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Less antibiotics in farm animals, less resistance

Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: a systematic review and meta-analysis.

Overview

Tang KL et al.. Lancet Planet Health 2017 · PMID 29387833 · DOI 10.1016/S2542-5196(17)30141-9

Restricting antibiotics in livestock reduced resistant bacteria in animals and, in fewer studies, in people.

Does the study support the specific claim? Yes · Methodological quality: high

Original publication

Plain-language summary

Study explained simply
What did the researchers want to find out?

Effect of restricting antibiotic use in food animals on resistance in animals and humans

How was the study done?

Systematic review and meta-analysis (WHO-commissioned)

How many people, animals or samples were studied?

181 studies (179 animal, 21 human); Food-producing animals; humans

What was actually found?

In animals resistance was usually 10-15 percentage points lower with restrictions (poultry 18 points); in studied humans 24 points lower, mainly in farm workers (29 points) and much less in non-farm people (9 points, 3 studies).

How large was the observed effect?

Random-effects risk differences

What do the results mean in everyday life?

Prudent farm antibiotic use protects human medicine.

What are the study's limitations?

Mostly cross-sectional, poorly adjusted studies; very high heterogeneity; few human studies, mostly farm workers; possible publication bias in human studies; almost no data from low- and middle-income countries.

What does it say about Elawady's specific claim?

Supports.

Do the results apply to Germany and Europe?

High.

What can explicitly not be concluded from this study?

Cannot quantify effect on all consumers.

Scientific in-depth review

1. Full reference

Authors
Tang KL et al.
Journal
Lancet Planet Health
Year
2017
Identifier
PMID 29387833 DOI 10.1016/S2542-5196(17)30141-9
Verification
verified – PubMed efetch 2026-10-25
Retracted
no
Corrections

Erratum: Lancet Planet Health 2017;1(9):e359

Extent checked
full text
Conflicts of interest and funding

Funded by WHO, which helped develop the question, design and protocol and peer-reviewed the search but had no role in extraction or interpretation. One author (JDK) reports Pfizer Canada and other vaccine-trial grants unrelated to the topic.

2. Research question

Effect of restricting antibiotic use in food animals on resistance in animals and humans

3. Study design and population

Study design
Meta-analysis – Systematic review and random-effects (DerSimonian-Laird) meta-analysis of observational and non-randomised intervention studies, commissioned by WHO AGISAR to inform WHO guidelines
Population

Food-producing animals; humans

Country

Multinational

Period

Databases searched from inception to 14 July 2016, updated 27 January 2017

Sample size

181 studies (179 animal, 21 human; 19 overlap); meta-analysed: 81 animal and 13 human studies. Animal designs: 126 cross-sectional, 50 longitudinal, 3 non-randomised trials; poultry (broilers/turkeys) in 87 studies.

Inclusion and exclusion criteria

Original studies of any intervention reducing antibiotic use in food-producing animals (bans, organic, antibiotic-free/free-range, voluntary reduction, stewardship) with a non-restricted comparator (historical allowed), reporting genotypic/phenotypic resistance in animals or humans; no language, date or quality limits. Pooling only if >=6 studies.

4. Methods and endpoints

Exposure / intervention

Restriction of antibiotic use

Comparator

No restriction

Endpoints

Prevalence of resistant bacteria

Statistical methods

Absolute risk differences by antibiotic class within five pre-specified animal groupings and one human meta-analysis; random effects; Q and I2; stratified analyses and meta-regression; quality per adapted Downs and Black checklist (duplicate); Begg's test and trim-and-fill for publication bias.

5. Actual results

Results

Animals: most pooled risk differences -0.10 to -0.15 (range -0.01 for cephalosporins in Enterobacteriaceae faecal samples, 95% CI -0.04 to 0.01, to -0.39 for macrolides in Enterococcus faecal samples, -0.56 to -0.23); e.g. tetracyclines -0.16 (-0.27 to -0.05), quinolones -0.01 (-0.02 to 0.00); poultry stratum -0.18 (-0.22 to -0.14); I2 51.3-99.4%. Humans (13 studies): pooled RD -0.24 (-0.42 to -0.06), I2 97.4%; farm workers and household members -0.29 (-0.54 to -0.04) vs non-farm workers -0.09 (-0.13 to -0.05; 3 studies). Lower-quality studies tended to show larger effects. Begg's test p=0.16 (animal), p=0.047 (human); trim-and-fill human RD -0.27 (-0.43 to -0.10).

Absolute risks

Absolute reductions in the proportion of resistant isolates mostly 10-15 percentage points in animals; 24 percentage points lower prevalence of resistant bacteria in studied humans (9 in non-farm populations, 3 studies).

