Antimicrobial resistance and bovine mastitis
319
Prevalence of antimicrobial resistance among bacterial pathogens isolated from bovine mastitis in northern Jordan M. O ALEKISH1*, K. M AL-QUDAH1, A. AL-SALEH2 1 2
*
Department of Veterinary Clinical Sciences, Jordan University of Science and Technology, P.O. Box 3030, 22330 Irbid, Jordan DVM, Msc. Jordan Food and Drug Administration. P.O. Box 811951-Amman- 11181, Jordan. Author corresponding:
[email protected],
[email protected]
SUMMARY
RESUME
Over the past decade a number of studies have been published on the prevalence of antibiotic resistance among bovine mastitis pathogens. So far, no similar studies have been performed in Jordan or neighboring countries. A pilot study, on emergence of antibiotics resistance among bovine mastitis pathogens, was carried out in the Veterinary Health Center (VHC) in Jordan University of Science and Technology. Records reviews were carried out on 205 mastitis cases between the years of 2002-2006. Culture and sensitivity tests were done. The most prevalent pathogens isolated were Staphylococcus aureus (S. aureus) (53.4%), E.coli (16 %), Streptococcus non-agalactiea (Strep non-ag) (5.9%), and coagulase negative Staphylococci (CNS)(5.9%). The antibiotics for which, most of the isolated pathogens were sensitive to were enrofloxacin (61.2%) and ciprofloxacin (58.7%). While the ones that the pathogens were mostly resistant against were sulfa/trimethoprim (87.4%), and penicillin (84.5%). Apparently, you can notice the risk of an emergence of an antimicrobial resistance among mastitis bacterial pathogens in Jordan.
Prévalence de la résistance aux antimicrobiens chez les bactéries pathogènes isolés de la mammite bovine au nord de la Jordanie
Keywords: Mastitis, Prevalence, Antibiotics, Resistance, Jordan
Au cours de la dernière décennie, un certain nombre d’études ont été publiées sur la prévalence de la résistance aux antibiotiques chez les pathogènes de la mammite bovine. Jusqu’à présent, aucune étude similaire n’a été réalisée en Jordanie ou les pays voisins. Une étude pilote sur l’émergence de la résistance aux antibiotiques chez les pathogènes de la mammite bovine, a été réalisée dans le Centre de santé vétérinaire (VHC) en Jordanie University of Science and Technology. En revue les dossiers ont été effectuées sur 205 cas de mammite entre les années 2002-2006. La culture et des tests de sensibilité ont été effectuées. Les agents pathogènes les plus fréquentes ont été isolés Staphylococcus aureus (53,4%), E. coli (16%), Streptococcus non-agalactiea (5,9%) et les staphylocoques à coagulase négative (5,9%). Les antibiotiques les plus sensibles pour la plupart des agents pathogènes isolés ont été enrofloxacine (61,2%) et la ciprofloxacine (58,7%). Les antibiotiques les plus résistants pour la plupart des agents pathogènes isolés ont été sulfamides / triméthoprime (87,4%), et de la pénicilline (84,5%). Évidemment, il ya une émergence d’une résistance antimicrobienne chez les bactéries pathogènes mammite en Jordanie.
