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Isolation and antibiotic sensitivity of uterine microbial pathogens a study of 30 endometritis affected mares.


Endometritis is the most common cause of infertility in brood mares and the condition can be categorized variously, viz. acute, chronic, clinical, sub-clinical, pre-partum, postpartum, bacterial, fungal and viral endometritis and persistent mating induced endometritis (PMIE) and Post-breeding metritis (PBM). Uterine infection is inevitable during breeding and foaling in brood mares and resolves within 72 hours post-breeding and 10-15 days post-foaling in postpartum mares (Ricketts and Mackintosh, 1987; Card, 1997). Young and maiden mares are resistant to such infections owing to adequate cellular and humoral immunological uterine defense mechanisms (Hughes, 1993; Hurtgen, 2006). However, old and pleuriparous mares are unable to overcome uterine infection, due to inadequate uterine defense mechanism and poor conformation, leading to accumulation of uterine fluid and subsequent development of endometritis associated with oedema and thickness of uterine wall (Hurtgen, 2006; Lu and Morresey, 2006). Brood mares also become highly susceptible to uterine infections under exogenous progesterone supplementation (Behrendt-Adam et al., 2000). The innate resistance of fertile mares to uterine bacterial and fungal endometritis can be compromised by pneumovagina, leading to vaginitis, pneumo uterus and persistent endometritis (Oral et al., 2009). The older multiparous mares that are more often affected by uterine infections are usually also the most valuable proven mares (Relias, 2001), so great effort and money is invested every year in managing and treating these conditions. Whatever the underlying cause for development of uterine infections, more often than not bacterial or fungal pathogens can be isolated from samples derived from uteri of such mares, during routine microbiological studies.

Many bacterial and fungal pathogens have been identified and isolated from uteri of endometritis mares. Bacterial pathogens reported in equine endometritis includes p-haemolytic Streptococcus sp. (S. zooepidimicus, S. equisimilis), Escherichia coli, Staphylococcus sp. (S. aureus, S. albus, S. intermedius), Pseudomonas aeruginosa. Klebsiella sp. (K. Pneumonae, K. aerogenes), Corynebacterium sp. Taylorella equigenitalis, Proteus sp. Enterobacter cloaca (Collins, 1964; Scott et al., 1971; Kuhad, 1995; Shin et al., 1979; Mohmmadsadegh et al., 2005; Crouch et al., 1972; Hughes et al., 1966; Ley, 1994; Miller and Francis, 1974, Watson, 1988; Asbury and Lye, 1993; Neilson, 2005; McCue, 2008; Riddle et al., 2007).The authors successfully isolated p-hemolytic Streptococcus, Corynebacterium sp. and Escherichia coli from enrometritis mares and found incidences of p-hemolytic Streptococcus more than that of Escherichia coli (Nafis, 2011, Nafis and Pandey, 2012a, Nafis and Pandey, 2012b). However, fewer workers have recorded high incidence of Escherichia coli (Albihn, 1998; Ghasemzade-Nava et al., 2004) and Coryne-bacterium sp. (Ball et al., 1988a) in equine uterine infections.

Commonly isolated fungal pathogens from equine endometritis include Candida tropicaiis (Bouters and Vandelplassche, 1973; Narwal and Monga, 1994), Candida parapsilosis (Freeman et al., 1986), Candida lusitaniae, Candida rugosa (Chengappa et al., 1984; Petrites-Murphy et al., 1996; Dascanio et al., 2000), Aspergillus fumigates, Aspergillus terreus, Aspergillus flavus, Aspergillus niger, Mucor sp., Rhizopus sp. (Narwal and Monga, 1994; Pugh et al., 1986b; Mahaffey and Rossdale, 1965). Authors isolated yeast sp. from one such case (Nafis, 2011).

