EFSA Journal 2012;10(6):2740

SCIENTIFIC OPINION1

Guidance on the assessment of bacterial susceptibility to antimicrobials of

human and veterinary importance2
EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP)3,4

European Food Safety Authority (EFSA), Parma, Italy

ABSTRACT
This Guidance document is intended to provide a method to identify resistance to antimicrobials of human and
veterinary importance in bacterial strains intended for use as feed additives. Such tests should be made in a
consistent manner using internationally recognised and standardised methods. As a basic requirement, the
minimum inhibitory concentration of the antimicrobials should be determined for each of the following
substances: ampicillin, vancomycin, gentamicin, kanamycin, streptomycin, erythromycin, clindamycin,
tetracycline, chloramphenicol and, in specific cases, tylosine, apramycin, nalidixic acid, sulfonamide and
trimethoprim. These antimicrobials are chosen to detect a wide range of determinants for resistance. The cut-off
values identified by the FEEDAP Panel should be seen as a pragmatic response intended to introduce
consistency in the separation of strains with acquired resistance from susceptible strains. These values are not
intended for any purpose other than the assessment of microbial products for the possible presence of
antimicrobial resistance. When a bacterial strain demonstrates higher resistance to a specific antimicrobial than
the other strains of the same taxonomical unit, the presence of acquired resistance is indicated and additional
information is needed on the genetic basis of the antimicrobial resistance. Any bacterial strain carrying an
acquired resistance to antimicrobial that is shown to be due to the acquisition of genetic determinant presents the
greatest potential for horizontal spread and should not be used as a feed additive.

© European Food Safety Authority, 2012

KEY WORDS
Antimicrobial, guidance, safety, resistance, bacteria

1
This guidance document replaces the previous EFSA opinion on the updating of the criteria used in the assessment of
bacteria for resistance to antibiotics of human or veterinary importance, adopted on 18 June 2008. (EFSA-Q-2008-004)
2
On request from EFSA, Question No EFSA-Q-2011-01108, adopted on 23 May 2012. Revision 2 – 20/11/2012: minor
editorial changes.
3
Panel members: Gabriele Aquilina, Georges Bories, Andrew Chesson, Pier Sandro Cocconcelli, Joop de Knecht, Noël
Albert Dierick, Mikolaj Antoni Gralak, Jürgen Gropp, Ingrid Halle, Christer Hogstrand, Lubomir Leng, Secundino López
Puente, Anne-Katrine Lundebye Haldorsen, Alberto Mantovani, Giovanna Martelli, Miklós Mézes, Derek Renshaw,
Maria Saarela, Kristen Sejrsen and Johannes Westendorf. Correspondence: FEEDAP@efsa.europa.eu
4
Acknowledgement: The Panel wishes to thank wishes to thank the members of the Working Group on Micro-organisms,
including Atte von Wright and Roland Leclercq, for the preparation of this opinion.

Suggested citation: EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP); Guidance on the
assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA Journal 2012;10(6):2740.
[10 pp.] doi:10.2903/j.efsa.2012.2740. Available online: www.efsa.europa.eu/efsajournal

© European Food Safety Authority, 2012

 Guidance on the assessment of bacterial antimicrobial susceptibility

TABLE OF CONTENTS
Abstract .................................................................................................................................................... 1
Table of contents ...................................................................................................................................... 2
Introduction .............................................................................................................................................. 3
1. Criteria for identifying bacterial strains with acquired resistance to antimicrobials ...................... 3
1.1. Microbiological cut-off values ............................................................................................... 4
1.2. Quantitative methods for the MIC determination ................................................................... 6
2. Defining the genetic basis of resistance .......................................................................................... 6
References ................................................................................................................................................ 8

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 Guidance on the assessment of bacterial antimicrobial susceptibility

INTRODUCTION
The development of resistance amongst bacteria to antimicrobials remains a serious concern. For this
reason, viable micro-organisms used as the active agent(s) in feed additives should not add to the pool
of antimicrobial resistance genes already present in the gut bacterial population or otherwise increase
the risk of transfer of drug resistance.

The European Food Safety Authority (EFSA) requires as part of its Qualified Presumption of Safety
approach to the safety assessment of bacteria deliberately introduced in the food chain, that acquired
resistance determinants to antimicrobials of clinical importance are absent.

When resistance to an antimicrobial is inherent to a bacterial species, it is generally referred to as

‘intrinsic resistance’ (sometimes called ‘natural resistance’) and is typical of all the strains of that
species. In contrast, when a strain of a typically susceptible species is resistant to a given
antimicrobial drug, it is considered to be ‘acquired resistance’. Acquired resistance can be due either
to added genes (genes acquired by the bacteria via gain of exogenous DNA) or to the mutation of
indigenous genes (Ammor et al, 2007; van Reenen and Dicks, 2011).

