Nigerian Veterinary Journal 39(3). 2018 Asambe et al.

NIGERIAN VETERINARY JOURNAL ISSN 0331-3026

Nig. Vet. J., September 2018 Vol 39 (3): 199 -208. https://dx.doi.org/10.4314/nvj.v39i3.3 ORIGINAL ARTICLE

In Vitro Comparative Activity of and against Clinical Isolates from Chickens in Benue State, Nigeria

Asambe, A.1*; Babashani, M2. and Salisu, U. S.1

¹.Federal University Dutsinma, Katsina State. 2.Ahmadu Bello University Zaria. *Corresponding author: Email: [email protected]; Tel No:+2348063103254

SUMMARY This study compares the in vitro activities of enrofloxacin and its main metabolite ciprofloxacin against clinical Escherichia coli and non-lactose fermenting enterobacteria isolates from chickens. Ten (10) Escherichia coli and 8 non lactose fermenting enterobacteriaceae species isolated from a pool of clinical cases at the Microbiology Laboratory of the Veterinary Teaching Hospital, University of Agriculture Makurdi were used in this study. Ten-fold serial dilution of 10 varying concentrations (0.1-50μg/mL) of enrofloxacin and ciprofloxacin were tested against the isolates in vitro by Bauer’s disc-diffusion method to determine and compare their antimicrobial activities against the isolates. The 18 isolates tested were susceptible to both enrofloxacin and ciprofloxacin, and their mean values in the susceptibility of Escherichia coli and non-lactose fermenters were significantly different (p < 0.01). The study concluded that the clinical isolates are susceptible to both enrofloxacin and ciprofloxacin though ciprofloxacin exhibit higher activity. Comparatively, ciprofloxacin was found to be more potent than enrofloxacin and the difference statistically significant. Ciprofloxacin was recommended as a better choice in the treatment of bacterial infections of chicken in this area compared to enrofloxacin. It was also recommended that proper steps should be taken in the administration of antimicrobials so as to reduce the incidences of bacterial resistance.

Key words: Escherichia coli, Non-lactose fermenter, Antimicrobials, Ciprofloxacin. Enrofloxacin, Chicken.

INTRODUCTION treatment of chronic respiratory and Fluoroquinolones are among the most gastrointestinal infections (Jelena et al., commonly used antibacterial drugs in 2006; Devreese et al., 2014; Vanni et al., general veterinary practice (Escher et al., 2014 Ruennarong et al., 2016). They also 2011; Kireewan and Suanpairintr, 2017). exhibit rapid bactericidal action against a Enrofloxacin and ciprofloxacin are synthetic wide variety of clinically important fluoroquinolones which acts by inhibiting microorganisms of human and animal origin the DNA gyrase enzyme and commonly (Jelena et al., 2006; Wayne et al., 2011). indicated in intensive poultry farming for the Though their usage in poultry have been

