Antimicrobial resistance of Staphylococcus aureus

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L. Intorre et al. Large Animal Review 2013; 19: 287-291
287
Antimicrobial resistance of Staphylococcus
aureus isolated from bovine milk in Italy
from 2005 to 2011
L. INTORREa, M. VANNIa, V. MEUCCIa, R. TOGNETTIa, D. CERRIa, B. TURCHIa,
G. CAMMIb, N. ARRIGONIb, C. GARBARINOb
a
b
Dipartimento di Scienze Veterinarie, Università di Pisa
Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna, Sezione di Piacenza
SUMMARY
Introduction - Bovine mastitis is a major cause of economic losses in the dairy sector and Staphylococcus aureus represents the
most prevalent and contagious aetiologic agent, resulting responsible for about one-third of clinical and subclinical mastitis
worldwide. β-lactams, lincosamides and macrolides are among the most recommended antimicrobial agents for treating mastitis and increasing level of acquired resistance to penicillin G, lincomycin, erythromycin, gentamycin and streptomycin has
been reported. Therefore, antimicrobial susceptibility tests are important for the selection of the most appropriate antimicrobial agent for treatment of bovine mastitis caused by S. aureus.
Aim - The aim of this retrospective study was to evaluate the antimicrobial resistance rates and the trend in resistance of S. aureus strains isolated from bovine with clinical or sub-clinical mastitis in Italy from 2005 to 2011.
Materials and methods - A total of 1,200 S. aureus isolates recovered from milk samples from bovine with clinical or sub-clinical mastitis were collected from 2005 to 2011 at the Diagnostic Sections of Piacenza of the Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna and tested for antimicrobial susceptibility by the disk diffusion method.
Results and discussion - High resistance rates were observed mostly for penicillin G, erythromycin and lincomycin, while a
high in vitro activity was showed by trimethoprim-sulfamethoxazole and cefquinome, confirming these antimicrobial agents
as an alternative choice for the treatment of bovine mastitis. Resistance showed a significant increasing trend for cephalotin,
cefquinome, enrofloxacin, lincomycin, nafcillin, oxacillin and tetracycline, while resistance to amoxicillin/clavulanic acid, cefoperazone, erythromycin, penicillin G and trimethoprim-sulfamethoxazole did not change significantly over the study period.
Conclusions - Periodic surveillance for antimicrobial resistance of S. aureus isolated from dairy cows with mastitis is strongly
recommended as an important component of prudent antimicrobial use practices.
KEY WORDS
Staphylococcus aureus / bovine mastitis / antimicrobial resistance / trend / Italy.
INTRODUCTION
Bovine mastitis is the most prevalent disease in dairy herds
worldwide, with average incidence rates of 30-50% reported
in many countries, and decrease in milk production due to
clinical and subclinical mastitis is widely recognized as the
main cause of the economic losses in the dairy sector1.
Among the several different causes of intra-mammary infections in dairy cattle, Staphylococcus aureus represents the
most prevalent and contagious aetiologic agent, resulting responsible for about one-third of clinical and subclinical mastitis worldwide2. In addition to the causative infective agent,
the environment is another major factor involved in mastitis
representing a considerable reservoir of pathogens, so that
“environmental mastitis” is more prevalent than contagious
transmission between animals in some countries3.
Although the environmental factors may be controlled through appropriate management practices, such as the use of
proper milking procedures and culling of chronically infec-
Autore per la corrispondenza:
Michele Vanni ([email protected]).
