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Characteristics of Escherichia coli isolated from livestock and related materials in the Philippines

BELOTINDOS, Lawrence Pascual 北海道大学

2021.09.24

概要

Antimicrobial resistance (AMR) is defined as the ability of microbes, such as bacteria, viruses, parasites or fungi to grow despite the presence of antimicrobials that would normally kill them. The development of drug resistance can be due to the inherent resistant characteristics of microorganisms or through the acquisition of genes from other organisms that can be passed both horizontally and vertically to their progeny [1]. However, AMR development was aggravated by many human factors largely through the misuse and abuse of antibiotics leading to the loss of antimicrobial efficacy and the spread of drug resistant pathogens in the community [2].

AMR is a serious concern in public and animal health, and the emergence of multipleantibiotic-resistant bacteria constitutes a global problem that needs to be addressed [3]. Livestock are considered as one of the major natural reservoirs for AMR. Antimicrobialresistant microorganisms in livestock may transfer their AMR genes to humans microflora via food animals and environmental contact [4] [5–7]. Additionally, foodborne diseases associated with food-producing animals are an important issue in developing countries where poor sanitation is maintained during collection and processing [8,9] and empirical treatment were common that could promote AMR development.

Major foodborne pathogens of great concern around the globe that causes outbreaks were Salmonella, Campylobacter and Escherichia coli [10]. According to WHO report, the estimated burden of foodborne diseases caused by 31 agents (bacteria, viruses, parasites, toxins and chemicals) each year was as many as 600 million, or almost 1 in 10 people in the world, fall ill after consuming contaminated food. Of these, 420,000 people die, including 125,000 children under the age of 5 years. The South-East Asia Region has the second highest burden of foodborne diseases per population, after the African Region. However, in terms of absolute numbers, more people fall ill and die from foodborne diseases every year than in any other WHO Region, with more than 150 million cases and 175,000 deaths in a year [4].

Documented foodborne disease outbreaks in the Philippines were caused by Salmonella, Vibrio, Aeromonas and E. coli. The top three food vehicles were meat-based dishes and processed meat products, fish and other sea dishes and bakery and confectionary products. According to the study, majority of morbidity cases were shown to be mainly outbreaks occurring outside the home, particularly in workplaces and schools [11]. Major contributory factors to the occurrence of outbreaks were improper storage temperature and poor hygienic practices [12]. In total, 115 food and water borne outbreaks were reported and verified from 2012-2016. During this period, a total of 17,246 cases and 143 deaths were reported [13].

In 2017, the WHO published a list of leading global pathogens and their antimicrobial resistance [14]. The resistance of leading global pathogens to quinolones were among the top priorities. Quinolones are considered a first choice in the treatment of intestinal bacterial infections in humans and animals. They were developed in the 1960s and 1980s. They were completely synthetic compound and has a bactericidal effect on most Enterobacteriaceae [15,16]. Nalidixic acid is one of the first-generation quinolones and effective against urinary tract infections [16]. Ciprofloxacin, norfloxacin, oxofloxacin, pefloxacin, and enrofloxacin belong to the second generation (fluoroquinolones), showing greater potency and a broader spectrum [23,24]. They are particularly effective against Gram-negative bacteria and several Gram-posibtive and intracellular bacteria. Fluoroquinolones had an additional fluorine atom at the C-6 position and a piperazinyl or related ring at the position C-7 on the quinolone molecule [16,17]. Soon after quinolone introduction, resistant isolates emerged, which seems unlikely because it is a fully synthetic drug [15,16]. Then, resistance towards quinolones has become widespread among Enterobacteriaceae in the decades, hampering its effectiveness towards stubborn bacterial pathogens [18].

Quinolones primarily inhibit the action of type II topoisomerases including DNA gyrase and topoisomerase IV. Type II topoisomerases are enzymes that mediate the relaxedsupercoiled and catenated-decatenated DNA and are crucial for several DNA-associated processes, such as replication and transcription [19]. DNA gyrase and topoisomerase IV are both heterotetrameric enzymes composed of two pairs of identical subunits, GyrA2GyrB2 and ParC2ParE2, respectively [20]. DNA gyrase was the primary target for Gram-negative bacteria, whereas topoisomerase IV in the Gram-positives bacteria [21]. Quinolones have been shown to bind to the DNA gyrase/topoisomerase IV–DNA complex. The intercalation of quinolone into DNA gyrase/topoisomerase IV-DNA complex is responsible for the inhibition of DNA replication and transcription, caused double-strand break [19,22].

Currently, the acquisition of quinolone resistance was associated with chromosomal mutations that alter the target sites and alter membrane permeability that reduced drug accumulation by efflux/influx pumps. Another quinolone resistance mechanism is by acquiring plasmid-mediated quinolone resistance (PMQR) genes [20].