The actual possibility of the transfer of resistance to human or animal pathogenic bacteria, which
could result from the use of microbial products based on drug-resistant strains, is related to the genetic
basis of resistance. Although it is reasonable to assume that gene transfer from viable micro-
organisms to other micro-organisms will occur in an open environment such as the gastrointestinal
tract, intrinsic resistance is presumed to present a minimal potential for horizontal spread, whereas
acquired resistance mediated by added genes is considered as having a high potential for lateral
spread (Devirgiliis et al, 2011; van Reenen and Dicks, 2011).

Added genes are the result of gene exchange between bacteria. The presence of added genes coding
for antimicrobial resistance, particularly when carried by mobile genetic elements, presents the
greatest risk for horizontal dissemination of resistance. Antibiotic resistance (AR) genes database
ARDB (http://ardb.cbcb.umd.edu/) provides a centralized compendium of information on antibiotic
resistance by providing a non-comprehensive list of AR gene sequences. Resistance by mutation of
chromosomal genes presents a low risk of horizontal dissemination (Devirgiliis., 2011; van Reenen
and Dicks, 2011).

In principle, the selection of micro-organisms for use as feed additives should be oriented towards the
least resistant organism whenever possible.

This guidance document replaces the previous EFSA opinion on the updating of the criteria used in
the assessment of bacteria for resistance to antibiotics of human or veterinary importance, adopted in
2008 (EFSA, 2008). It will be subject to regular updating when data from the scientific community
and other relevant sources (e.g., the European Medicines Agency, the European Centre of
Diseases Prevention and Control) become available.

1. CRITERIA FOR IDENTIFYING BACTERIAL STRAINS WITH ACQUIRED RESISTANCE TO

ANTIMICROBIALS

All bacterial products intended for use as feed additives must be examined to establish the
susceptibility of the component strain(s) to a relevant range of antimicrobials of human and veterinary
importance. It is essential that such tests are made in a consistent manner using internationally
recognised and standardised methods. As a basic requirement, the minimum inhibitory concentration
(MIC) of the antimicrobials expressed as mg/L or µg/mL should be determined for each of the
following substances: ampicillin, vancomycin, gentamicin, kanamycin, streptomycin, erythromycin,
clindamycin, tetracycline, chloramphenicol and, in specific cases, tylosine, apramycin, nalidixic acid,

EFSA Journal 2012;10(6):2740 3

 Guidance on the assessment of bacterial antimicrobial susceptibility

sulfonamide and trimethoprim (see Table 1). These antimicrobials are chosen to detect a wide range
of determinants for resistance.

1.1. Microbiological cut-off values

For the purpose of distinguishing resistant from susceptible strains, the FEEDAP Panel defines
microbiological cut-off values. Microbiological cut-off values are set by studying the distribution of
MICs of the chosen antimicrobials in bacterial populations belonging to a single taxonomical unit
(species or genus). The part of the population that clearly deviates from the normal susceptible
populations is categorised as resistant. The data used for the definition of microbiological cut-off
values, as reported in Table 1, were derived from the published body of research, the European
Committee on Antimicrobial Susceptibility Testing (EUCAST, http://www.eucast.org/), and from
national and European monitoring programmes.

For the assessment of bacteria used as feed additives, strains can be categorised as susceptible or
resistant to antimicrobials:

Susceptible (S): a bacterial strain is defined as susceptible when it is inhibited at a

concentration of a specific antimicrobial equal or lower than the established cut-off value (S ≤
x mg/L).
Resistant (R): a bacterial strain is defined as resistant when it is not inhibited at a
concentration of a specific antimicrobial higher than the established cut-off value (R > x
mg/L).
The cut-off values identified should be seen as a pragmatic response intended to introduce
consistency in the separation of strains with acquired resistance from susceptible strains. The cut-off
values are not intended for any purpose other than the assessment of microbial products for the
possible presence of antimicrobial resistance.

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 Guidance on the assessment of bacterial antimicrobial susceptibility

Table 1. Microbiological cut-off values (mg/L)

chloramphenicol
erythromycin
streptomycin

clindamycin
vancomycin

tetracycline
gentamicin

kanamycin
ampicillin
Lactobacillus obligate homofermentativea 1 2 16 16 16 1 1 4 4

Lactobacillus acidophilus group 1 2 16 64 16 1 1 4 4

Lactobacillus obligate heterofermentativeb 2 n.r. 16 32 64 1 1 8 4

Lactobacillus reuteri 2 n.r. 8 64 64 1 1 16 4
c
Lactobacillus facultative heterofermentative 4 n.r. 16 64 64 1 1 8 4
Lactobacillus plantarum/pentosus 2 n.r. 16 64 n.r. 1 2 32 8
Lactobacillus rhamnosus 4 n.r. 16 64 32 1 1 8 4
Lactobacillus casei /paracasei 4 n.r. 32 64 64 1 1 4 4