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Nigerian Veterinary Journal 39(2). 2018 Asambe et al. restricted in some countries to avoid the problem to the poultry industry. The development of antimicrobial-resistant indiscriminate use of antimicrobials without bacteria, they are still of importance in the recourse to susceptibility testing is often treatment of human infections (Ferrari et al., attributed to be the major cause (Ramanan et 2015). However, ciprofloxacin usage al., 2013). particularly has persisted with arguments for The aims of this study therefore was to asses its use in animals intensified on the basis of and compare the antimicrobial activities of results of bacterial culture and antimicrobial ciprofloxacin and enrofloxacin against sensitivity testing demonstrating resistance clinical isolates to ascertaining the most to enrofloxacin but susceptibility to appropriate and desirable amongst the two ciprofloxacin (Sumano and Sunamo, 2001; thereby limiting the development of resistant Boothe et al., 2006). strains. Ciprofloxacin is a major metabolite of enrofloxacin used in human medicine MATERIAL AND METHODS (EMEA, 1998), but is only metabolised to a Escherichia coli and non-lactose limited range of 5–10 % in broiler chickens fermenting enterobacteria isolates (Redman, 2007; Slana et al., 2014). It also Ten Avian Escherichia coli and 8 non has similar spectrum of activity with lactose fermenting enterobacteriaceae enrofloxacin but with no reported effect species isolates were tested. The isolates against gram-positive bacteria (Slana et al., were collected from a pool of clinical cases 2014). from Veterinary Microbiology Laboratory of Ciprofloxacin and enrofloxacin are widely the Veterinary Teaching Hospital, used in Nigeria in the management and University of Agriculture, Makurdi. Proper treatment of poultry diseases. Several history of each flock including management reports point to the fact that the (mis)use of practices and previous treatment were noted. fluoroquinolone in chickens have resulted in Liver, spleen, kidney, lungs and bile higher incidences of bacteria resistance samples were collected from either (Abu-Basha et al., 2012; Devreese et al., moribund or dead birds during post-mortem 2014; Vanni et al., 2014). According to the examination and labelled individually. European Food Safety Authority (EFSA), The isolates were identified on the basis of (2014), Salmonella spp., Campylobacter culture, morphological and biochemical jejuni, Campylobacter coli and E. coli characteristics. On the basis of microscopic derived from domestic chickens’ resistance examination, morphology of bacteria was to ciprofloxacin stood at 37.3 %, 44.1 %, noted as rod, spiral or filament. It was 78.4 % and 57.6 %, respectively. differentiated by Biochemical Resistant bacteria from food animals can characterization as per Reynolds (2005). On spread to humans directly or indirectly cultural basis, MacConkey agar and Eosin- (Adenipekun et al., 2015; Rugumisa et al., methylene blue agar (EMBA) were used to 2016). This microbial resistance as well as confirm the identity of the E. coli isolates. the spread to human population are growing Swabs collected were directly inoculated and the outlook for the use of antimicrobial onto blood agar and MacConkey agar in drug in the near future is uncertain. This is a duplicates for every sample inoculum and significant public health concern when incubated at 37ºC for 24 hours. Similar animal husbandry practices promote colonies from growth observed were resistance to medically important “Gram” stained and examined on the basis (Anderson et al., 2003; Rugumisa et al., of size, morphology and staining 2016). Several reports of outbreaks of characteristics. The Gram negative bacterial diseases of poultry are of public coccobacilli colony types were further health concern and have posed enormous characterized.