Intrauterine antibiotics along with parenteral antibiotic therapy are often advocated in equine endometritis. Further, pre-treatment with uterine ecbolics increases therapeutic efficacy of antibiotic treatment in endometritis mares (Pycock and Newcombe, 1996). Persistent uterine infection with highly pathogenic organisms such as Klebsiella, Pseudomonas and Taylorella warrants preference for intrauterine antibiotics over parentral antibiotic therapy (Watson, 1997; Hughes et al., 1966). Further, minimum inhibitory concentration (MIC) is more rapidly achieved with intrauterine administration of antibiotics as compared to their systemic antibiotic therapy (Bowen et al., 1984; Spensley et al., 1986). Indiscriminate use of antibiotics in post-partum equine endometritis favours establishment of fungal uterine infection along with growth of resistant bacteria populations in uterine lumen (Davis and Abbitt, 1977; Ricketts, 1997) and thus such therapy should not be adopted in treating uterine infections. This is further complicated by the fact that in Veterinary indications related to reproduction, treatment practices exist that can't be considered evidence based (Pyorala et al., 2014).

It was in this backdrop that the current investigation was conceived so as to establish the sensitivity and resistance patterns of common prevalent bacterial and fungal uterine pathogens viz Streptococcussp., Corynebacterium sp., Escherichia coli and Yeast to routinely used intrauterine antibiotics. The basic aim of the study was to serve as an empirical guide from time to time, while prescribing antibiotics for treatment of uterine infections in mares.

Materials and Methods

Experimental animals and laboratory

Mares stationed at Equine Breeding Stud (EBS) of Remount Veterinary Corps (RVC) of Indian Army at Hisar, Haryana were used during the investigation. Out of 30 mares that showed some degree of endometritis upon examination by uterine cytology and uterine ultrasonography, uterine microbes were identified only in 15 of them by using uterine culture technique. The uterine samples were collected by low volume flush technique (LeBlanc, 2008; Card et al., 2004; Ball et al., 1988a) using two way Foley's catheter (Bard Urological Georgia, USA; No. 24) and sterilized phosphate buffer saline (pH, 7.2). The samples were processed for microbiological investigation (Fig. 1-4). The uterine ultrasound was done using a linear array probe operating at 5/7 interchangeable frequency. Three bacterial pathogens (p-Streptococcus sp./7 mares, Corynebacterium pyogens/5 mares and Escherichia coli/2 mares) and a single fungal pathogen (yeast/1 mare) were isolated from these endometritis mares.

In-Vitro Antibiotic sensitivity test (ABST)

The in-vitro antibiotic sensitivity test (ABST) was performed to understand the sensitivity and resistance pattern of different antibacterial and antifungal agents which find place in prescriptions for equine uterine infections. The sensitivity for a total of 12 antibacterial and 6 antifungal antibiotics was evaluated. Antibiotics selected for this purpose were all reportedly used by different equine practitioners via intrauterine route for treatment of uterine infections. The pattern of sensitivity of various bacterial isolates to different antibiotics was studied by single disc diffusion method (Ellner, 1978) using commercially available discs. Antibiotic discs of different concentrations were used. Penicillin-G 100 units; Streptomycin 10pg; Tetracycline 30pg; Am picillin 10pg; Gentamicin 10pg; Ciprofloxacin 5pg; Ceftriaxone 30pg; Cephalexin 30pg; Chloramphenicol 30pg; Cefuroxime 30pg; Norfloxacin 10pg; Co-trimoxazole 25pg. Nutrient agar medium or Muller-Hinton Agar medium was used for AST. The diameters of complete zones of inhibition were recorded and interpretation was made as per standards provided in zone size interpretative chart for antibiotics (Fig. 5).






In-vitro sensitivity of fungal isolates to different antibiotics was carried out by disc diffusion method according to recommendations described in M44-A guidelines (NCCLS, 2004). Sensitivity was evaluated against following antibiotic discs. Ketoconazole 10pg; Itraconazole 10[micro]g; Clotrimazole 10[micro]g; Fluconazole 10[micro]g; Amphotericin 100 units and Nystatin 100 units. Sabouraud's dextrose agar (SDA) medium was used for the test. The isolates were classified as resistant or sensitive to a particular antibiotic based on diameter of zone of inhibition (Pfaller et al., 2004).