Mots-clés: Mammite, Prévalence, Résistance, de la Jordanie
Introduction Bovine mastitis is the single most costly disease of dairy cattle and a major monetary drain on the dairy industry [3]. Mastitis is inflammation of the mammary gland that is nearly always caused by microorganisms, usually bacteria that invade the udder, multiply and produce inflammatory toxins. Even in the best managed herds, it occasionally becomes necessary to treat a dairy cow for mastitis. Successful treatment depends on a specific and accurate diagnosis, followed by treatment with an appropriate antibacterial product. Accordingly, therapy treating mastitis is the most common cause for antibacterial use in lactating dairy cattle [20, 29, and 48]. Due to this aggressive use of antibacterial, the resistance against this type of treatment has been evolving in the last few years [45]. Therefore, currently; the judicious use of these drugs is of great global concern [8]. Antibiotics are fundamental for the control of infectious diseases in man and animals. In recent years, however, there has been considerable concern about the emergence and diffusion of antibiotic resistance resulting from haphazard Revue Méd. Vét., 2013, 164, 6, 319-326
Antibiotiques,
antibiotic use in the veterinary sector, with possible risks for the human population [5, 25]. Since their discovery during the 20th century, antimicrobial agents have substantially reduced the threat posed by mastitis pathogens. The use of these drugs combined with improvements in sanitation, housing, and nutrition, and the advent of widespread vaccination programs for major environmental pathogens, has led to a dramatic drop in incidence of mastitis that was previously widespread, untreatable, and frequently fatal. These gains are now seriously jeopardized by another recent development: the emergence and spread of microbes that are resistant to cheap and effective first-choice, or “first-line” drugs. The consequences are severe. Infections caused by resistant microbes fail to respond to treatment, resulting in prolonged illness and greater risk of cull or death. Treatment failures also lead to longer periods of infectivity, which increase the numbers of infected cows moving in the farm and thus ex pose the whole herd to the risk of contracting a resistant strain of infection.
320 When infections become resistant to first-line antimicrobials, treatment has to be switched to secondor third-line drugs, which are nearly always much more expensive and sometimes more toxic as well, e.g. enrofloxacin (which does not even exist as an intramammary infusion) is over 3 times more expensive than penicillin the first-line drugs used to treat non-resistant forms. Literature is affluent with articles describing antibacterial resistance patterns among bovine mastitis pathogens either isolated from clinical studies or submitted to diagnostic laboratories [4, 7, 8, 10,12, , 27, 31, 32, 39, 40, 41, 47]. Despite the presence of this numerous number of studies, convincing evidence is lacking to support a widespread, emerging resistance among mastitis pathogens to antibacterial drugs [11, 18, 27, 30]. Ultimately, definite conclusions on resistance patterns of mastitis pathogens are difficult given the limitations of the data presented in the literature. There is no formal system for monitoring or surveillance of antibiotic resistance in animal bacterial isolates in Jordan. In the last few decades, only one study had been commenced to estimate the prevalence of bovine mastitis in Jordan [21]. However, few mastitis investigations were conducted on small ruminant [22, 1]. No studies were conducted to investigate the pattern of mastitis pathogens in resistance to antimicrobial drugs. The lack of historical data is compounded by the fact that little, if any was published in readily available form. The aim of this study was to provide epidemiological data, which may serve as a basis for the formulation of recommendations for prudent use of antimicrobials for treatment of bovine mastitis in Jordan. To our knowledge, the present study is the first retrospective study that investigates the susceptibility patterns for mastitis pathogens isolated from dairy cattle in northern Jordan.
Materials and methods Study area and study population
O ALEKISH (M.) AND COLLABORATORS Study design, sampling microbiological methods
procedures
and
A retrospective type of study was carried out to investigate the prevalence of mastitis, identify the major bacterial pathogens and test the antimicrobial resistance of milk bacterial isolates among dairy cows in northern Jordan. A review of VHC records for all of presented mastitis cases during the period of 2002-2006 was completed. A total of 205 cows with mastitis were included in the study. All of the cases had been sampled one time. The mastitis cases presented to VHC were thoroughly examined by vet students and then by their clinicians. If decided, milk samples were collected following standard milk sampling techniques [43, 33] mainly by vet students if not the clinicians themselves, except for few cases were brought by the farmers. Samples were sent to the VHC diagnostic laboratory for culture and sensitivity testing. Samples were cultured on blood and MacConkey agar then incubated aerobically at 37°C for up to 48 hrs. Bacteria on culture-positive plates were specified mainly according to their gram-stain reaction, hemolytic feature, and colony morphology. Other biochemical tests had been done when needed. Mycoplasma spp. could not be detected due to the lack of the facilities for the cultivation of this pathogen in our laboratory. Mueller-Hinton agar was used as a culture medium to test the in-vitro antibiotic sensitivity of the isolates employing the Kirby-Bauer disk diffusion method [6]. The following antimicrobial drugs were used: ampicillin (AMP, 10µg), penicillin G (PEN) (10 IU), streptomycin (STR) (10 µg), gentamycin (GEN) (10 µg), erythromycin (ERY) (15 µg), ciprofloxacin (CIP) (5 µg), oxytetracycline (OXTE) (30 µg), trimethoprim/sulphamethoxazole (Trim/SULPHA) (25 µg), enrofloxacin (ENR) (5 µg), doxycyclin (DOX) (30 µg) and neomycin (NEO) (30 µg). The breakpoints (diameters) used to classify the bacteria as susceptible, intermediate or resistant for each antibiotic is included in Table I.