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On MacConkey agar only lactose susceptibility to the antimicrobials while fermenting (LF+) pink coloured colonies growth around the disc implies resistance. were isolated and sub cultured for further The diameters of the zones of inhibition as characterization to check whether the judged by an unaided eye were measured to bacteria are E. coli (i.e., there are other the nearest whole millimetre (mm) using a lactose fermenters like: Klebsiella and calibrated scale. The average diameters of Enterobacter). The LF+ colonies were the zones of inhibition were calculated and reinoculated on EMB agar for presence of result interpreted for each by metallic sheen characteristics of E. coli, comparing to the standard chart which while non-lactose fermenting (LF-) represents the National Committee for colourless colonies were isolated and sub Clinical Laboratory Standards (NCCLS) cultured on Muller Hinton agar to obtain subcommittee’s recommendation for the pure cultures of non-lactose fermenting particular bacteria of interest. However, as enterobacteriaceae. Pure cultures of both the study was not designed to assess the isolates grown in nutrient broth were mixed incidence of resistance to the antimicrobial with sterile glycerol 1:1 and stored at agents, any isolate that was not sensitive to −20°C. an antimicrobial in the concentration range tested was deemed resistant and excluded Preparation of antibacterial drug stock from the analyses. solutions and dilution trays Standard ciprofloxacin and enrofloxacin Data analyses with 99 % purity were both sourced from The means were determined standard error Sigma-Aldriech, USA. The serial dilutions of mean (SEM). Mean difference between of the antimicrobial agents were prepared groups were compared using one-way from a stock solution of 10 varying analysis of variance (ANOVA) followed by concentrations (50 – 0.1 μg/ml) using Tukey’s post hoc test, while t-test was appropriate solvents with positive growth applied to compare the effect of the two control tubes without an antimicrobial agent fluoroquinolones at varying concentrations (Andrews, 2001). on all isolates at 5 % significant level (p ≤ 0.05) using the Statistical Package for Social Disc diffusion test Sciences (SPSS) version 20.0. The isolates were tested by the Kirby- Bauer’s disk-diffusion method as described RESULTS by Bauer et al. (1966). A lawn culture was The results from the determination of zones prepared using the primary inoculums by of inhibition by disc diffusion test showed spreading the inoculums onto the agar that Escherichia coli was susceptible to the surface nicely using a sterile glass spreader two antimicrobials at concentrations of (sterilized by 70 % alcohol). (12.50 - 50.00) μg/mL exhibiting larger After 15 minutes, ciprofloxacin and zones of inhibition in ciprofloxacin than enrofloxacin (50 – 0.1 μg) impregnated enrofloxacin. E. coli showed resistance to discs in triplicates were applied onto the the two antimicrobials at concentrations agar surface by applicator/ sterile forceps below 12.50 (μg/mL). The results of with optimum distance between each Escherichia coli isolates susceptibility to antimicrobial discs. All the varying ciprofloxacin and enrofloxacin as estimated concentrations were prepared on separate from growth inhibition zone diameters are plates. The petri plates embedded with presented in TABLE 1. antimicrobial discs were then incubated at The non-lactose fermenters exhibited 37ºC for 24 hours. susceptibility to the two antimicrobials Zones of inhibition indicated by a clear area within concentrations range of 6.25 - 50.50 around the discs were measured to imply the (μg/mL) respectively over the entire 24-hour

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Nigerian Veterinary Journal 39(2). 2018 Asambe et al. incubation period. The non-lactose against Enterobacteriaceae, fastidious fermenters were however resistant to the two Gram-negative bacteria and some Gram antimicrobials in concentrations below 6.25 positive bacteria (Wayne (μg/mL). Ciprofloxacin also produced et al., 2011). Many Gram-negative bacteria higher zones of inhibition TABLE 2. that have become resistant to other classes The t-test comparing the mean differences in of antibacterial agents remained susceptible zones of inhibition between E. coli and non- to the fluoroquinolones (Sárközy, 2001). lactose fermenting (NLF) Several reports about in vitro activities of Enterobacteriaceae measured at varying the fluoroquinolones against bacterial concentrations of each of the two clinical isolates of animal origin exist (Pohl antimicrobial agents at p ≤ 0.05 was et al., 1991; Cid et al., 1994; Šeol, 2005). significantly associated (TABLES 3 and 4). Ciprofloxacin and enrofloxacin have been used extensively in this area in recent years DISCUSSION in the management of poultry diseases The majority of the 18 tested isolates in this generally. Šeol, (2005) reported the proved study were susceptible to enrofloxacin and usefulness of ciprofloxacin and enrofloxacin ciprofloxacin. In general, the as potent alternatives for the treatment of fluoroquinolones exhibit excellent activity

TABLE 1: Average zones of inhibition of Escherichia coli against varying concentrations of ciprofloxacin and enrofloxacin Concentration Inhibition mean ± SEM (Cipro) Inhibition mean ± SEM (Enro) 50.000 1.502 ± 0.295 0.367 ± 0.184 25.000 1.204 ± 0.266 0.178 ± 0.120 12.500 0.822 ± 0.212 0.014 ± 0.014 6.250 = = 3.125 = = 1.560 = =

TABLE 2: Average zones of inhibition of Non-lactose fermenters against varying concentrations of ciprofloxacin and enrofloxacin Concentration Inhibition mean ± SEM (Cipro) Inhibition mean ± SEM (Enro) 50.000 2.530 ± 0.347 1.279 ± 0.260 25.000 1.834 ± 0.456 0.896 ± 0.226 12.500 1.726 ± 0.399 0.546 ± 0.269 6.250 1.626 ± 0.379 0.413 ± 0.226 3.125 = = 1.560 = =