ted animals, antimicrobial therapy continues to be a primary
tool to control staphylococcal mastitis. β-lactams, particularly penicillin G, are considered as first choice for treating
mastitis due to penicillin-susceptible S. aureus, while lincosamides and macrolides represent an alternative in case of βlactamase-producing isolates4. Although S. aureus isolated
from bovine mastitis is generally reported as susceptible to
antimicrobials commonly used in animal husbandry, including β-lactams, macrolides, lincosamides and aminoglycosides5, increasing level of acquired resistance to penicillin G,
lincomycin, erythromycin, gentamycin and streptomycin has
been reported6. Moreover, multi-resistant strains, defined as
strains resistant to at least three different antimicrobial classes7, have recently emerged, mainly due to the rapid spread of
methicillin-resistant S. aureus (MRSA) and the detection of
methicillin- and multi-resistant S. aureus in milk or dairy
cattle have recently expanded in many countries8. Therefore,
antimicrobial susceptibility tests are important for the selection of the most appropriate antimicrobial agent for treatment of bovine mastitis caused by S. aureus.
The aim of the present study was to retrospectively investigate the trends in antimicrobial resistance of S. aureus strains
isolated from bovine with clinical or sub-clinical mastitis in
Italy from 2005 to 2011.
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Antimicrobial resistance of Staphylococcus aureus isolated from bovine milk in Italy from 2005 to 2011
MATERIALS AND METHODS
Bacterial strains
A total of 1,200 S. aureus isolates, recovered from milk samples from bovine with clinical or sub-clinical mastitis were
included in this study. The isolates were collected from 2005
to 2011 at the Diagnostic Sections of Piacenza of the Istituto
Zooprofilattico Sperimentale della Lombardia e dell’Emilia
Romagna, which routinely receives more than 40,000 milk
samples a year from bovine farms located in central and
northern Italy. No more than one isolate of S. aureus from
the same herd per year was included in the study. Animals
have not been treated with antimicrobial agents in the 3
weeks prior to sample collection. Bacterial strains were isolated on Aesculin Blood Agar (Oxoid, Milano, Italy) at 37°C
for 24 h and routinely identified on the basis of colony
morphology, Gram staining, and free coagulase test (Coagulase Plasma EDTA, Biolife Italiana, Milano, Italy). Identification was confirmed by using the API ID32STAPH system
(bioMérieux, Marcy l’Etoile, France) according to the manufacturer’s instructions. All isolates were immediately subcultured on Brain Heart Infusion broth and subjected to antimicrobial susceptibility testing.
Antimicrobial susceptibility testing
S. aureus isolates were routinely tested for their susceptibility
to a panel of antimicrobials by the disk diffusion method9 on
Mueller Hinton Agar (Oxoid, Milano, Italy). The following
antimicrobial agents were tested: amoxicillin/clavulanic acid
(20 µg/10 µg), cephalotin (30 µg), cefoperazone (75 µg), cefquinome (30 µg), enrofloxacin (5 µg), erythromycin (15 µg),
lincomycin (15 µg), penicillin G (10 IU, International Units),
oxacillin (1 µg), nafcillin (1 µg), tetracycline (30 µg), and trimethoprim/sulfamethoxazole (1.25/23.75 µg). The choice of
antimicrobials to be tested over the seven-year period was
based on the requests of submitting veterinarians, as well as
on the basis of specific fields requirements. This resulted in a
“core number” of 703 out of 1,200 S. aureus isolates which
were tested for susceptibility against all the considered antimicrobials, while the remaining 497 isolates were tested with
a variable number of the above mentioned antimicrobials.
Regular quality assurance by using the American Type Culture Collection reference strain of S. aureus (ATCC 25923,
Oxoid, Milano, Italy) was performed. Isolates were classified
as resistant or susceptible towards the tested antimicrobials
in accordance with breakpoints proposed by the Clinical and
Laboratory Standards Institute10,11,12, except for enrofloxacin
and lincomycin for which standards and criteria of the Comité de l’Antibiogramme de la Société Française de Microbiologie were applied13. Intermediate isolates were grouped
with the resistant ones.
