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Systematic Review
Revised

The use of essential oils as a growth promoter for small ruminants: a systematic review and meta-analysis

[version 2; peer review: 2 approved]
PUBLISHED 28 Aug 2020
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Abstract

Background: Due to their antimicrobial properties and safety, essential oils are currently proposed as a sustainable option for antibiotic alternatives in the livestock sector. This current systematic review and meta-analysis investigated the effects of dietary essential oil supplements on dry matter intake (DMI), average daily gain (ADG), and feed conversion ratio (FCR) of small ruminants.
Methods: A total of 12 studies (338 small ruminants) were included in this meta-analysis. The overall effect size was quantified using Hedges’ g with 95% confidence interval (CI) using a fixed-effect model. Publication bias was inspected using Begg’s and Egger’s tests, followed by trim and fill method to detect the number of potential missing studies.
Results: Insignificant heterogeneity among studies was detected both on 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%). The overall effect size showed that essential oils supplementation had no significant impact on DMI (Hedges’ g = -0.12; 95% CI = -0.50 to 0.26; P = 0.429) and FCR (Hedges’ g = -0.17; 95% CI = -0.55 to 0.22; P = 0.284), but had a significant positive impact on ADG (Hedges’ g = 0.44; 95% CI = 0.12 to 0.76; P = 0.002). The result of publication bias analysis showed that DMI, ADG, and FCR did not present any significant biases ( P > 0.10), and no potential missing studies detected.
Conclusions: Dietary essential oil could improve ADG of small ruminants, without any alteration on DMI and FCR. Further research in this topic is still required to provide stronger evidence of the potency of essential oil as a growth promoter for small ruminants.

Keywords

Antibiotics alternative, Average daily gain, Goats, Natural feed additives, Protozoa, Secondary metabolites, Sheep.

Revised Amendments from Version 1

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

Introduction

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.

Methods

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.

Eligibility criteria

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.

Table 1. PICOS criteria.

Inclusion criteriaExclusion criteria
ParticipantsSheep or goatOther species
InterventionsDietary essential oil
supplementation
Irrelevant
treatment
ComparisonsControl group (basal
diet only)
OutcomesDMI, ADG, and FCRNo related
outcome
Study designRandomized controlled
in vivo trials
In vitro trials

DMI: dry matter intake; ADG: average daily gain; FCR: feed conversion ratio.

Literature search strategy

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.

Table 2. Search strategy.

DatabaseSearch strategy
Scopus(TITLE (oil) AND TITLE (growth OR performance)
AND TITLE (sheep OR goat OR lamb OR kid))
PubMed((oil[Title]) AND (growth[Title] OR
performance[Title])) AND (sheep[Title] OR
goat[Title] OR lamb[Title] OR kid[Title])
SciELO(ti:(oil)) AND (ti:(growth OR performance)) AND
(ti:(sheep OR goat OR lamb OR kid))

Study selection

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 extraction

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.

Effect size quantification

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 analysis

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.

Results

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 oregano11,2224, 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.

8a18167e-5574-429b-a066-3f4849d21afa_figure1.gif

Figure 1. PRISMA flow diagram.

Table 3. Main characteristics of the studies included in the meta-analysis.

AuthorsSpeciesnType of rationEO sourceExperimental
design
Response variables
Aydin et al.24Sheep18Pasture grass + CFOreganoCRDDMI, ADG, FCR
Ribeiro et al.26Sheep40TMRThymeRBDDMI, ADG
Lei et al.8Goats45TMRNICRDADG
Parvar et al.27Sheep40TMRChavilCRDDMI, ADG, FCR
Canbolat et al.11Sheep40TMROreganoCRDDMI, ADG, FCR
Yesilbag et al.28Goats18TMRJuniperCRDADG
Gümüş et al.23Sheep24Wheat straw + CFOreganoCRDADG
Baytok et al.25Sheep15Lucerne hay + CFThymeRBDADG, FCR
Malekkhahi et al.9Sheep10TMRMix ACRDDMI, FCR
Özdoǧan et al.29Sheep20Alfalfa hay + CFMix BRBDDMI, ADG, FCR
Canbolat and Karabulut22Sheep48TMROreganoFDADG
Chaves et al.7Sheep20TMRJuniperRBDDMI, 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.