TABLE 3: Comparative effects of ciprofloxacin (C) and enrofloxacin (E) against Escherichia coli Concentration Difference in mean ± SEM 95 % CI/t-test p-value C1 vs E1 1.135 ± 0.357 0.381 to 1.889/ 3.177 0.005 C2 vs E2 1.026 ± 0.303 0.386 to 1.666/ 3.383 0.003 C3 vs E3 0.808 ± 0.224 0.334 to 1.281/ 3.601 0.002 C4 vs E4 = = = C5 vs E5 = = = C6 vs E6 = = =

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TABLE 4: Comparative effects of ciprofloxacin (C) and enrofloxacin (E) against Non-lactose fermenters Concentration Difference in mean ± SEM 95 % CI/t-test p-value

C1 vs E1 1.251 ± 0.433 0.322 to 2.180/2.889 0.011

C2 vs E2 0.938 ± 0.509 -0.154 to 2.029/1.843 0.086

C3 vs E3 1.180 ± 0.481 0.148 to 2.212/ 2.453 0.027

C4 vs E4 1.214 ± 0.441 0.269 to 2.159/ 2.755 0.015

C5 vs E5 = = =

C6 vs E6 = = = methicillin-resistant strains. This is an the introduction of ciprofloxacin and might indication that inappropriate use might have developed acquired resistance. favour the development of resistant strains Cid et al. (1994) reported excellent in vitro in vivo. Results of our study are very similar activities of the fluoroquinolones against E. to those discussed above and confirmed the coli. The report indicated that 71.0 % of excellent activity of fluoroquinolones tested strains were sensitive to enrofloxacin, particularly enrofloxacin and ciprofloxacin 26.2% were resistant and 2.7% were against Escherichia coli and intermediate in sensitivity, while the Enterobacteriaceae. majority of tested strains (93.4 %) were In this study, ciprofloxacin has shown to be susceptible to ciprofloxacin, 3.8% were a more potent antimicrobial agent compared resistant and 2.7% showed intermediate to enrofloxacin as evidenced in the larger sensitivity. Among the quinolone antibiotics, zones of inhibition. Abu-Basha et al. (2012) ciprofloxacin was still be the most active or and Kotilainen et al. (2005) similarly potent agent, which also agrees with our reported of better ciprofloxacin activity findings. compared to enrofloxacin against Pohl et al. (1991) have reported that Escherichia coli and salmonella infections relatively high percentages of E. coli isolates respectively. This is also similar to previous of bovine origin were resistant to reports of Hoogkamp-Korstanje, (1984) and enrofloxacin activity in vitro, whereas our Ridgway et al. (1984) whose separate isolates were highly susceptible to studies showed ciprofloxacin of being a enrofloxacin. Hamisi et al. (2014) also more potent fluoroquinolone by exhibiting reported higher resistance (54.5%) among E. the broadest spectrum of activity against all coli isolates to the fluoroquinolone but with Gram-negative bacteria and streptococci a relatively limited resistance to tested. Prescott and Yielding, (1990) also ciprofloxacin (3.5%). This difference might reported of a similar activity of be explained, in part, by published ciprofloxacin compared to enrofloxacin observations that ciprofloxacin is more though both are reported to have structural active and potent than other similarity and similar antibacterial spectrum. fluoroquinolones against most bacteria Several other reports of pharmacokinetics of (Lautzenhiser et al., 2001; Rugumisa et al., ciprofloxacin in domestic animals (Dowling 2016). et al., 1995; Ovando et al., 2000) showing Spencer (1996) in an 8-year survey of 29 good pharmacokinetic properties and 425 hospital P. aeruginosa isolates found therapeutic possibilities exist. The present 95% susceptibility to ciprofloxacin and report is expected due to the fact that attributed the higher susceptibility to very enrofloxacin has been used in this area for limited use of ciprofloxacin in veterinary the treatment of animal infections long after practice in Croatia. Contrastingly, Mueller-