Data and statistical analyses
Antimicrobial resistance rate of S. aureus was calculated for
each year as the number of resistant/intermediate isolates divided by the total number of tested isolates for a given antimicrobial. The χ2 test to determine the trend of resistance of S.
aureus towards the selected antimicrobials over the seven-year
period was performed. A trend was considered statistically significant for P<0.05. The regression coefficient, or slope, was
provided as well. The slope represented the mean change in
the antimicrobial susceptibility rate for every 1-year increase
in time. The direction of the trend was indicated by the sign of
the regression coefficient, a negative slope indicating a decrease in susceptibility over time, while a positive slope indicating
an increase in susceptibility over time. Statistical analyses were performed using the GraphPad Prism 5.0 for Windows
(GraphPad Software, San Diego, CA, USA).
RESULTS
The resistance rates and the trends in resistance of S. aureus
isolates towards individual antimicrobials are shown in Table
1. In 2011, the tested isolates resulted resistant mostly to lincomycin (92.6%) and penicillin G (63.1%), as well as to
erythromycin (41.7%), tetracycline (37.5%), enrofloxacin
(36.9%) and cefoperazone (36.1%), while only 3.3% showed
resistance to trimethoprim-sulfamethoxazole. Isolates
showed a statistically significant increasing trend of resistance over the whole study period to cephalotin (from 2.4 to
16.4%), cefquinome (from 1.2 to 12.3%), enrofloxacin (from
5.9 to 36.9%), lincomycin (from 90.5 to 92.6%), nafcillin
(from 1.2 to 16.4%), oxacillin (from 2.9 to 18.9%) and tetracycline (from 15.3 to 37.5%). No significant changes in resistance rates (P≥0.05) from 2005 to 2011 for amoxicillin/clavulanic acid, cefoperazone, erythromycin, penicillin G
and trimethoprim-sulfamethoxazole were found.
The antimicrobial resistance and multi-resistance patterns of
the “core number” of 703 out of 1,200 S. aureus isolates are
summarized in Tables 2 and 3, respectively. Forty-six isolates
(6.5%) showed no resistance towards all the tested antimicrobial agents. Sixty-seven different resistance patterns were
observed: 21.8%, 26.3%, 24% and 11.5% of the isolates resulted resistant to one, two, three and four antimicrobials, respectively, while 9.8% showed resistance from five to twelve
antimicrobial agents (Table 2). Multi-resistance was detected
in 216 out of 703 S. aureus strains of the “core number”
(30.7%) (Table 3). The large majority of multi-resistant isolates showed resistance towards three (18.8%) and four
(7.9%) antimicrobial classes, respectively, while less than 4%
showed resistance from five to seven antimicrobial classes.
The most prevalent multi-resistance pattern, shown by 73
isolates, included resistance towards β-lactams, lincosamides
and macrolides.
DISCUSSION
This study reports on the antimicrobial resistance rates and
the trend in resistance of S. aureus isolates collected from bovine with clinical or sub-clinical mastitis in Italy between
2005 and 2011. Antimicrobial agents are frequently used in
cattle for the therapy of many disease conditions, included
mastitis that represents the most common reason for antimicrobial treatment of dairy cows4. As a result, the extensive
use of antimicrobials in cattle and the consequent selective
pressure have intensified the risk of the emergence of resistant bacteria. In the present study, the antimicrobial agents
most commonly used for the treatment of S. aureus-caused
bovine mastitis were taken into account, including those
suggested as first (β-lactams) and alternative choice (macrolides, lincosamides) according with the guidelines of prudent
use of antimicrobials4.
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Table 1 - Antimicrobial resistance rates of 1,200 S. aureus strains isolated from bovine mastitis.
% of resistant isolates a
(no. of tested isolates)
Antimicrobials
Statistical analysis
2005
2006
2007
2008
2009
2010
2011
total
Pb
Rc
amoxicillin/clav. ac.
