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High Level Aminoglycoside Resistance in Enterococcus, Pediococcus and Lactobacillus Species from Farm Animals and Commercial Meat Products

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High Level Aminoglycoside Resistance in Enterococcus, Pediococcus and Lactobacillus Species from Farm Animals and Commercial Meat Products Ann Microbiol (2016) 66:101–110 DOI 10.1007/s13213-015-1086-1 ORIGINAL ARTICLE High level aminoglycoside resistance in Enterococcus, Pediococcus and Lactobacillus species from farm animals and commercial meat products George Jaimee1 & Prakash M. Halami1 Received: 10 September 2014 /Accepted: 8 April 2015 /Published online: 2 May 2015 # Springer-Verlag Berlin Heidelberg and the University of Milan 2015 Abstract Inappropriate use of aminoglycosides in animal I40a suggesting its involvement in antibiotic resistant gene husbandry has led to the selection and emergence of high- transfer. Besides, strains of L. plantarum, a species used as level aminoglycoside resistance (HLAR) in lactic acid bacte- probiotic, isolated in this study showed the occurrence of ria (LAB). The objective of this study was to assess the pres- aph(3′)IIIa as well as aac (6′)Ie-aph(2″)Ia genes that could ence of aminoglycoside resistant LAB in farm animals and be of concern in human health. The findings of the study meat products. Gentamicin resistant LAB (n=138) were se- highlight the spread and emergence of multi-resistance genes lectively isolated from 50 different meat and farm animal for aminoglycoside antibiotics among beneficial LAB. sources. These native isolates of LAB were subsequently characterized for their minimum inhibitory concentration to Keywords Lactic acid bacteria . Minimum inhibitory seven different aminoglycoside antibiotics. HLAR to genta- concentration . Aminoglycoside . Random amplified micin, kanamycin and streptomycin was found to be 38 %, polymorphic DNA . Integrase 45 % and 15 %, respectively. Selected cultures of LAB were identified by random amplified polymorphic DNA (RAPD)-PCR and 16S rDNA gene sequencing. Subsequent Introduction detection for the presence of nine aminoglycoside modifying genes [aac(6′)Ie-aph(2″)Ia, aph(3′)IIIa, aad6, ant(6)Ia, The spread of resistance to antibiotics among bacteria is ant(9)Ia, ant(9)Ib, aph(2″)Ib, aph(2″)Ic and aph(2″)Id] was alarming. In the global scenario, the development and carried out by PCR. The Enterococcus spp. (n=64) and spread of resistance to clinically significant drugs in com- Lactobacillus plantarum (n=6) isolated from farm animals mensal bacteria is associated with their improper use in and chicken sausages, respectively, were positive for the animal husbandry (Mathur and Singh 2005). The situation bifunctional gene, aac(6′)Ie-aph(2″)Ia in PCR. In addition, is of serious concern when it comes to lactic acid bacteria Enterococcus sp. (n=17), Lactobacillus plantarum (n=3), (LAB), which are beneficial microflora that can develop and Pediococcus lolii (n=2) possessed the kanamycin resis- resistance to life-saving aminoglycoside drugs (Jackson tance gene, aph(3′)IIIa. Other LAB viz. Enterococcus faecalis et al. 2010). Aminoglycosides are regarded as vital drugs (n=2), E. faecium (n=2) and L. plantarum (n=1) harbored for the treatment of life-threatening infections (United the streptomycin resistance gene, aad6. The integrase (int) States Pharmacopeial Convention 2008). High level resis- gene, characteristic to Tn 916-Tn 1545 was detected in tance to aminoglycosides in bacteria may lead to ineffec- Enterococcus faecalis CS11+ and Enterococcus cecorum tive therapeutic crisis. Many countries have banned the administration of certain antibiotics in animal husbandry due to their preferred usage in human medicine (Shwarz * Prakash M. Halami et al. 2000). However, aminoglycosides are recommended [email protected] for therapy and prophylaxis in farm animals owing to their efficient bactericidal mode of action against Gram- 1 Microbiology and Fermentation Technology, CSIR-Central Food negative and Gram-positive bacteria (United States Technological Research Institute, Mysore 570020, India Pharmacopeial Convention 2008). 102 Ann Microbiol (2016) 66:101–110 Bacterial resistance to aminoglycosides occurs due to mu- LAB are in demand industrially, because of their beneficial tations, impaired transport and acquired resistance (Ramirez aspects in fermented food and pharma-based therapeutics and Tolmasky 2010). The most common mode of aminogly- (Popova et al. 2012). The quality presumption safety (QPS) coside resistance in Gram-positive bacteria is the acquisition status, which ensures the absence of acquired resistance, has of aminoglycoside-modifying genes (Bismuth and Courvalin to be attained in order to use LAB in food or probiotic product 2010). Clinically, the bifunctional gene aac(6′)Ie-aph(2″)Ia development (EFSA 2012). However, this norm becomes di- confers resistance to almost all aminoglycosides except