In-vitro sensitivity of uterine bacterial and fungal pathogens recovered from infertile mares are shown in Table 1.

All uterine bacterial pathogens were sensitive to Gentamicin, Ceftriaxone and Cefuroxime (100%), followed by Tetracycline and Chloramphenicol (92.8%), Ciprofloxacin and Cephalexin (85.7%), Ampicillin (71.5%) and Penicillin (50%). Uterine pathogens were least sensitive to Streptomycin (7.2%) followed by Co-trimoxazole (42.8%). Maximum uterine bacterial pathogens showed resistance against Streptomycin (92.8%) followed by Co-trimoxazole (57.2%), Penicillin (50%), Ampicillin (28.5%), Cephalexin (14.3%) and Ciprofloxacin (14.3%). The single uterine fungal pathogen recovered from an infertile mare was sensitive to Amphotericin, Fluconazole, Ketoconazole and Nystatin and resistant to Cotrimazole and Itraconazole. The results of sensitivity of uterine bacterial and fungal pathogens to different antibiotics are shown in Fig. 6.

Sensitivity pattern (sensitivity and resistance) of uterine bacterial pathogens revealed a wide variation as same pathogen recovered from different mares showed different sensitivity pattern to antibiotics. The in-vitro sensitivity of individual bacterial isolates to different antibiotics is given in Table 2.

Streptococcus sp. showed maximum sensitivity to Ampicillin, Cephalexin, Cefuroxime, Ceftriaxone, Chloramphenicol, Ciprofloxacin, Gentamicin and Tetracycline antibiotics (100% sensitive) and moderate sensitivity to Penicillin (71.4% sensitive) and Co-trimoxazole (57.1%). Streptococcus sp. was least sensitive to Streptomycin (14.2%). Maximum isolates of Corynebacterium pyogenes were sensitive to Cephalexin, Cefuroxime, Ceftriaxone and Gentamicin (1 00%) followed by moderate sensitivity to Chloramphenicol (80%), Ciprofloxacin (80%), Tetracycline (80%), Ampicillin (60%) and Penicillin (40%). All Corynebacteria were resistant to Co-trimoxazole. Escherichia coli was sensitive to Cefuroxime, Ceftriaxone, Chloramphenicol, Co-trimoxazole, Gentamicin and Tetracycline (100%) followed by Ciprofloxacin (50%). The isolates of Escherichia coli were resistant to Ampicillin, Cephalexin and Streptomycin (1 00% resistance). The in-vitro sensitivity pattern of uterine pathogens is also shown in Fig. 7 below.


The in vitro sensitivity pattern of uterine bacterial and fungal pathogens to different antibiotics showed maximum susceptibility of uterine bacterial pathogens to Gentamicin, Ceftriaxone and Cefuroxime (100% effective in all bacterial isolates), followed by Tetracycline and Chloramphenicol (92.8% bacterial isolates were sensitive), Ciprofloxacin and Cephalexin (85.7% bacterial isolates sensitive to each) and Ampicillin (71.5% bacterial isolates sensitive). Streptomycin was least effective against uterine bacterial pathogens (7.2%bacterial isolates sensitive), followed by Co-trimoxazole (42.8% effective). Uterine bacterial pathogens were equally sensitive and resistant to Penicillin (50% sensitive and 50% resistant). Similar observations of high susceptibility of uterine bacterial pathogens to Gentamicin (99-100%) and Chloramphenicol (77.76-88.9%) was reported by Sharma et al. (1986) and Houdeshell and Hennessey (1972) respectively. Other workers also recorded similar susceptibility pattern of uterine bacterial pathogens to Chloramphenicol (Narwal and Monga, 1994; Albihn et al., 2003), and to Ampicillin, Gentamicin and Tetracycline (Moreno et al., 1995; Berwal et al., 2006). However, high sensitivity of uterine bacterial pathogens to Penicillin (100%) and Streptomycin (72.2%) was reported by Uppal et al. (1994) and Berwal et al. (2006), respectively.