Statistical analysis The prevalence rate for every pathogen isolated was calculated as defined by the revision of the records. The antibiotics for which most of the isolated pathogens were sensitive or resistant were determined according to invitro antimicrobial susceptibility test results. PASW (SPSS program) Statistical Analysis Software was used to analyze the data.
The current cattle population in Jordan is about 69,100 [9]. The governorate of Irbid, where this study had been commenced, holds the 2nd largest number of cows (16,950) in the country. The largest population (63,220) of cattle is Frisian-Holstein with the rest (5,880) being mixed of Shami and local breeds [9].
Results
The Veterinary Health Center (VHC) (the only veterinary teaching clinic in Jordan) of Jordan University of Science and Technology (JUST) is located in Irbid. The clinic receives approximately 2,000 large and small animal patients annually that are referred from practices all over the country, especially the northern part of Jordan.
From 205 recorded mastitis cases (both clinical and subclinical), 11 different pathogens were isolated [Table II], of which S. aureus had the highest prevalence (110 cases, 53.7%), followed by E.coli (33 cases, 16%), CNS (12 cases, 5.9%), Strep non-ag (12 cases, 5.9%), Corynebacterium spp. (8 cases, 3.9%), Pseudomonas aeruoginosa (7 cases, 3.4%), Revue Méd. Vét., 2013, 164, 6, 319-326
Antimicrobial resistance and bovine mastitis
321
*Zone of Inhibition (Diameter) in mm for Sensitivity Disks Antimicrobial agent Resistant Intermediate Ampicillin 22 or less 23-30 Ciprofloxacin 15 or less 16-20 Doxycycline 12 or less 13-15 Erythromycin 13 or less 14-22 Enrofloxacin 15 or less 16-20 Gentamycin 12 or less 13-14 Neomycin 12 or less 13-16 21-28 Penicillin 20 or less 12-14 Streptomycin 11 or less 15-18 Oxytetracycline 14 or less 12-16 Trimethoprim/Sulphamethoxazole 11 or less
Sensitive 31 or more 21 or more 16 or more 23 or more 21 or more 15 or more 17 or more 29 or more 15 or more 19 or more 17 or more
*According to the data sheet attached to the sensitivity test kit, provided by Arcomex Arab Company for Medical Diagnostics. Table I: The breakpoints used to classify the bacteria as susceptible, intermediate or resistant for each antibiotic used.
Bacterial Isolated
Frequency
Prevalencerate
Staphylococcus aureus E.coli Streptococcus non agalactiea CNS Staphylococcus Corynobacterium spp. Pseudomonas aeruginosa Klebsiella pneumonia Streptococcus agalactiea Proteus spp. Bacillus spp. Actinomyces spp. Fungus Mixed culture No grounds
110 33 12 12 8 7 6 5 2 1 1 1 6 1
53.7 16 5.9 5.9 3.9 3.4 2.9 2.4 1 0.5 0.5 0.5 2.9 0.5
Table II: Frequency and prevalence rate of the isolated pathogens
ANTIBIOTICS
SENSITIVE
RESISTANCE
INTERMEDIATE
Ciprofloxacin
121 (58.7%)
38 (18.4%)
21 (15%)
Enrofloxacin
126 (61.2%)
41 (19.9%)
30 (14.6%)
Doxycycline
19 (9.2%)
107 (51.9%)
9 (4.4%)
Gentamycin
97 (47.1%)
49 (23.8%)
55 (26.7%)
Penicillin
19 (9.2%)
174 (84.5%)
7 (3.4%)
Trimethoprim/sulfamethoxazole
9 (4.4%)
180 (87.4%)
5 (2.4%)
Ampicillin
27 (13.1%)
145 (17%)
14 (6.8%)
Neomycin
44 (21.4%)
97 (47.1%)
16 (7.8%)
Erythromycin
28 (13.6%)
145 (70.4%)
9 (4.4%)
Tetracycline
12 (5.8%)
160 (77.7%)
9 (4.4%)
Streptomycin
4 (1.9%)
127 (61.7%)
67 (32.5%)
Table III: In-vitro antimicrobial susceptibility test results of all milk bacterial isolates.