strep- luted in the case of food products, in view of the scale of tomycin. It has been associated with high-level gentamicin operation, wherein such stringent tests to avoid the inclusion resistance (HLGR) and high level kanamycin resistance of resistant LAB are ignored. Most countries in Asia and (HLKR) with minimum inhibitory concentration (MIC) Africa lack proper guidelines on the judicious use of antibi- values >500 μg/mL (Murray 1990; Del Campo et al. 2000; otics and there is much use of low cost antibiotics in animal Donabedian et al. 2003; Jackson et al. 2004; Bismuth and husbandry that is not being monitored. The persistent use of Courvalin 2010). This bifunctional gene is highly prevalent aminoglycoside antibiotics such as apramycin, neomycin, among clinical strains of Staphylococcus and Enterococcus streptomycin in farms may co-select for antibiotic resistance spp. (Culebras and Martinez 1999), and its frequent spread in LAB and pathogenic species via the food chain among Gram-positive organisms has been attributed to its (Guardabassi et al. 2004). In such instances, antibiotics deliver lower G+C content (Byrne et al. 1989). Of late, the selective a competitive advantage, thereby triggering the acquisition advantage of this fused gene has been related to the structure and rapid spread of resistance genes via horizontal gene trans- and rigidity of the two encoded functional enzymes (Boehr fer (Nielsen et al. 2014). The hazards of acquired resistance et al. 2004). The monofunctional genes [aph(2″)Ib, aph(2″)Ic and its rampant spread in nosocomial enterococci is of major and aph(2″)Id] depicted lower MIC values (≤500 μg/mL) for concern (Kuhn et al. 2005; Hammerum et al. 2010). Such gentamicin, while aph(2″)Ie was observed with HLGR findings illustrate that there is a high risk of acquisition and (≥1024 μg/mL) in enterococci (Chow et al. 1997;Tsaietal. transfer of aminoglycoside resistance by LAB via the food 1998; Kao et al. 2000;Chenetal.2006). The aminoglycoside chain. Thus, extreme care should be taken to avoid the emer- resistance genes mentioned above are known to modify gence of aminoglycoside-resistant LAB, as they can be a po- 4,6 deoxystreptamines, especially clinically significant antibi- tent source of antibiotic resistance genes (Mathur and Singh otics such as amikacin, gentamicin, kanamycin and tobramycin 2005). As a result, protocols to monitor the development of (Chen et al. 2006; Bismuth and Courvalin 2010). Other aminoglycoside resistance among LAB from farm animals are resistance-conferring genes found in Gram-positive organisms required. are kanamycin modifying aph(3′)IIIa, streptomycin modifying From the above understanding of the risk related to amino- aad6, ant(6)Ia and spectinomycin modifying ant(9′)Ia, glycoside resistance and its spread via the food chain, an at- ant(9′)Ib (Bismuth and Courvalin 2010). A high-level strepto- tempt was made in the present study to evaluate the presence mycin resistance (HLSR) in enterococci, despite the absence of of aminoglycoside resistance in native LAB from farm and aad6orant(6)Ia genes has been explained due to a mutation in meat origin in the Mysore region of Karnataka, India. We the 30S ribosome (Simjee and Gill 1997). Therefore, high MIC report the widespread presence of the aminoglycoside resis- levels may not necessarily correlate with the presence of the tant bifunctional gene along with the kanamycin and strepto- above-mentioned resistance genes. mycin modifying genes in different native isolates of In the past decade, the rise and spread of aminoglycoside Enterococcus sp., Lactobacillus plantarum,andPediococcus resistance in Enterococcus sp. from domestic and other farm lolii. animals has been documented (Donabedian et al. 2003; Jackson et al. 2004, 2009, 2010; Ramos et al. 2012; Klibi et al. 2014). Enterococci from clinical settings and farm ani- Material and methods mals from the same region were positive for aminoglycoside resistance, and the genetic relatedness signified their rapid Media, antibiotics, chemicals and control strains spread among the human population (Donabedian et al. 2003). Earlier, Tenorio et al. (2001) described the emergence The Iso-sensitest broth was purchased from Thermo Fisher of aac(6′)Ie-aph(2″)Ia in Lactobacillus acidophilus, Scientific (Basingstoke, UK). de Mann, Rogosa and Sharpe Lactobacillus salivarus and Pediococcus acidilactici from fe- (MRS) medium and antibiotics such as amikacin, apramycin, cal samples of healthy pigs and pets, which is the only report gentamicin, kanamycin, neomycin, streptomycin and specti- of its kind to date to have described the gene in Lactobacillus nomycin were procured from Hi-Media Laboratories and Pediococcus sp. Documented studies on the occurrence of (Mumbai, India). Antibiotic powder was weighed as required aminoglycoside resistance in LAB from food origin have been and dissolved in water. The dNTPs mix, 25 mM MgCl2,ly- very
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