All Streptococcal isolates recovered from uteri of mares were sensitive to Ampicillin, Cephalexin, Cefuroxime, Ceftriaxone, Chloramphenicol, Ciprofloxacin, Gentamicin and Tetracycline (100% each), but were relatively less susceptible to Cotrimoxazole (57.1%) and Penicillin (71.4%). Similarly, Albihn et al. (2003) found that all Streptococcal isolates were sensitive to Ampicillin (100%) and Chloramphenicol (100%), but less susceptible to Gentamicin (52%) and Tetracycline (23%). However, Berwal et al. (2006) recorded lesser sensitivity of Streptococcal pathogens to Gentamicin and Chloramphenicol (66.6% each) and resistance to Penicillin. Variation in sensitivity pattern of uterine pathogens to different antibiotic is due to indiscriminate use of antibiotics often without in vitro antibiotic sensitivity test or inadequate uterine sampling (Ball et al., 1988a).

Corynebacterium pyogenes were 100% sensitive to Cephalexin, Cefuroxime, Ceftriaxone and Gentamicin and 80% isolates were sensitive to Ampicillin and Penicillin respectively. Similar sensitivity pattern of Corynebacterium pyogenes to Gentamicin (100%) was recorded by Sharma et al. (1986). However, Berwal et al. (2006) recorded 100% sensitivity of Corynebacterium pyogenes to Ampicillin.

Escherichia coli isolates recovered from uteri of infertile mares were 100% sensitive to Cefuroxime, Ceftriaxone, Chloramphenicol, Gentamicin and Tetracycline antibiotics and 50% isolates were susceptible to Ciprofloxacin. Similar pattern of sensitivity of Escherichia coli was recorded by Berwal et al. (2006). The recorded resistance of Escherichia coli to Streptomycin and Ampicillin simulates with observations of Narwal and Monga (1994), Albihn et al. (2003) and Berwal et al. (2006).

The only isolate of yeast was found sensitive to Fluconazole, Ketoconazole, Amphotericin B and Nystatin and resistant to Clotrimazole and Itraconazole antibiotics. Sensitivity pattern of fungal uterine pathogen (yeast) agrees with reported sensitivity of yeast to Ketoconazole (Berwal et al., 2006; Narwal et al., 1994).


The in vitro antibiogram of 14 uterine bacterial isolates showed that all pathogens were sensitive to Gentamicin, Ceftriaxone and Cefuroxime antibiotics (100%), followed by Tetracycline and Chloramphenicol (92.8%), Ciprofloxacin and Cephalexin (85.7%), and Ampicillin (71.5%). Uterine bacterial pathogens were least sensitive to Streptomycin (7.2%), followed by Cotrimoxazole (42.8%). Penicillin was found to be effective against 50% uterine pathogens. The single fungal isolate (yeast) was sensitive to Amphotericin, Fluconazole, Ketoconazole and Nystatin and resistant to Cotrimazole and Itraconazole. The different isolates of particular uterine bacterial pathogens recovered from different mares showed different sensitivity patterns to various antibiotics. 100% isolates of Streptococcus sp. were sensitive Ampicillin, Cephalexin, Cefuroxime, Ceftriaxone, Chloramphenicol, Ciprofloxacin, Gentamicin and Tetracycline, followed by Penicillin (71.4%) and Co-trimoxazole (57.1%). However, only 14.2% of Streptococcus sp. was sensitive to Streptomycin. Corynebacterium pyogenes was 100% sensitive to Cephalexin, Cefuroxime, Ceftriaxone and Gentamicin, followed by Chloramphenicol, Ciprofloxacin and Tetracycline (80%). Ampicillin was effective against 60% and Penicillin against 40% isolates of Corynebacterium sp. All Corynebacteria (100%) were resistant to Cotrimoxazole. All isolates of Escherichia coli (100%) were sensitive to Cefuroxime, Ceftriaxone, Chloramphenicol, Co-trimoxazole, Gentamicin and Tetracycline antibiotics. Ciprofloxacin was effective against 50% isolates of E.coli. Escherichia coli were 100% resistant to Ampicillin, Cephalexin and Streptomycin.


