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Detection and characterization of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli isolated from retail raw foods and children with diarrhea in Khanh Hoa province, Vietnam

Le Quoc Phong 大阪府立大学 DOI:info:doi/10.24729/00017709

2022.07.05

概要

Antibiotics, the most important medical achievement in the last 50 years, are hailed as a miracle in modern medicine due to their ability in fighting bacterial infections, then saving lives. The first antibiotic, namely penicillin was found in 1928 (Fleming, 1929). Since then, various antibiotics or antimicrobials have been discovered, synthesized and deposited into the pharmaceutical market. As of September 1st, 2019, there are 50 existing antibiotics in the clinical pipeline (WHO, 2019a). These antibiotics were arranged into different classes such as aminoglycosides, carbapenems, cephalosporins, quinolones, glycopeptides, macrolides, monobactams, oxazolidinones, penicillins, polypeptides, rifamycins, sulfonamides, streptogramins, tetracyclines, polymyxins. However, many antibiotics are no longer effective to many pathogenic bacteria since the rise of antimicrobial resistance (AMR) (WHO, 2019b). AMR has become one of the greatest challenges in the 21st century. In recent years, AMR is a really major public health issue worldwide. It increased morbidity, mortality as well as healthcare costs due to longer hospitalization and multiple antimicrobial therapies needed (Bowe, 2014; Prestinaci et al., 2015). AMR currently causes at least 700.000 deaths yearly and was predicted to be able to result in 50 million deaths each year by 2050 unless effective actions are taken (WHO, 2019b). Furthermore, newly developed antibiotics were almost very few for a long period even though there is still a clear mismatch between the few newly approved antibiotics and the current priority pathogens list as published by the World Health Organization (WHO), especially for bacteria producing metallo-β-lactamases which can catalyze the hydrolysis of a broad range of β-lactam antibiotics including carbapenems (WHO, 2017b, 2019a). AMR occurs naturally, but the massive misuse of antimicrobials in human medicine is one of the leading factors in AMR development. Recently, the ongoing COVID-19 (Corona Virus Disease 2019 caused by SARS-CoV-2) pandemic has been causing a high number of patients hospitalized and some of them were admitted to intensive care units (ICU) with vulnerable for secondary infections, resulting in an increase use of antibiotics for COVID-19 patients in healthcare settings which might contribute to the misuse of antibiotics and foster the increase the AMR burden in many countries (Manohar et al., 2020). Besides, overuse and misuse of antimicrobials in veterinary medicine, livestock, and aquaculture in many countries including Vietnam have also contributed to the emergence and spread of AMR bacteria in different environments and various backbones (Pham-Duc et al., 2019; Shea, 2003). Bacteria in the animal gut can develop resistance to the used antibiotics and the resistant bacteria may transmit to humans via contact, consumption, or handling of contaminated animals or animal-originated foods. Therefore, food-producing animals and foods of animal origin could be served as sources and reservoirs for AMR bacteria (Le et al., 2015; Pérez-Rodríguez and Mercanoglu Taban, 2019).

