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Persistence of gentamicin residues in cow milk after intramammary

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62
Persistence of gentamicin residues in cow milk after
intramammary treatment
T. MARTINS1, A.F.S. SANTOS1, M.S. MIRANDA1, T.P. MOTTA1, L.A. AMBRÓSIO1, C.R. POZZI1, J.R. ARCARO1*
Centro Apta Bovinos de Leite, Instituto de Zootecnia, Apta-SAA, Rua Heitor Penteado, 56, Nova Odessa, São Paulo, Brasil, CEP 13460-000.
1
Corresponding author: juarcaro@iz.sp.gov.br
SUMMARY
The indiscriminate use of the drugs for the treatment of mammary gland
infections can leave residues in cow milk destined for consumption. The
objective of this study was to evaluate the persistence of antibiotic residues
in milk of lactating cows with and without mastitis after intramammary
treatment with gentamicin. Twenty Black and White Holstein cows, 10 with
mammary quarter inflammation and 10 without inflammation diagnosed
by the California Mastitis Test, were selected. Gentamicin sulfate was
administered by intramammary infusion into each quarter once daily.
The treatment was performed after afternoon milking and repeated for
3 days. After application of the last antibiotic dose, milk samples were
collected from the mammary quarters and collecting balloons over a
period of 6 days for the detection of antibiotic residues by the Delvotest®
SP. The microorganisms most frequently isolated from milk samples of
cows without and with inflammation were Corynebacterium spp.(48.27%
and 38.46%, respectively), Streptococcus spp.(13.79% and 46.15%), and
coagulase-negative Staphylococcus (24.14% and15.38%).The Staphylococcus
aureus isolates were resistant to neomycin and coagulase-negative
staphylococci were resistant to oxacillin and penicillin G. Antibiotic residues
were detected after the withdrawal period established by the manufacturer
of the drug in 44.4% and 55.5% of samples collected from cows without
and with inflammation, respectively, and in 20.0% and 40.0% of collecting
balloons. Milk producers in Brazil should be advised to perform tests for the
detection of antibiotic residues before releasing milk for consumption and
the veterinary pharmaceutical industry should reevaluate the withdrawal
period of intramammary administered antibiotics.
Keywords: Milk, Mastitis, Milk quality, Delvotest®SP,
residues
Introduction
Mastitis is an inflammatory process of the mammary
gland that has a marked economic impact on milk production
by dairy cows, causing losses to milk producers and the
dairy industry. The costs of this disease vary according to
its severity, with the indiscriminate use of drugs and the
disposal of milk containing antibiotic residues being the
main causes of economic losses [33, 12, 6]. Mastitis usually
occurs in response to a bacterial infection, but can also be
caused by other microorganisms or by physical and chemical
trauma [38].
The indiscriminate use of antimicrobial agents for
the treatment of mastitis can lead to residues of these
drugs in milk and to the selection of bacterial strains
that are resistant to antibiotic therapy [32, 37]. The main
causes of the persistence of antibiotic residues in milk
are the administration of not recommended drugs whose
MARTINS (T.) AND COLLABORATORS
RÉSUMÉ
Persistance de résidus de gentamicine e dans le lait de vache après
traitement intramammaire
L’utilisation des antibiotiques dans le traitement des mammites peut
entraîner la présence de résidus dans le lait de vache destiné à la
consommation. L›objectif de cette étude était d›évaluer la persistance de
residus de gentamicine dans le lait des vaches atteintes ou non de mammite
suite à une traitement avec de la gentamicine par voie intramammaire.
Vingt vaches de race Holstein, dont 10 présentant une inflammation au
niveau d’un quartier mammaire et 10 saines ont été sélectionnées à l’aide du
Californian Mastistis Test (CMT). Le sulfate de gentamicine a été administré
par perfusion intramammaire dans chaque quartier une fois par jour. Le
traitement a été effectué après la traite après-midi et répété pendant 3 jours.
Après application de la dernière dose d’antibiotiques, des échantillons de lait
ont été prélevés dans les quartiers mammaires et des ballons de collecte sur
une période de 6 jours pour la détection des résidus d’antibiotiques par le
Delvotest ® SP. Les bactéries les plus fréquemment isolées des échantillons de
lait de vache ne présentant pas d’inflammation ont été: Corynebacterium sp.
(48.27% et 38.46% respectivement), Streptococcus spp. (13,79% et 46,15%),
et Staphylococus coagulase négative (24.14% et 15.38%). Les isolats de
Staphylococus aureus ont présenté un phénotype résistant à la néomycine
et ceux de Staphylococus coagulase négatives ont présenté une résistance à
l›oxacilline. La présence d’antibiotiques a été détectée après le délai d’attente
du fabricant dans 44.4% et 55.5% des échantillons prélevés chez les vaches
avec sans et sans mammites, respectivement, et dans 20% et 40% des tanks à
lait. Des tests pour la détection des résidus d’antibiotiques dans le lait destiné
à la consommation devraient être conseillés aux producteurs de lait du Brésil
et l’industrie pharmaceutique vétérinaire devrait réévaluer le délai d’attente
des antibiotiques administrés par voie intramammaire.
Mots-clés: vache, mammite, gentamicine, résidus
pharmacokinetics is not completely established, excess dose