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322
O ALEKISH (M.) AND COLLABORATORS
Klebsiella pneumonia (6 cases, 2.9%), and Streptococcus agalactiae (5 cases, 2.4%), with few cases of minor pathogens and fungus.
Isolates of S. aureus and E.coli showed higher susceptibility to enrofloxacin (68%, 67%), ciprofloxacin (64%, 66%), gentamycin (51%, 59%), and neomycin (28%, 41%). Meanwhile both pathogens showed higher resistance to streptomycin (96%, 95%), trimethoprim / sulphamethoxazole (90%, 100%), penicillin (87%, 94%), and tetracycline (85%, 96%). Streptococcus agalactiae isolates’ susceptibility pattern was similar to S. aureus and E.coli in terms of sensitivity and resistance rate to various antimicrobials except for its additional resistance (100%) against doxycycline. S. non ag isolates represented susceptibility to most of the antimicrobials used with few isolates showed resistance to streptomycin and trimethoprim/sulphamethoxazole. Coagulase negative Staphylococcus isolates showed 100% resistance to trimethoprim/ sulphamethoxazole, streptomycin, tetracycline, in addition to doxycycline.
All isolates were tested for antimicrobial susceptibility as illustrated in Table III. Of the entire antibiotics used in this study, the highest rate of sensitivity was to enrofloxacin (61.2%) among all of the pathogens, followed by ciprofloxacin (58.7%), gentamycin (47.1%), and neomycin (21.4%). Where as, the highest rate of resistance among the isolates was against trimethoprim/sulfamethoxazole (87.4%), penicillin (84.5%), tetracycline (77.7%), and erythromycin (70.4%), respectively. In-vitro susceptibility and resistance patterns of each bacterial isolates strains are shown in Table IV, and Table V.
Responses to application of antimicrobial disks (susceptible in %) Isolates
No.
CIPRa
ENR
S. aureus
110
64
68
15
51
9
7
16
28
22
9
4
E.coli
33
66
67
10
59
6
0
13
41
4
4
0
St.non agalactiae
12
73
75
44
42
33
18
50
50
30
2
20
CNS Staph
12
70
75
0
42
0
0
0
29
8
0
0
Corynebacterium spp.
8
13
38
0
25
13
0
13
33
13
0
0
Pseudomonas aeruginosa
7
86
43
0
29
0
0
0
20
0
0
0
DOX GEN
PEN SULPH AMP
NEO
ERY OXTE
STR
Klebsiella pneumonia
6
50
33
20
50
0
0
0
0
0
0
0
St. agalactiae
5
75
75
0
40
13
0
25
0
25
0
0
Proteus spp.
2
50
0
0
0
0
0
0
0
0
0
0
Bacillus spp.
1
0
0
0
100
0
0
0
0
0
0
0
Actinomyces spp.
1
100
100
0
0
100
0
0
0
0
0
0
a
The distribution of each antibiotic is mentioned in material and methods section.
Table IV: In vitro susceptibility of each bacterial isolates strains obtained from bovine mastitis cases in northern Jordan.
Responses to application of antimicrobial disks (Resistance in %) Isolates
No.
CIPRa
S. aureus
110
14
11
75
23
87
90
79
61
72
85
96
E.coli
33
28
30
90
19
94
100
84
44
93
96
95
St.non agalactiae
12
09
17
45
33
58
82
38
50
70
78
80
CNS Staph
12
30
25
100
17
92
100
82
71
92
100
100
Corynebacterium spp.