5.3
(170)
9.9
(232)
8.8
(194)
10.8
(194)
11.6
(121)
8.7
(46)
12.3
(81)
9.4
(1,038)
0.08
0.6
nafcillin
1.2
(170)
1.7
(234)
7.8
(206)
5.6
(197)
12.1
(140)
13.3
(128)
16.4
(122)
7.3
(1,197)
<0.0001
0.96
oxacillin
2.9
(170)
5.1
(235)
10.2
(206)
17.3
(197)
27.1
(140)
18.8
(128)
18.9
(122)
13.1
(1,198)
<0.0001
0.83
penicillin G
61.8
(170)
72.6
(234)
71.4
(206)
56.3
(197)
61.4
(140)
59.4
(128)
63.1
(122)
64.5
(1,197)
0.052
-0.41
cephalotin
2.4
(170)
1.7
(233)
9.3
(204)
8.2
(196)
10.7
(140)
14.1
(128)
16.4
(122)
8.0
(1,193)
<0.0001
0.96
cefoperazone
28.2
(170)
50.2
(235)
50.0
(206)
40.6
(197)
37.7
(138)
28.1
(128)
36.1
(122)
40.2
(1,196)
0.08
-0.28
cefquinome
1.2
(170)
0.9
(235)
5.3
(206)
7.2
(194)
8.6
(139)
2.3
(128)
12.3
(122)
4.9
(1,194)
<0.0001
0.71
15.3
(170)
21.3
(235)
16.7
(204)
27.4
(197)
37.1
(140)
30.5
(128)
37.5
(120)
25.1
(1,194)
<0.0001
0.89
5.9
(170)
9.0
(234)
8.7
(206)
16.2
(197)
35.7
(140)
26.6
(124)
36.9
(122)
17.5
(1,193)
<0.0001
0.91
50.6
(170)
40.5
(232)
39.2
(204)
39.1
(197)
45.0
(140)
47.7
(128)
41.7
(120)
42.9
(1,191)
0.76
-0.11
90.5
(169)
84.3
(235)
77.5
(204)
82.7
(197)
95.7
(140)
89.8
(128)
92.6
(122)
86.5
(1,195)
0.018
0.43
3.5
(170)
2.6
(234)
2.9
(206)
5.6
(195)
1.4
(139)
4.7
(128)
3.3
(122)
3.4
(1,194)
0.7
0.12
Penicillins
Cephalosporins
Tetracyclines
tetracycline
Fluoroquinolones
enrofloxacin
Macrolides
erythromycin
Lincosamides
lincomycin
Potentiated sulfa
drugs
trimethoprim/
sulfamethoxazole
a
b
c
Intermediate isolates were grouped with the resistant ones.
χ2 for the trend (a trend was considered statistically significant for P<0.05).
Regression coefficient.
At present, β-lactams are among the most widely used antimicrobial classes for treatment and prevention of bovine
mastitis14. Although the efficacy of systemic administration
of penicillins has been shown in several clinical trials15,16, the
massive use of these antimicrobials has been proposed to
exert a selection pressure favoring the emergence and the
spread of penicillin-resistant S. aureus strains. As a consequence, high rates of mastitis-causing S. aureus that are resistant to penicillin G have been repeatedly reported
worldwide17,18 and changes in prevalence of resistance with
time have been identified. After a rapid trend of increase, the
percentage of resistant strains has not changed over time or
slightly decreased17. Accordingly, more than 60% of S. aureus isolates included in our study were penicillin G-resistant, although no statistically significant changes over time
were observed. On the contrary, the combination of amoxicillin with clavulanic acid, a β-lactamase inhibitor, revealed
a high in vitro activity over time, with less than 10% of ove-
rall resistant isolates. Although information on the susceptibility of S. aureus from bovine milk to amoxicillin/clavulanic acid is rare in the literature, our results are similar to those already reported5. Low level of resistance was
observed also for nafcillin and oxacillin, two β-lactamaseresistant penicillins frequently used to treat infections caused by penicillin G-resistant staphylococci. Considering that
oxacillin disk diffusion represents a marker of methicillinresistance in staphylococci12, the significant increase of oxacillin-resistant isolates observed in the considered sevenyear period, which reached 19% in 2011, suggests that MRSA could be an emerging problem in dairy herds5,19. Detection of MRSA is of key importance as methicillin-resistance
is associated with resistance towards all the β-lactams, often
in addition to a large number of non-β-lactam antimicrobials, therefore making infections extremely difficult to
treat20. However, it must be emphasized that the present
study is limited in terms of its methodology for the detec-
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Antimicrobial resistance of Staphylococcus aureus isolated from bovine milk in Italy from 2005 to 2011
Table 2 - Antimicrobial resistance patterns of 703 S. aureus strains isolated from bovine milk.