administration, lack of compliance with the milk discard
period in the case of treated animals, identification errors of
treated animals, and confusion of milk after milking treated
animals [18, 17]. The withdrawal period of antimicrobial
agents is reported on the information leaflet and should be
followed to prevent the contamination of milk. However, the
occurrence of antimicrobial residues in commercialized milk
and milk derivatives has been reported [2, 1]. Intramammary
treatment of dry cows and pre-calving heifers has been
identified as another important factor for the occurrence of
antibiotic residues in milk [23, 24].
Milk containing antimicrobial residues is inappropriate
for consumption and presents a public health risk [31].
Antibiotic residues in milk can cause allergic reactions in
susceptible individuals and problems to the processing
industry, interfering mainly with the fermentation of milk
derivatives [32]. In contrast to other countries [34], no
Revue Méd. Vét., 2014, 165, 3-4, 62-67
PERSISTENCE GENTAMICIN IN MILK
restrictions exist in Brazil regarding the use of gentamicin
for the treatment of mastitis. Therefore, the objective of the
present study was to evaluate the persistence of antibiotic
residues in milk of lactating cows after intramammary
treatment with gentamicin sulfate.
Material and methods
CHARACTERIZATION AND SELECTION OF THE ANIMALS
Milk samples were collected from mammary quarters
of 20 Black and White Holstein cows for the diagnosis of
subclinical mastitis by the California Mastitis Test (CMT)
[7]. The CMT reaction was classified as negative (-), weak
(+), moderate (++), or strong (+++). Ten of the animals
submitted to the test exhibited strong reactions and were
selected as animals with subclinical mastitis. Animals
presenting negative reactions in all mammary quarters were
classified as having no inflammation.
TREATMENT AND COLLECTION OF MILK SAMPLES
The animals had not been treated with any antibiotic at
least 30 days prior gentamicin administration. Before the
treatment, each infected quarter was thoroughly milked out
by hand and the teat end was cleaned using a cotton swab
soaked with 70% alcohol.
The treatment consisted of intramammary infusion
syringe with 10ml commercial product (150 mg gentamicin
sulfate, 50 mg bromhexine hydrochloride, and 10 ml excipient,
Mastifin®, OurofinoAgronegócioLtda, Brasil).The infusion
was performed once daily after the afternoon milking and
repeated for 3 days. The withdrawal period reported on the
information leaflet is 96 hoursafter application of the last
dosein agreement with the withdrawal time of gentamicin
that is commercialized in Brazil and France.
The milk samples were collected from the mammary
quarters before treatment for determination of the
microbiological profile, antimicrobial susceptibility profile,
and detection of antimicrobial residues. For this purpose,
the mammary quarters were washed and dried with paper
towel and antisepsis was performed with 70% alcohol.
Twenty-four hours after application of the last drug dose,
milk samples were collected daily during afternoon milking
Negative
n %
Culture-Positive Quarter 26 48,15
Culture-Negative-Quarter 28 51,85
Total 54 100
CMT California Mastitis Test
n=number
Table I: Score CMT and percentage of culture positive or negative mammary quarter
Revue Méd. Vét., 2014, 165, 3-4, 62-67
63
for 6 consecutive days. In addition, milk samples were
collected from the collecting balloons for the determination
of antimicrobial residues.
ANALYSIS OF MILK SAMPLES
The milk samples were seeded onto 5% defibrinated
sheep blood agar and incubated at 37ºC.The bacterial
isolates were identified as described by Murray et al. [21]
The antimicrobial susceptibility profile of coagulase-negative
staphylococci (CoNS)and Staphylococcus aureus isolates
was determined by the Mueller-Hinton agar diffusion test
using disks impregnated with the following antibiotics:
oxacillin (1µg), gentamicin (10µg), kanamycin (30µg),
cefaclor (30 µg), neomycin (10µg), and penicillin G (10µg).
Antibiotic susceptibility was evaluated according to the
recommendations of the National Committee for Clinical
Laboratory Standards (NCCLS) [22].
The presence of antibiotic residues in milk was evaluated
using the Delvotest®SP microbiological test system (DSM
Foods Specialties,) according to manufacturer instructions.
Before the test, the milk samples were treated for the
inactivation of possible nonspecific inhibitors present in
milk and prevention of false-positive results according to
KosikowskiandO’Leary [15].The occurrence of antibiotic
residues in milk was evaluated in the selected animals before
and after treatment with gentamicin. Antibiotic-free raw
milk (obtained from an animal that had not been treated for
a long period of time) served as negative control. The positive
control consisted of negative milk samples enriched with a
solution of gentamicin sulfate Sigma® (St. Louis, MO, USA)
at concentrations of 10, 50, 100, 200, 300 and 500 µg/L.
STATISTICAL ANALYSIS
The chi-square test was used to determine differences
between groups, adopting a confidence level of 95%. Statistical
analysis was performed using the Minitab software, version
15.1.3. [19].
Results
Table I shows the CMT scores and results of the
microbiological tests obtained for 80 mammary quarter
milk samples collected from lactating cows selected for
CMT
1 (+) 2 (++) 3 (+++)