Authors' conclusion

Restrictions associated with reduced resistance in animals; smaller evidence in humans; general population implications less clear.

6. Strengths

  • Very comprehensive search of 9 databases plus grey literature, experts and WHO GDG; no language restriction
  • Duplicate screening (kappa 0.74), extraction and quality assessment
  • Pre-specified analytic groupings, stratified analyses and publication-bias assessment
  • Absolute risk differences reported

7. Weaknesses

  • Underlying studies mostly cross-sectional with few adjusting for confounders
  • Extreme heterogeneity (I2 up to 99.4%; human 97.4%)
  • Human evidence limited (13 pooled studies), mostly farm workers; only 3 studies in non-farm populations
  • Possible publication bias in human studies (Begg p=0.047)
  • Lower-quality studies overestimate effects
  • Almost no data from major antibiotic-using countries (one study from India, China or Brazil); none from Egypt
  • Protocol pre-determined but no registration number given in retrieved text

8. Risk of bias

Orienting tool
AMSTAR 2
Type of assessment
structured assessment based on the full text by a single reviewer (no formal double review)
Full formal assessment
no
Overall risk of bias
some concerns
Rationale

AMSTAR 2 overall confidence: moderate to low (no critical flaw clearly present; non-critical weaknesses and unverifiable excluded-study list). Overall unchanged (some_concerns). Single-reviewer structured judgement; a formal assessment needs two independent reviewers and the protocol.

8. Risk of bias
DomainJudgementRationale
1 PICO componentslowPopulation, intervention, comparator and outcome clearly specified.
2 Protocol established a priori (critical)some concerns'Predetermined protocol' developed with WHO, but no registration reported in the retrieved text.
3 Explanation of included designslowInclusive approach justified to be comprehensive; quality handled by sensitivity analyses.
4 Comprehensive search (critical)lowNine databases, grey literature, reference lists, conference proceedings, experts; no language limits.
5 Duplicate selectionlowTwo reviewers independently (kappa 0.74).
6 Duplicate extractionlowTwo reviewers extracted data.
7 List of excluded studies with reasons (critical)some concernsFlow diagram with exclusion categories; full excluded list not visible in retrieved text (appendix not available).
8 Description of included studieslowStudy characteristics tabulated and in appendix.
9 Risk of bias of individual studies (critical)lowAdapted Downs and Black criteria applied in duplicate.
10 Funding of included studieshighNot reported.
11 Appropriate meta-analytic methods (critical)some concernsRandom effects and minimum of 6 studies, but pooling of very heterogeneous, mostly unadjusted cross-sectional data (I2 up to 99.4%).
12 Impact of RoB on resultslowStratified analyses by quality criteria and meta-regression.
13 RoB considered in interpretation (critical)lowAuthors state human evidence less robust and lower-quality studies overestimate effects.
14 Heterogeneity explainedsome concernsExplored by stratification/meta-regression; largely unexplained.
15 Publication bias (critical)lowFunnel plots, Begg's test, trim-and-fill reported.
16 Conflicts of interest of reviewlowFunding and author interests declared; WHO role described.

Full-text review (25 October 2026): Added search dates/databases, design mix (126 cross-sectional), poultry stratum RD -0.18, class-specific RDs, I2 values, human subgroups (farm workers -0.29 vs non-farm -0.09), Begg's tests, WHO role and COI; AMSTAR 2 itemised. Bias unchanged.

9. Assessment of the statistical interpretation

Consistent direction across species, bacteria and quality strata supports a real association, but pooled magnitudes are uncertain given heterogeneity and confounding. Evidence for transmission to the general (non-farm) population via food is weak and indirect.

10. Relevance to the specific claim

C-CHK-05.

11. Independent contrary findings

Not applicable.

12. Transferability to Germany and Europe

High: most studies from Europe and North America; EU has banned antibiotic growth promoters since 2006.

13. Overall methodological judgement

High-quality, WHO-commissioned review showing that restricting antibiotic use in food animals is associated with less resistance in animals (including poultry) and in people with direct animal contact; the effect on consumers in general is plausible but poorly quantified.

Multidimensional assessment
Multidimensional assessment
Authenticity of the sourceverified
Methodological qualityhigh
Risk of biassome concerns
Precision of resultsmoderate
Directnessdirect
Reproducibilityreplicated
Consistency with the overall evidenceconsistent
Regional transferabilityhigh
Adequacy of the interpretation (by the archive)not applicable

14. Open questions

Effect on general consumers via food; data from low- and middle-income countries including Egypt; resistome-level effects.

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