Sincere thanks to the administration of EBS-Hisar for providing us the mares and assistance in terms of manpower. Special thanks are due to Lt. Col (Dr) A H Haldar and Lt. Col (Dr) J Taneja for their valuable cooperation.


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(1.) Resesrch Scholar and Corresponding author. E-mail:

(2.) Professor

(3.) Senior Scientist, Central Laboratory

Nafis I. Assad (1), N.S. Bugalia (2), R.K. Chandolia (2) and Anshu Sharma (3)

Department of Veterinary Gynaecology and Obstetrics

College of Veterinary Sciences

Lala Lajpat Rai University of Veterinary and Animal Sciences (LUVAS)

Hisar--125004 (Haryana)
Table 1: In-vitro sensitivity pattern of uterine
bacterial and fungal pathogens

Antibiotic                           Sensitive       Resistant
                                     Pathogens       pathogens

Antibacterials   Ampicillin        71.5% (10/14)   28.5% (4/14)
                 Cephalexin        85.7% (12/14)   14.3% (2/14)
                 Cefuroxime        100% (14/14)    0.00% (0/14)
                 Ceftriaxone       100% (14/14)    0.00% (0/14)
                 Chloramphenicol   92.8% (13/14)    7.2% (1/14)
                 Ciprofloxacin     85.7% (12/14)   14.3% (2/14)
                 Co-trimoxazole    42.8% (6/14)    57.2% (8/14)
                 Gentamicin        100% (14/14)    0.00% (0/14)
                 Penicillin        50.0% (7/14)    50.0% (7/14)
                 Streptomycin       7.2% (1/14)    92.8% (13/14)
                 Tetracycline      92.8% (13/14)    7.2% (1/14)
Antifungals      Amphotericin       100% (1/1)      0.00% (0/1)
                 Cotrimazole        0.00% (0/1)     100% (1/1)
                 Fluconazole        100% (1/1)      0.00% (0/1)
                 Itraconazole       0.00% (0/1)     100% (1/1)
                 Ketoconazole       100% (1/1)      0.00% (0/1)
                 Nystatin           100% (1/1)      0.00% (0/1)

Table 2: In vitro sensitivity pattern of individual bacterial
isolates to different antibiotics.

Bacterial isolate     A (a)    Pr (b)   Cu (c)    Ci (d)     C (e)

Streptococcus sp.     100%      100%     100%      100%      100%
pyogenes              60.0%     100%     100%      100%      80.0%
Escherichia coli      0.0%      0.0%     100%      100%      100%

Bacterial isolate    Cf (f)    Co (g)     G (h)     P (i)     S (j)

Streptococcus sp.     100%      57.1%     100%      71.4%     14.2%
pyogenes              80.0%     0.0%      100%      40.0%     0.0%
Escherichia coli      50.0%     100%      100%      0.0%      0.0%

Bacterial isolate     T (k)

Streptococcus sp.     100%
pyogenes              80.0%
Escherichia coli      100%

(a) Ampicillin; (b) Cephalexin; (c) Cefuroxime; (d) Ceftriaxone; (e)
Chloramphenicol; (f) Ciprofloxacin; (g) Co-trimoxazole; (h)
Gentamicin; (i) Penicillin; (j) Streptomycin; (k) Tetracycline.
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Title Annotation:Research Article
Author:Assad, Nafis I.; Bugalia, N.S.; Chandolia, R.K.; Sharma, Anshu
Publication:Intas Polivet
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Date:Jul 1, 2015
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