n % n % n %
2 40,00 1 33,34 16 88,89
3 60,00 2 66,66 2 11,11
5 100 3 100 18 100
64
intramammary administration of gentamicin. Among the 54
samples with a negative CMT result, microbiological growth
was detected in 26 (48.15%) and cultures were negative in
28 (51.85%). Among the 26 mammary quarter milk samples
with a positive CMT, cultures were negative in seven (26.92%)
and positive in 19 (73.08%).
Table II shows the relative and absolute frequencies of
microorganisms isolated from milk samples of cows with
mastitis (strong CMT) and without mastitis(negative CMT).
Streptococcus (38.89%), Corynebacterium spp. (38.89%), and
CoNS (14.82%) were the most frequent bacteria isolated
from animals with subclinical mastitis. The most frequent
pathogens isolated from cows without inflammation were
Corynebacterium spp. (50.0%), CoNS (28.57%), and Gram-
negative bacilli (14.29%). The frequency of isolation of
Staphylococcus aureus was low in the present study. The CoNS
strains isolated from cows with and without inflammation
were resistant to oxacillin and penicillin G and Staphylococcus
aureus was resistant to neomycin (Table III).
Persistence of antimicrobial residues was observed 2
days after the withdrawal period recommended by the
manufacturer of the drug (4 days) in 55.5% and 44.4% of
mammary quarter milk samples from treated cows without
and with inflammation, respectively (Table IV). In addition,
antimicrobial residues were detected in 40% and 20% of milk
samples collected from the collecting balloons of treated
cows without and with inflammation, respectively (Figure
1).No significant differences in the presence of antimicrobial
residues after the withdrawal period were observed between
animals with a strong CMT and a negative CMT reaction
(P>0.05).
Figure 1: Percentage of gentamicin detected in milk from ballons collec-
tors after treatment
Discussion
With respect to the various infectious agents responsible
for the development of mastitis, Leslie et al. [16] suggested
the existence of minor and major pathogens depending on
the cellular immune response to the pathogen triggered by
the mammary gland. Minor pathogens cause low somatic cell
counts and include Corynebacterium spp. and some CoNS.
MARTINS (T.) AND COLLABORATORS
Major pathogens are responsible for high somatic cell counts
and include Staphylococcus aureus, coliform bacteria, and
Streptococcus spp.
Staphylococci and streptococci are the microorganisms
most frequently isolated from animals with subclinical
mastitis. Species of the genus Staphylococcus are the main
etiological agents of contagious mastitis due to their ability
to penetrate and establish deep infection in mammary
gland tissues [3]. In the present study, Staphylococcus
aureus was isolated from only 3.84% of milk samples
of cows with inflammation. The most prevalent species
were Corynebacterium spp., Streptococcus spp. and CoNS.
The role of Corynebacterium bovis as a causative agent of
mastitis is controversial. Some investigators consider this
microorganism to be of minor importance. However, studies
have drawn attention to the high percentage of isolation of
C. bovis from mammary quarters with mastitis, with this
microorganism often being the most prevalent agent in dairy
herds [13, 35]. The high frequency of isolation of bacterial
species of this genus from milk samples is often related to
failure of teat disinfection and milking hygiene [5, 28].
In the present study, the highest frequency of isolation of
Corynebacterium spp. was observed for mammary quarters
with negative CMT reactions.
The percentage of isolation of secondary mastitis
pathogens such as Corynebacterium spp. and CoNS was
higher for mammary quarters with negative CMT reactions,
a finding highlighting the importance of isolation of the
causative agents of mastitis for the diagnosis of the disease
[5]. The group of CoNS plays an important role in contagious
mastitis and different species have been isolated from infected
mammary quarter milk samples [27].
Aminoglycoside antibiotics are widely used in Brazil
for the treatment of mastitis and no restrictions exist
regarding their veterinary use. The Program for the
Control of Biological Residues elaborated by the Ministry
of Agricultures, the organ responsible for the control of
milk quality in Brazil, does not provide recommendations
regarding the upper limits for gentamicin in milk [4]. Despite
the demonstration of the efficacy of aminoglycosides such
as gentamicin in the treatment of mastitis [29], evaluation
of the withdrawal period of these drugs is necessary since
determinant factors are often not taken into account in
preliminary pharmacokinetic tests. In the present study,
antibiotic residues were detected in mammary quarters and
collecting balloons of animals for an additional 2 days after
the withdrawal period recommended by the manufacturer.
Raiaand Costa [30] observed the persistence of gentamicin
residues in milk beyond the withdrawal period in animals
with clinical mastitis after intramammary treatment. In the
study of Pedersoli et al.[25] evaluating the persistence of
gentamicin after systemic and intramammary administration,
this antibiotic was detectable for a period of up to 228 hours.
The persistence of aminoglycoside residues seems to vary
depending on factors such as the formulation used, dose
Revue Méd. Vét., 2014, 165, 3-4, 62-67
PERSISTENCE GENTAMICIN IN MILK 65