Among the antibiotic groups in the pipeline, the carbapenems, cephalosporins, monobactams, and penicillins are subclasses of β-lactams characterizing with a β-lactam ring structure. β-lactam antibiotics target to interrupt the cell-wall synthesis of bacteria by disrupting peptidoglycan biosynthesis through covalent linking to penicillin-binding proteins (WHO, 2019a). β-lactams, one of the most vital groups of antimicrobials, are used popularly in human medicine. They have been extensively used in human medicine with approximately 50% of all prescribed antibiotics and account for 60% of all antimicrobial use by weight worldwide (Livermore and Woodford, 2006; Pitout, 2012; Rahman et al., 2018). Among antibiotics of the β-lactam group, cephalosporins (3rd, 4th and 5th generations) were classified as “Highest Priority” of antimicrobials categorized as “Critically Important” in The WHO List of Critically Important Antimicrobials for Human Medicine (WHO, 2017a). However, the resistance to these important antibiotics has been increasingly recognized worldwide, including Vietnam (Bergšpica et al., 2020; Le et al., 2015). There are different resistance mechanisms in Gram-negative bacteria against β-lactams. Among them, the production of β- lactamase was the most popular mechanism of resistance in Gram-negative bacteria. Currently, more than 500 different β-lactamases have been reported (Rahman et al., 2018). They are grouped into four classes including A, B, C, and D based on Ambler classification. Particularly, class B is zinc-metallo-β-lactamase, whereas classes A, C, and D are characterized β-lactamases having serine at the active site (Rahman et al., 2018). Among βlactamases, extended-spectrum β-lactamases (ESBLs) are specifically concerned due to their broad-spectrum activity to hydrolyze oxyimino cephalosporins (cephalosporin 3rd and 4th generations) and monobactams but excluding cephamycin (cefoxitin) and carbapenems (Rahman et al., 2018). Until now, various types of ESBLs have been reported. Out of them, TEM, SHV, and CTX-M enzymes are the most popular in Enterobacteriaceae (Arpin et al., 2009). Variants of TEM and SHV were predominant ESBLs during the 1990s, whereas CTXM type ESBLs have recently been becoming the most globally dominant genotypes (Adamski et al., 2015). To date, there have been more than 172 variants of CTX-M types that are clustered into 5 major groups based on their sequence homologies including CTX-M-1, -2, -8, -9, and -25 (Ramadan et al., 2019). Among variants in CTX-M groups, the CTX-M-14 (belong to CTX-M-9 group) and CTX-M-15 (belong to CTX-M-1 group) are the most common ESBL identified in clinical isolates worldwide (Lahlaoui et al., 2014). Consequently, the increase of ESBL-producers such as Enterobacteriaceae has rendered many important antimicrobials belonging to the β-lactam group, even the latest cephalosporins, ineffective. Especially, those bacteria cause hard-to-treat or even untreatable infections with exiting antimicrobials are posing great threats to public health and changing the landscape of healthcare. Worryingly, ESBL-producing bacteria such as Enterobacteriaceae or the ESBL genes themselves, might be transmitted to humans via various reservoirs such as livestock, companioned animals, wild animals, sewage water, intercontinental travel, etc. (Fig. I) (Woerther et al., 2013).

In a context of increasing AMR problem with the popular of multidrug-resistant (MDR) bacteria especially carbapenemase-producing pathogens as well as the absence of newly developed antimicrobials against these “superbugs” and because of limited therapeutic options with antimicrobials in the current pipeline, the polymyxins colistin has been reintroduced as a last-line antibiotic despite their toxicity and uncertain dosing (Andrade et al., 2020; WHO, 2017a). The mechanism of colistin against Gram-negative bacteria is through binding to the lipid A – a key component of lipopolysaccharide (LPS) of the outer membrane, resulting in the leaking of cell contents, and subsequently, cell death (Dijkmans et al., 2015). This antibiotic was first discovered in 1949 in Japan from the Bacillus polymyxa and was available for clinical use in 1959 (Reed et al., 2001). However, colistin had gradually been less used or even abandoned in human medicine worldwide since the early 1980s due to its severe side effects as nephrotoxicity (Brown et al., 1970). Meanwhile, in veterinary medicine, colistin has been used for decades for both prophylactic purpose and treatment of infections. For example, colistin was widely used in pig production to treat diarrhea caused by E. coli or used as a growth promoter in the poultry industry (Kempf et al., 2016; Shen et al., 2016). Unfortunately, the intensive use of colistin in agricultural production and veterinary medicine might contribute to the emergence of colistin resistance. Before 2015, the mechanism of colistin resistance was mainly assigned to chromosomal-mediated genes such as phoPQ, pmrAB, and mgrB (Olaitan et al., 2014). However, in 2015, a plasmid-mediated colistin resistance gene, namely mobile colistin resistance (mcr)-1, was first described in E. coli from livestock and patients in China (Liu et al., 2016). After that, different variants from mcr-1 to mcr-10 have been reported consecutively (Wang et al., 2020). The colistin resistance mechanism of mcr genes is as target modification of colistin. The mcr gene encodes phosphoethanolamine (PEA)-lipid A transferase that transfer PEA to the lipid A creating an altered lipid A of the outer membrane of Gram-negative bacteria that lowers the affinity of colistin, then reduces activity of this antibiotic (Fig. II) (Aghapour et al., 2019; Hinchliffe et al., 2017). Since discovery of mcr gene, colistin resistance brought strong attention to scientific society because the mcr-1 gene was plasmid-mediated and possible to horizontally transfer between bacteria and even from animals to humans (Luo et al., 2020; MalhotraKumar et al., 2016). To date, ten variants of mcr genes (mcr-1 to mcr-10) have been reported worldwide in various bacterial species and different sources such as animals, foods, the environment and humans (Hussein et al., 2021). The wide dissemination of mcr genes might pose a great threat to public health due to their threatening to the clinical use of colistin, the last-line antibiotic for severe infections caused by MDR bacteria (Luo et al., 2020).

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