8
50
50
100
50
88
88
63
50
88
88
100
Pseudomonas aeruginosa
7
14
43
100
29
100
100
86
80
100
86
100
Klebsiella pneumonia
6
33
67
80
33
100
83
100
80
100
100
100
St. agalactiae
5
25
25
100
20
50
100
75
100
80
100
100
Proteus spp.
2
50
50
100
100
100
100
100
100
100
100
100
Bacillus spp.
1
100
0
100
0
100
100
0
0
100
100
100
Actinomyces spp.
1
0
100
0
100
0
100
100
100
100
100
100
a
ENR DOX
GEN
PEN SULPHA AMP NEO ERY OXTE
STR
The distribution of each antibiotic is mentioned in material and methods section.
Table V: In vitro resistance pattern of each bacterial isolates strains obtained from bovine mastitis cases in northern Jordan. Revue Méd. Vét., 2013, 164, 6, 319-326
Antimicrobial resistance and bovine mastitis Generally, the current antimicrobial sensitivity test indicated that the responses of the various milk bacterial isolates to different antimicrobial agents were almost consistent.
Discussion According to our records, milk samples submitted from the VHC to our diagnostic laboratory were generally from cows having mastitis. However, whether the submissions were from suspected subclinical or clinical mastitis cases is not reported in our reviewed records. Thus, our data can be interpreted only as a general measure of the prevalence rate of various pathogens causing mastitis but not as an aid to contrast the difference between several forms of mastitis. Nevertheless, as a tertiary referral center most of the presented cases to our VHC are chronic cases or acute on top of chronic cases that were repeatedly treated with no or poor response, and though, referred for further investigation. We focused in this study on the most commonly reported pathogens cultured in our laboratory. Our diagnostic laboratory determines the susceptibility patterns of the isolated pathogens against antibacterials that are most likely to be used in a clinical setting as a therapy for mastitis and are present in the local market.
323 farmers do not follow the label instruction about the length of using antibiotics so that recurrence is always an issue. As mentioned before in this paper, absence of Mycoplasma spp. among our isolates is due to the lack of the facilities for the cultivation of this pathogen in our laboratory. Among the other isolates in this study E.coli and other environmental pathogens (CNS, Strep. non-ag) had the highest prevalence rate (16%, 5.9%, 5.9%) respectively. This finding was similar to reports from earlier investigations in other countries [14, 23, 28, 35, 46, 49, 50]. Presence of high prevalence of environmental pathogens is suggestive of managemental mistakes includes overcrowding; poor ventilation; inadequate manure removal from the back of stalls, alleyways, feeding areas and exercise lots; poorly maintained free stalls; access to farm ponds or muddy exercise lots; dirty maternity stalls or calving areas; and general lack of farm cleanliness and sanitation [19, 34]. All of the above mentioned practices can be noticed in most of the farms in northern Jordan, since they are small family-managed farms.
Our data is compared with international studies since no similar previous studies were conducted in Jordan or surrounding countries. However, variation in the climate, herd size, management practices, and other risk factors might have participated to the differences in prevalence rates of mastitis pathogens among the findings of the preceded works.
The beta-lactams, tetracycline, sulfonamides, and some aminoglycosides have become the first line of antimicrobial agents used for treatment of bovine mastitis in Jordan. Among these classes penicillin, oxytetracycline, sulphamethoxazole, and streptomycin are the most commonly used agents and are present as intramammary infusions in the market. In our study, 61.2% of the isolates were susceptible to enrofloxacin, 58.7% to ciprofloxacin, 47.1% to gentamycin, and 21.4% to neomycin. On the other hand, 87.4% of the isolates were resistant against trimethoprim/ sulphamethoxazole, 84.5% against penicillin, 77.7% against oxytetracycline, and 70.4% against erythromycin.
