the quantitative effects of dietary essential oil supplementation on dry matter intake (DMI), average daily gain (ADG), and feed conversion ratio (FCR) of small ruminants using a systematic review and meta-analysis approach.
The systematic review and meta-analysis was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline12. A completed PRISMA checklist is available in Reporting guidelines13.
The inclusion and exclusion of the study were based on participants, interventions, comparisons, outcomes, and study design (PICOS) criteria as indicated in Table 1. Additionally, only publications written in English which was included in this study. All dates up until the date last searched were included.
The literature search was carried out using the following electronic databases: Scopus, PubMed, and SciELO. The search was last performed on 30 April 2020. Table 2 shows the full electronic search strategy.
Results from the search were firstly checked for duplicates. After duplicate studies were removed, the titles and abstracts were screened using the eligibility criteria (Table 1). Full texts of the selected studies were then further examined to find eligible studies. The authors of the included studies were not contacted for further clarification.
Data extracted included the following items: 1) authors; 2) animal species; 3) number of animals; 4) type of ration; 5) essential oil source; 6) experimental design, and 7) growth response variables. Growth response variables consisted of DMI, ADG, and FCR. Standard error or standard error of means were converted into standard deviation14. The data was pooled when a study used more than one dose of essential oils or tested both sexes of experimental animals15.
The overall effect size was quantified using Hedges’ g16 using a fixed-effect model. This model was chosen due to the insignificant heterogeneity among studies after checked using Cochran’s Q16 and I-square17.
Publication bias was inspected using Begg’s18 and Egger’s tests19, with P <0.10 set to determine the existence of publication bias. The trim and fill method20 was employed to detect the number of potential missing studies and to adjust the overall effect size. All meta-analysis procedures were performed using Meta-Essentials version 1.421.
Figure 1 shows the PRISMA flow diagram. A total of 137 records were identified through database searching. Of these, 12 studies were eligible for the current meta-analysis. The essential oil sources included oregano11,22–24, thyme25,26, chavil27, juniper7,28, and mixed product9,29. Unfortunately, one study did not define the source of essential oil8. The main characteristics of the included studies are shown in Table 3. Extracted data of outcome measures is available as Extended data30.
Authors | Species | n | Type of ration | EO source | Experimental design | Response variables |
---|---|---|---|---|---|---|
Aydin et al.24 | Sheep | 18 | Pasture grass + CF | Oregano | CRD | DMI, ADG, FCR |
Ribeiro et al.26 | Sheep | 40 | TMR | Thyme | RBD | DMI, ADG |
Lei et al.8 | Goats | 45 | TMR | NI | CRD | ADG |
Parvar et al.27 | Sheep | 40 | TMR | Chavil | CRD | DMI, ADG, FCR |
Canbolat et al.11 | Sheep | 40 | TMR | Oregano | CRD | DMI, ADG, FCR |
Yesilbag et al.28 | Goats | 18 | TMR | Juniper | CRD | ADG |
Gümüş et al.23 | Sheep | 24 | Wheat straw + CF | Oregano | CRD | ADG |
Baytok et al.25 | Sheep | 15 | Lucerne hay + CF | Thyme | RBD | ADG, FCR |
Malekkhahi et al.9 | Sheep | 10 | TMR | Mix A | CRD | DMI, FCR |
Özdoǧan et al.29 | Sheep | 20 | Alfalfa hay + CF | Mix B | RBD | DMI, ADG, FCR |
Canbolat and Karabulut22 | Sheep | 48 | TMR | Oregano | FD | ADG |
Chaves et al.7 | Sheep | 20 | TMR | Juniper | RBD | DMI, ADG, FCR |
n: number of experimental animals; CF: concentrate feed; TMR: total mixed ration; EO: essential oil; NI: no information; Mix A: a mixture of thymol, carvacrol, eugenol, limonene, and cinnamaldehyde EO; Mix B: a mixture of thyme leaf, daphne leaf, sage tea leaf, fennel seed, orange cortes, and myrtle leaf EO; CRD: completely randomized design; RBD: randomized block design; FD: factorial design; DMI: dry matter intake; ADG: average daily gain; FCR: feed conversion ratio.