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Premru and Gubina (2000) found 45.7% of to enrofloxacin was also noted both in the tested strains resistant to ciprofloxacin. Grobbel et al. (2007) data and in other Shawar et al. (1999), similarly reported a reports (Riddle et al., 2000). Previous higher resistance of 20.7 % to ciprofloxacin. studies have shown limited evidence for In contrast, enrofloxacin showed a relatively preferential activity for ciprofloxacin against low activity against P. aeruginosa isolates E. coli (Zhao et al., 2005) but a more when compared to ciprofloxacin but also consistent body of evidence indicates that S. higher compared to the results of other aureus is more susceptible to enrofloxacin authors (Cid et al., 1994). (Watts et al., 1997; Jones et al., 1998). A study by Frazier et al. (2000) showed that Minimum Inhibitory Concentrations (MICs) among , enrofloxacin, results also indicates susceptibility to ciprofloxacin and ; marbofloxacin ciprofloxacin at 1 (μg/mL) and 2 (μg/mL) has greater Cmax (maximum plasma drug for enrofloxacin (Pohl et al., 1991; Cid et concentration curve lg/ml · h) and ACU0- al., 1994) thereby supporting better last (the area under the plasma drug antimicrobial activity of ciprofloxacin when concentration versus time curve lg/ml · h) compared to enrofloxacin. compared to enrofloxacin, ciprofloxacin, The interest of the medical community in enrofloxacin plus ciprofloxacin combined, fluoroquinolones has not decreased during or difloxacin. Those results suggest that the last 10 years and many new ones have even though ciprofloxacin showed better been developed and are under investigation activity than enrofloxacin (Ovando et al. (Ovando et al., 2004). Ciprofloxacin use in 1999) and similar activity to marbofloxacin, human medicine has proved effective in because of its pharmacokinetic properties, several infections (Grobbel et al., 2007). marbofloxacin should be the quinolone of Because of its broad and intense activity choice. against Gram negative bacteria and the fact Grobbel et al. (2007) in their studies showed that no cross-resistance with beta-lactams or that ciprofloxacin had significantly greater aminoglycosides occurs, it was also in vitro antibacterial activity than suggested to be of considerable usefulness in enrofloxacin against M. haemolytica, P. veterinary medicine (Nouws et al., 1988; multocida and E. coli, whereas enrofloxacin Brown, 1996). showed greater activity than ciprofloxacin Our in vitro data show ciprofloxacin to have against S. aureus. Comparison of the greatest potency against E. coli and non- sensitivities of individual pathogen isolates lactose fermenting enterobacteria isolates to enrofloxacin and ciprofloxacin tested in comparison to enrofloxacin. In this highlighted notable differences in the MIC50 case, our in vitro fluoroquinolone activity profiles, in particular when considering E. data suggest that treatment with coli and S. aureus. Available data showed ciprofloxacin is preferential to use of 54 of 70 E. coli isolates to be at least one enrofloxacin, as ciprofloxacin has the log2 step more sensitive to ciprofloxacin highest in vitro activity against the tested than enrofloxacin; conversely 33 of 47 S. isolates. aureus isolates were more sensitive to enrofloxacin than ciprofloxacin. This CONCLUSION difference is reflected in the MIC50 values The study concluded that enrofloxacin and for each agent in the case of E. coli ciprofloxacin are still effective in the (0.016μg/mL for ciprofloxacin and management and treatment of bacterial 0.03μg/mL for enrofloxacin) but not for S. infections of chicken in Benue State. aureus (0.12μg/mL for both agents). Higher However, ciprofloxacin was reported to sensitivity of E. coli ATCC 25922 to have exhibited higher activity compared to ciprofloxacin and of S. aureus ATCC 29213 enrofloxacin. The mean values in the zones

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