No. of
antimicrobial
agents
Antimicrobial resistance patterns
(number of isolates)
Resistant
isolates
n
%
0
No resistance
46
6.5
1
L (103); P (44); E (3); Z (2); C (1); F (1)
153
21.8
2
LP (94); EL (60); PZ (13); LT (6); FL (4); EP (2); CL (1); CP (1); ET (1); FP (1); IP (1); LZ (1)
185
26.3
3
LPZ (96); ELT (23); ELP (21); EFL (11); LPT (6); PTZ (3); ELZ (2); CLP (1); EPZ (1); FLP (1); FLT (1); FPT (1); ILP (1); LQZ (1)
169
24
4
ELPZ (48); LPTZ (9); ELPT (7); EFLT (6); FLPZ (3); ELTZ (2); CELT (1); CLPZ (1); EFLP (1); EFTZ (1); EPTZ (1); FLPT (1)
81
11.5
5
ELPTZ (21); EFLPZ (6); EFLPT (4); CELPZ (2); EILPZ (2); CEFLT (1); EFLQT (1); EFLTZ (1); ILNPZ (1)
39
5.5
6
EFLPTZ (5); CELPTZ (2); CEFLPZ (1); EFILPZ (1); EILPTZ (1); EFLPQZ (1); ELOPTZ (1)
12
1.7
7
CEFLPTZ (4); EFILPTZ (2)
6
0.8
9
ACEFLNOPZ (1); AILNOPQTZ (1)
2
0.3
10
AEILNOPQTZ (4)
4
0.6
11
AEFILNOPQTZ (3)
3
0.4
12
ACEFILNOPQTZ (3)
3
0.4
A: amoxicillin/clavulanic acid; I: cephalotin; Z: cefoperazone; Q: cefquinome; C: cotrimoxazole; F: enrofloxacin; E: erythromycin; L: lincomycin; P: penicillin G;
O: oxacillin; N: nafcillin; T: tetracycline.
Table 3 - Multi-resistance of 703 S. aureus strains isolated from bovine milk.
No. of
antimicrobial
agents
Antimicrobial resistance patterns
(number of isolates)
Resistant
isolates
n
%
No multi-resistance
487
69.3
3
LA-LI-MA (73); LI-MA-TE (23); LA-LI-TE (16); FQ-LI-MA (11); FQ-LA-LI (4); LA-LI-PS (2); FQ-LA-TE (1); FQ-LI-TE (1);
LA-MA-TE (1)
132
18.8
4
LA-LI-MA-TE (36); FQ-LA-LI-MA (9); FQ-LI-MA-TE (6); LA-LI-MA-PS (2); FQ-LA-LI-TE (1); FQ-LA-MA-TE (1);
LI-MA-PS-TE (1)
56
7.9
5
FQ-LA-LI-MA-TE (16); FQ-LA-LI-MA-PS (2); LA-LI-MA-PS-TE (2); FQ-LI-MA-PS-TE (1)
21
2.9
6
FQ-LA-LI-MA-PS-TE (7)
7
0.9
0-2
LA: β-lactams; FQ: fluoroquinolones; LI: lincosamides; TE: tetracyclines; MA: macrolides; PS: potentiated sulfonamides.
tion of MRSA. The use of genotypic methods to detect the
presence of mecA gene is considered to be the gold standard
while performing a single phenotypic test could lead to false-negative or false-positive results21.