8a18167e-5574-429b-a066-3f4849d21afa_figure2.gif

Figure 2. Forest plot of the effect of essential oil supplementation on growth response of small ruminants.

DMI: dry matter intake; ADG: average daily gain; FCR: feed conversion ratio.

Table 4. Summary of publication bias analysis of the effect of dietary essential oil intervention on growth response of small ruminants.

ParametersP of Begg’s testP of Egger’s testMissing studies
DMI0.6520.8790
ADG1.0000.6050
FCR0.6520.4630

DMI: dry matter intake; ADG: average daily gain; FCR: feed conversion ratio.

Discussion

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.

Conclusions

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.

Data availability

Underlying data

All data underlying the results are available as part of the article and no additional source data are required.

Extended data

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).

Reporting guidelines

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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Andri F, Huda AN and Marjuki M. The use of essential oils as a growth promoter for small ruminants: a systematic review and meta-analysis [version 2; peer review: 2 approved]. F1000Research 2020, 9:486 (https://doi.org/10.12688/f1000research.24123.2)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Current Reviewer Status: ?
Key to Reviewer Statuses VIEW
ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
Version 1
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PUBLISHED 01 Jun 2020
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Reviewer Report 01 Jul 2020
Liang Chou Hsia, Department of Tropical Agriculture and International Cooperation, National Pingtung University of Science and Technology, Pingtung, Taiwan 
Approved
VIEWS 15
The main purpose of this paper tries to investigate whether essential oils have any positive or negative effects on growth performance, such as dry matter intake (DMI), average daily gain (ADG), and feed conversion ratio (FCR). The results shown that ... Continue reading
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HOW TO CITE THIS REPORT
Hsia LC. Reviewer Report For: The use of essential oils as a growth promoter for small ruminants: a systematic review and meta-analysis [version 2; peer review: 2 approved]. F1000Research 2020, 9:486 (https://doi.org/10.5256/f1000research.26610.r64168)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 28 Aug 2020
    Faizal Andri, Doctoral Program of Animal Science, Faculty of Animal Science, Gadjah Mada University, Yogyakarta, 55281, Indonesia
    28 Aug 2020
    Author Response
    We would like to thank the reviewer for his helpful comments and suggestions. Please see our responses and changes as detailed below.
     
    1. Please indicate the original words and ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 28 Aug 2020
    Faizal Andri, Doctoral Program of Animal Science, Faculty of Animal Science, Gadjah Mada University, Yogyakarta, 55281, Indonesia
    28 Aug 2020
    Author Response
    We would like to thank the reviewer for his helpful comments and suggestions. Please see our responses and changes as detailed below.
     
    1. Please indicate the original words and ... Continue reading
Views
20
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Reviewer Report 17 Jun 2020
C.J. Linde du Toit, Department of Animal and Wildlife Sciences, University of Pretoria, Pretoria, South Africa 
Approved
VIEWS 20
In this article the researchers conducted a meta analysis on the effects of essential oils on production parameters of small ruminants. 

This is a well written article. The objective and methods employed are suitable and clearly defined within ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
du Toit CJL. Reviewer Report For: The use of essential oils as a growth promoter for small ruminants: a systematic review and meta-analysis [version 2; peer review: 2 approved]. F1000Research 2020, 9:486 (https://doi.org/10.5256/f1000research.26610.r64169)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 28 Aug 2020
    Faizal Andri, Doctoral Program of Animal Science, Faculty of Animal Science, Gadjah Mada University, Yogyakarta, 55281, Indonesia
    28 Aug 2020
    Author Response
    We are grateful to the reviewer for his valuable comments and suggestions. Please see our responses and changes as detailed below.
     
    1. The authors could have included the experimental ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 28 Aug 2020
    Faizal Andri, Doctoral Program of Animal Science, Faculty of Animal Science, Gadjah Mada University, Yogyakarta, 55281, Indonesia
    28 Aug 2020
    Author Response
    We are grateful to the reviewer for his valuable comments and suggestions. Please see our responses and changes as detailed below.
     
    1. The authors could have included the experimental ... Continue reading

Comments on this article Comments (0)

Version 2
VERSION 2 PUBLISHED 01 Jun 2020
Comment
Alongside their report, reviewers assign a status to the article:
Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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