Bifidobacterium 2 2 64 n.r. 128 1 1 8 4

Pediococcus 4 n.r. 16 64 64 1 1 8 4
Leuconostoc 2 n.r. 16 16 64 1 1 8 4
Lactococcus lactis 2 4 32 64 32 1 1 4 8
Streptococcus thermophilus 2 4 32 64 64 2 2 4 4
Bacillus spp n.r. 4 4 8 8 4 4 8 8
Propionibacterium 2 4 64 64 64 0.5 0.25 2 2
Other Gram + 1 2 4 16 8 0.5 0.25 2 2
n.r. not required.
a
including L. delbrueckii, L. helveticus
b
including L. fermentum
c
including the homofermentative species L. salivarius

chloramphenicol
erythromycin
streptomycin

clindamycin
vancomycin

tetracycline
gentamicin

kanamycin
ampicillin

tylosine

Enterococcus faecium 2 4 32 1024 128 4 4 4 4 16

chloramphenicol

nalidixic acid

trimethoprim
streptomycin

sulfonamide
tetracycline
gentamicin

kanamycin

apramycin
ampicillin

Escherichia coli 8 2 8 16 8 16 16 256 2 8

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 Guidance on the assessment of bacterial antimicrobial susceptibility

The content of Table 1 is reviewed on a regular basis and modified as necessary when new data are
made available.

1.2. Quantitative methods for the MIC determination

For the assessment of the susceptibility to antimicrobials of bacterial strains, serial two-fold dilution
procedures in agar or broth should be used and include relevant quality control strains. The tests
should be performed according to internationally recognised standards such as the Clinical and
Laboratory Standard Institute (CLSI; www.clsi.org), ISO standard or similar. An ISO standard is
currently available for bifidobacteria and non-enterococcal lactic acid bacteria (ISO 10932:2010 (IDF
223:2010)) . After incubation, the MIC is defined as the lowest concentration of the antimicrobial that
inhibits bacterial growth. Qualitative or semi-qualitative methods to determine MIC indirectly, such
as diffusion methods, are generally not acceptable. The existing body of scientific information related
to that specific or related bacterial species must be considered when the procedure for MIC
determination (dilution method, growth media and incubation conditions) is chosen, keeping in mind
the possible interference of media and growth conditions.

2. DEFINING THE GENETIC BASIS OF RESISTANCE

The detection of the MIC above the cut-off values, identified by the FEEDAP Panel for one or more
antimicrobials, requires further investigation to determine the nature of the resistance. Initially, it may
be necessary to make the distinction between acquired and intrinsic resistance. This would only arise
when there is limited or no information on the MIC distribution within the considered taxonomical
unit. In these cases the structural nature and genetic basis of the resistance must be demonstrated
analysing a representative selection of strains belonging to that taxonomical unit. Since intrinsic
resistance is specific for a bacterial species or genus, an indispensable pre-requisite is the correct
identification of the strain at species level by means of molecular taxonomy methods. Where all
strains within a given taxonomic group show phenotypic resistance to an antimicrobial, such
resistance can be considered intrinsic to the taxonomic group.

When a bacterial strain demonstrates higher resistance to a specific antimicrobial than the other
strains of the same taxonomical unit, the presence of acquired resistance is indicated and additional
information is needed on the genetic basis of the antimicrobial resistance. A single exception to this
approach is E. faecium and ampicillin. Strains with ampicillin MIC >2 µg/mL are not considered
suitable for feed use since this is a marker for the hospital associated clade and not considered safe.5

Acquired resistance can be due either to acquired genes (genes acquired by the bacteria via gain of
exogenous DNA) or to the mutation of indigenous genes. The absence of known antimicrobial
resistance genes (e.g. based on analysis utilising the ARBD) is not sufficient to explain the nature of
the detected resistance.

The scheme proposed by the FEEDAP Panel for the antimicrobial resistance assessment of a bacterial
strain used as a feed additive is shown in Figure 1.

5
See Guidance on the safety assessment of Enterococcus faecium in animal nutrition at
http://www.efsa.europa.eu/en/efsajournal/pub/2682.htm

EFSA Journal 2012;10(6):2740 6

 Guidance on the assessment of bacterial antimicrobial susceptibility

Figure 1. Proposed scheme for the antimicrobial resistance assessment of a bacterial strain used as
a feed additive

Molecular taxonomy

Quantitative MIC determination

MIC ≤ cut-off MIC > cut-off

ACCEPTABLE Genetic basis of resistance

Acquired Demonstration of
intrinsic resistance

Acquired resistance ACCEPTABLE

Added genes Demonstration of

genomic mutation
genomic mutation

GENERALLY
NOT ACCEPTABLE ACCEPTABLE

The FEEDAP Panel considers that:

Any bacterial strain carrying an intrinsic resistance to antimicrobial(s) presents a minimal

potential for horizontal spread and thus, may be used as a feed additive

Any bacterial strain carrying an acquired resistance to antimicrobial(s) that is shown to be

due to chromosomal mutation(s) presents a low potential for horizontal spread and generally
may be used as a feed additive

Any bacterial strain carrying an acquired resistance to antimicrobial(s) that is shown to be

due to the acquisition of genetic determinant(s) presents the greatest potential for horizontal
spread and should not be used as a feed additive

In the absence of information on the genetic nature of a demonstrated resistance, the strain
should not be used as a feed additive

EFSA Journal 2012;10(6):2740 7

 Guidance on the assessment of bacterial antimicrobial susceptibility

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