CMT +++ CMT negative

Pathogens
n % n %
Corynebacterium spp. 10 38.46 14 48,27
Streptococcus spp. 12 46.15 4 13,79
Coagulase-negative Staphylococci 4 15.38 7 24,14
Staphylococcus aureus 1 3.84 2 6,90
Bacilo gram negative 0 0,00 2 6,90
Total 26 100 29 100

Table II: Number and percentage of pathogens isolates from mammary quarters with and without mastitis

Microorganism (%)
Coagulase-negativeStaphylococci Staphylococcus aureus
(n=11) (n=3)
Antimicrobial Sensitive Intermediate Resistent Sensitive Intermediate Resistent
Gentamicin (10µg) 100 0 0 100 0 0
Kanamycin (30µg) 90,91 9,09 0 100 0 0
Oxacillin (1µg) 81,82 0 18,18 100 0 0
Penicillin (10UI) 63,64 0 36,36 100 0 0
Cefaclor (30µg) 100 0 0 100 0 0
Neomicin (10µg) 100 0 0 33,33 0 66,67

Table III: Antimicrobial resistance profile of Staphylococci isolates from cow with and without mastitis

Mammary quarters
Days after treatment
1º 2º 3º 4º 5º 6°
N % N % N % N % N % N %
CMT -. 18 100,0 18 100,0 18 100,0 17 94,4 11 61,1 8 44,4

CMT+++ 18 100,0 18 100,0 17 94,4 16 88,8 11 61,1 10 55,5

N= Number of mammaryquarters
Qui-square test. P > 0,05

Table IV: Antibiotic residues in milk after treatment with gentamicin intramammary and score CMT

administered, dose interval, health status of the animal, and
physiological factors [9, 34].
The CoNS strains isolated from treated mammary quarters
were resistant to oxacillin and penicillin G and Staphylococcus
aureus was resistant to neomycin. The indiscriminate use of
antibiotics for different therapeutic purposes in veterinary
medicine, especially for the treatment of mastitis, has led
to the selection of resistant strains [20, 10]. Among the
different mastitis-causing species, Staphylococcus aureus
is the most important and most common microorganism
in dairy herds worldwide. This microorganism is difficult
to control because of the production of beta-lactamases,
enzymes that cleave beta-lactam antibiotics and thus confer
resistance to these antibiotics [14, 11, 26]. The animals
selected in the present study come from a farm which has a
history of the indiscriminate use of beta-lactam antibiotics
and the recent use of gentamicin. The high level of resistance
of Staphylococcus aureus and CoNS to beta-lactam and
aminoglycoside antibiotics reported in studies conducted
in different countries clearly shows that the prolonged
use of antimicrobial agents, in the absence of isolation
and identification of the microorganisms involved and
concomitant susceptibility testing, will lead to the selection
of resistant strains [28, 8, 36].
In conclusion, antibiotic residues were detected in
milk beyond the withdrawal period recommended by the

Revue Méd. Vét., 2014, 165, 3-4, 62-67

66
manufacturer of the drug; a finding posing a health risk to
consumers. Milk producers should perform rapid tests before
the release of milk for consumption to prevent its contamination
with gentamicin sulfate residue. Veterinary pharmaceutical
industry should reevaluate the withdrawal period of
intramammary administered antibiotics as gentamicin.
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