The prevalence rate of S. aureus as the major cause of mastitis (53.7%) in the present study is in agreement with the studies conducted in Jordan (37.5%) [21], Kenya (34.2%) [46], Switzerland (61%) [39], Canada (47%, 21.7%) [37, 38], and in Ethiopia (42.6%, 24.1%) [13,23]. The high prevalence of S. aureus could be due to its ability to evade and influence the host immune system by production of various enzymes and toxins that cause damage to mammary tissue and allow tissue invasion. Furthermore, S. aureus is capable to survive in the keratin of the teat canal of healthy cows, and to confront phagocytosis. In addition, many S. aureus strains have the ability to resist antibiotic therapy by production of betalactamase an enzyme that inactivates penicillin and closely related antibiotics. Probably around 50% of mastitis S. aureus strains produce beta-lactamase and there is evidence that these strains are more difficult to cure with all antibiotics. [35,26]. Relatively low rate of Streptococcus agalactiae isolates might be due their readily response to treatment as a cause of mastitis, so that cows affected with Streptococcus agalactiae will rarely be presented to our clinic. However, the cases reviewed in this study had the same susceptibility pattern like other pathogens, and that is most likely due its repeating treatment with the same antibiotics over time, since quite few
Analyzing the resistance of each strains isolated revealed the following. Although CNS are considered minor pathogens and can be treated successfully with antibiotic [44], 100% resistance of CNS spp. against trimethoprim/ sulphamethoxazole, oxytetracycline, and streptomycin was revealed. Previous reports recorded high susceptibility of CNS isolates to most of the antibiotics used [11, 13, 17, 39, and 50]. However, a report from Uruguay [14] shared the same results of ours. S. aureus and E.coli isolates showed high resistance against trimethoprim/sulphamethoxazole (90%, 100%), oxytetracycline (85%, 98%), penicillin (87%, 94%) and streptomycin (96%, 95%). Results from Britain [50], Sweden [2], Finland [31], European countries [17], the United States [11, 36] and Germany [42] are in contrast with our findings, except for the resistance against penicillin regarding S. aureus, and the resistance against oxytetracycline regarding E.coli which share the same results. Nevertheless, results from Uruguay [15] agree with our findings. Regarding Strep non-ag nearly 70% of the12 isolates were resistant to most of the antibiotics used except for enrofloxacin and ciprofloxacin. The similarity between the resistance patterns of most of the pathogens might blame to the frequent use of the previous mentioned antibiotics for treatment of mastitis
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324 without even regarding to the culture and sensitivity testing because of their availability and low cost for the farmer in northern Jordan. On the other face of the mirror, enrofloxacin and ciprofloxacin showed the highest sensitivity among all of the isolates in this study, including S.aureus (68%, 64%), E.coli (67%, 66%), Strep non-ag (75%, 73%), CNS (75%, 70%), and Streptococcus agalactiae (75%, 75%). This finding is most probably attributed to the rare use of these types of drugs in the treatment of bovine mastitis in Jordan. There are no abundant previous studies used those antibiotic in their testing. A study in Finland [24] showed the same susceptibility pattern regarding ciprofloxacin. In Germany [16] enrofloxacin and its metabolite ciprofloxacin showed the highest in vitro activities against most bovine pathogens tested especially against S. aureus and E.coli which agrees with our results.
Conclusion Data on antimicrobial resistance among bovine mastitis isolates in northern Jordan is sparse, but resistance patterns are not far dissimilar from those reported from overseas countries and reflect the type of antibiotics which have been used for mastitis treatment. According to the results reported here, the antimicrobial sensitivity test indicated that responses of the various milk bacterial isolates to different antibiotics were almost taking the same pattern, which reflects the possibility of an emergence of an antimicrobial resistance among mastitis bacterial pathogens in northern Jordan and that is would be due to ill-usage and haphazard employment of the antimicrobials that is for sure an issue in our country as our view point as clinicians. Nevertheless, a follow up with culturing more of mastitis cases from different parts of the country is necessary to ensure the presence of this problem. It is critical for Jordanian dairy cattle production that there is continued access to antibiotics for treatment and prevention of mastitis disease. Use of antibiotics must however, be in accordance with guidelines that minimize the risk of emergence or amplification of resistant bacteria. All over, our results demonstrate the importance of establishing a nationwide plan for monitoring the resistance of antibiotics and ensuring the cautious use of antibiotics in the veterinary sector.
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