Specific point mutations in DNA gyrase and topoisomerase IV, mostly confer highlevel resistance are often found in a region termed the quinolone resistance determining region (QRDR) [19,20]. Mutations in the QRDRs of these genes result in amino acid substitutions that architecturally altered the target protein, and subsequently, the drug-binding affinity of the enzyme. Mutations in QRDRs of GyrA and ParC are commonly found and less frequent in those of GyrB and ParE [23]. Resistance-conferring mutations outside the traditional QRDR have also been identified [19].

Recently, PMQR genes have been identified as an emerging clinical problem that usually leads to low-level resistance [19,20,23]. Currently, there are three clinically relevant genes related to plasmid-mediated quinolone resistance: (i) qnr, which encodes proteins belonging to the pentapeptide repeat proteins that protect target site; (ii) aac(6′)-Ib-cr, acetylates the unsubstituted nitrogen of the C7 piperazine ring of norfloxacin and ciprofloxacin, which decreases drug activity; (iii) qepA and oqxAB, which mediates antibiotic efflux. Nonetheless, many PMQR determinants have been identify recently since the first PMQR was discover.

As with the 2019 Philippine AMR surveillance program report, clinical E. coli rates of resistance against fluoroquinolones and third generation cephalosporins have been increasing for the past 10 years [24]. The resistance rates against ciprofloxacin was 41.3% to 46.6% and ceftriaxone was 24.2% to 39.9%. Emerging resistance to carbapenem was also reported in 2019 with resistance rates of 1.1% to 6.4% for meropenem and slight decrease in imipenem from 10.6% to 6.0%, but not statically significant. Of all E. coli tested for extended-spectrum β – lactamase (ESBL) production, 53.2% were positive. Salmonella enterica serovar Typhi isolates have remained susceptible to first line antibiotics. Resistance rates of S. Typhi against ampicillin, co-trimoxazole, ceftriaxone and chloramphenicol still remained at less than 5% for the past 10 years. There has been an increase in resistance in S. Typhi to ciprofloxacin for the past two years, although not statistically significant. In non-typhoidal Salmonella, increasing resistance to levofloxacin was noted with resistance rates of 20.9%, which was higher than the rate of 5% reported in 2018 [24]. The resistance of non-typhoidal Salmonella against ciprofloxacin was seen to be decreasing from 14.3% to 9.8%. Among the confirmed non-typhoidal Salmonella, the most common identified were S. enterica serovar Typhimurium and S. enterica serovar Enteritidis, which were also the most common for the past five years. All of these data were mainly obtained through the antimicrobial resistance surveillance and monitoring system of Research Institute for Tropical Medicine of the Department of Health, the Philippines.

Unlike in human health sector, AMR surveillance system in animal health sector in the Philippines is still under development. The AMR surveillance system on animal health sector will prioritized zoonotic pathogen species (Salmonella spp.., and Campylobacter spp.) and commensal bacteria (E. coli and Enterococcus spp.). According to Philippine Action Plan to Combat AMR 2019-2023, it is reported that limited studies were conducted in AMR related to livestock animals [25–30]. Surveillance of AMR within the entire agricultural sector is not yet unified, as some organizations conduct their own surveillance activities. Moreover, researches were difficult to access, and data were not yet disseminated to inform/share to both animal and human health stakeholders [2].

Likewise, the detection of quinolone/fluoroquinolone-resistant bacteria has been increasing in animal and their food products in the Philippines. For instance, the prevalence rates of nalidixic acid and ciprofloxacin resistance in strains isolated from food-producing animals and their food products were found from 10% to 97.5% and 5% to 88.4%, respectively [25,27,30–32]. In environmental samples from soil and agricultural irrigation water, the detected resistance rate against nalidixic acid and ciprofloxacin was up to 35.4% and 6.8%, respectively [28,29]. Previous studies focused on the phenotypic characterization of the resistance determinants of bacteria to some extent. However, those studies mostly scrutinized the ESBL resistance mechanism of bacteria [31,32].

Despite on molecular research advancement, study on genetic diversity and antimicrobial resistance genes (ARGs) profile of foodborne bacterial isolates was still limited in the Philippines. Molecular data on foodborne bacteria can provide better epidemiological view for tracing foodborne infection. Hence, I carried out a research including surveillance and characterization of antimicrobial resistant E. coli in the Philippines. This thesis aimed to provide overview of the AMR status in food-producing animals and animal-derived food and clonal distribution of quinolone non-susceptible E. coli in the Philippines. In addition, the generated molecular data on this study would fill up the AMR information/data gap in animal health sector in the Philippines. In chapter I, the prevalence of E. coli and quinolone resistant determinant were studied from various food-producing animals and animal-derived food. In chapter II, characterization of plasmids among qnr-harboring isolates were further investigated.

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