Data of ADG from two studies11,25 were considered as outliers because their standardized residual was >|3| and thus were excluded from effect size quantification. Insignificant heterogeneity among studies was detected both for DMI (P of Q = 0.810; I-square = 0.00%), ADG (P of Q = 0.286; I-square = 17.61%), and FCR (P of Q = 0.650; I-square = 0.00%). As can be seen in Figure 2, the overall effect size showed that essential oil supplementation had no significant impact on DMI (P = 0.429) and FCR (P = 0.284), but had a significant positive impact on ADG (P = 0.002). The result of publication bias analysis showed that DMI, ADG, and FCR did not present any significant biases (P >0.10) (Table 4). The trim and fill method also did not detect any potential missing studies for all parameters.
DMI: dry matter intake; ADG: average daily gain; FCR: feed conversion ratio.
The current meta-analysis showed that dietary essential oils significantly increased ADG of small ruminants. This finding probably related to the antimicrobial activity of essential oils, which could reduce ruminal protozoa population31,32. Protozoa population may represent up to 50% of the total biomass of rumen microbes33. They have a negative impact on nitrogen utilization by ruminants because they engulf and digest bacteria, thus reducing microbial protein flow to abomasum34. Additionally, the presence of protozoa is also associated with methane production, which is responsible for the loss of up to 12% of gross energy intake by ruminants35. Thereby, the reduction of the ruminal protozoa population by essential oil could increase microbial protein, as well as energy supply, which ultimately could improve the growth rate of small ruminants.
This study provides insight of the potency of essential oil as a growth promoter for small ruminants. However, the current findings should be interpreted with caution due to the limited data available. Moreover, the literature search only covers published literature, which could lead to publication bias. For that reason, further research in this topic is highly encouraged to provide stronger evidence.
The current meta-analysis reveals that dietary essential oil could improve ADG of small ruminants, without any alteration on DMI and FCR. However, further research in this topic is still highly recommended to provide more robust evidence.
All data underlying the results are available as part of the article and no additional source data are required.
Figshare: Extended data for ‘The use of essential oils as a growth promoter for small ruminants: a systematic review and meta-analysis’. https://doi.org/10.6084/m9.figshare.12298913.v330.
This project contains extracted data of outcome measures (dry matter intake, average daily gain, and feed conversion ratio).
Figshare: PRISMA checklist for ‘The use of essential oils as a growth promoter for small ruminants: a systematic review and meta-analysis’. https://doi.org/10.6084/m9.figshare.12298034.v213.
Data are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication).
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Are the rationale for, and objectives of, the Systematic Review clearly stated?
Yes
Are sufficient details of the methods and analysis provided to allow replication by others?
Yes
Is the statistical analysis and its interpretation appropriate?
Yes
Are the conclusions drawn adequately supported by the results presented in the review?
Yes
Competing Interests: No competing interests were disclosed.
Reviewer Expertise: Agricultural production; Aquaculture production; Ecologic system; Conservation; Rural education and extension; Reproduction of animal (ex AI for animals); Nutrition on poultry, pigs, cattle, sheep, goat, dog and cat, etc.; Management for animal production; Animal house design and arrangement; Animal behavior and welfare; Feed processing; Animal waste management; Extension education.
Are the rationale for, and objectives of, the Systematic Review clearly stated?
Yes
Are sufficient details of the methods and analysis provided to allow replication by others?
Yes
Is the statistical analysis and its interpretation appropriate?
Yes
Are the conclusions drawn adequately supported by the results presented in the review?
Yes
Competing Interests: No competing interests were disclosed.
Reviewer Expertise: Small ruminant nutrition and livestock GHG emissions
Alongside their report, reviewers assign a status to the article:
Invited Reviewers | ||
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Version 1 01 Jun 20 |
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