First-generation cephalosporins usually demonstrate good
to excellent activity against Gram-positive bacteria22. Similar
to previous research19, low resistance rates to cephalotin were observed in our study. Not surprisingly, high level of resistance was observed towards cefoperazone, confirming the
moderate activity of third generation cephalosporins against
Gram-positive bacteria22. Cefquinome, a fourth generation
cephalosporin approved only for veterinary use23, resulted
the most active β-lactam among those tested in the present
study, although a significant increasing trend of resistance
was observed in the seven-year period. Our results are in
agreement with those of previous reports that already suggested that cefquinome might be of value in the treatment of S.
aureus mastitis24. Nevertheless, according to the EU position
on the prudent use of antimicrobials, fourth generation
cephalosporins are recognized as critically important antimicrobials in human medicine and their veterinary use
should be reserved for the treatment of clinical conditions
which have responded poorly, or are expected to respond
poorly, to other classes of antimicrobials25.
Macrolides and lincosamides are considered as second-line
antimicrobial agents in bovine mastitis treatment and crossresistance between the two antimicrobial classes has been reported due to a similar mechanism of action against the 50S
subunit of the bacterial ribosome26. The resistance rates observed in our study for erythromycin and lincomycin were
considerably higher than those reported in other countries18,
with 35% of the “core number” of isolates showing cross-resistance between lincosamides and macrolides. Considering
that 57% of the macrolides/lincosamides-resistant isolates
resulted also resistant to penicillin G, this finding may represent a potential risk of therapy failure of bovine mastitis caused by penicillin-resistant S. aureus 4.
Tetracyclines have been used extensively to treat animal infections because of their relative safety and broad-spectrum
activity27. Nevertheless, increasing resistance rates in S. aureus strains from bovine mastitis have been reported6. Accordingly, a relatively high level of resistance and a significant
increasing trend of resistance in the considered seven-year
period were found for tetracycline in our study. The low le-
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vel of tetracycline in vitro activity against S. aureus, together
with its low bioavailability due to the irreversible binding
with milk components, make the use of this antimicrobial of
limited effectiveness in the control of bovine mastitis27.
Although not specifically recommended for bovine mastitis
treatment4, potentiated sulphonamides are among the most
used antimicrobials in bovine husbandry. In accordance with
previous studies, which already reported low resistance rates
to trimethoprim-sulphametoxazole for S. aureus 7, a relatively stable high degree of the in vitro activity of this antimicrobial combination was found in the present study.
High in vitro activity of enrofloxacin, a second generation
fluoroquinolone, has been reported for S. aureus 18, nevertheless enrofloxacin-resistant isolates have been observed5 maybe due to the frequent extra-label use of this drug for bovine
mastitis treatment. Accordingly, in the present study resistance to enrofloxacin resulted particularly high in 2011 and
a significant increasing trend was observed throughout the
study period. However, as already stated for fourth generation cephalosporins, fluoroquinolones should be limited for
use in cattle do to their importance in the treatment of severe and invasive infections in humans and, whenever possible,
the use of this antimicrobial class should be based on in vitro susceptibility test results28.
CONCLUSIONS
High resistance rates and a significant increasing trend in resistance between 2005-2011 towards antimicrobial agents commonly used for the treatment of mastitis caused by S. aureus
were observed in the present study, as well as a relatively high
rate of multi-resistant isolates. Although a successful control
program should consider overall management practices, the
use of antimicrobials continues to be a prerequisite for treatment of bovine mastitis. For this reason, periodic surveillance
for antimicrobial resistance of S. aureus isolated from dairy
cows with mastitis is strongly recommended as an important
component of prudent antimicrobial use practices.
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