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Microbiology (Medical)

Role of plasmids in antibiotic resistance in clinical infections and implications for epidemiological surveillance: a review

Ayodele Oluwaseun Ajayia Faculty of Science, Department of Microbiology, Federal University, Oye-Ekiti, NigeriaCorrespondence[email protected]
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Olajide Joseph Akinjogunlab Faculty of Science, Department of Microbiology, University of Uyo, Uyo, NigeriaView further author information
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Adebowale Toba Odeyemic Landmark University SDG 2 and 3, Landmark University, Omu Aran, NigeriaORCID Iconhttps://orcid.org/0000-0002-8524-464XView further author information
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Akinyomade Oladipo Owolabid Department of Microbiology, Landmark University SDG 3: Good Health and Wellbeing, Omu-Aran, NigeriaView further author information
Article: 2350414 | Received 19 Sep 2023, Accepted 22 Apr 2024, Published online: 06 Jun 2024

Abstract

The global upsurge in antibiotic resistant bacteria (ARB) is putting immense pressure on healthcare. The spreading of antimicrobial resistance is facilitated by mobile genetic elements, most especially plasmids. The widespread use of antibiotics in clinical and veterinary environments creates selective pressure that drives the evolution of ARB. Plasmids contribute to the propagation of AR in different types of clinical infections. The role plasmids play in this evolution necessitates their utilization in molecular surveillance to detect the emergence of ARB and track the spread of AR plasmids. Recent technologies like replicon typing and whole genome sequencing (WGS) have become the gold standard for molecular epidemiology of plasmids for the detection and control of epidemics in clinical settings. Unfortunately, access to such technologies is limited in low- and middle-income countries (LMICs). The major aim of this review is to examine the specific contributions of plasmids to the upsurge of AR in clinical settings and elucidate the various replicon types that have been attributed to specific antibiotic-resistant infections in healthcare settings. Healthcare in LMICs should be supported to build capacity in WGS and molecular surveillance to effectively prevent and control AR bacterial infections.

Introduction

Plasmids are extrachromosomal genetic entities that are capable of independent replication and mostly found among bacteria (Shintani et al. Citation2015; Hernandez et al. Citation2022; Dewan and Uecker Citation2023). They thrive among bacteria in different environments, including water, land, and human and animal microbiomes (Alawi et al. Citation2022). They are generally smaller in size, compared to the vast majority of bacterial chromosomes, with some being circular in shape while others are linear in orientation. Most of the knowledge acquired in microbial genetics was obtained through the careful study of plasmids from different organisms and ecosystems (Galata et al. Citation2019; Helinski Citation2022).

Plasmids have been attributed to wide array of biological characteristics in microorganisms where they are located (Wein and Dagan Citation2020). This is due to their ability to mobilize accessory and functional genes that confer specific attributes on bacteria (Wein and Dagan Citation2020). These attributes often reflect the various environments where the organisms thrive (Finks and Martiny Citation2023). Although plasmids are not considered as an essential feature among bacteria and other organisms that carry them, they often confer some competitive advantages that enable them to thrive within their respective environments. They also play a major role in evolution due to their ability to mobilize accessory genes by horizontal gene transfer (HGT) (Rodríguez-Beltrán et al. Citation2021). Plasmids replicate extensively and are exchanged between bacterial populations, making them genetic entities that serve as vehicles for the transfer of biological attributes across different populations (Wein and Dagan Citation2020).

Such attributes associated with plasmids in aquatic environments include antimicrobial (AR) resistance and tolerance of environmental pollutants (Segura et al. Citation2014; Alawi et al. Citation2022). In terrestrial environments, the plasmid-encoded attributes include AR, resistance to chemical and industrial pollutants, synergistic associations among bacteria in the soil, and production of numerous secondary metabolites that can be harnessed for various uses (Meng et al. Citation2022). Plasmids have also been found to carry genes that confer resistance to chemical and industrial pollutants found in the soil and also enhance their degradation (Garbisu et al. Citation2017). Plasmids may also carry genes that are responsible for removal of xenobiotics from environments where the bacteria are found, and plasmid-mediated spread of such genes can occur within these environments (Bhatt et al. Citation2021).

In addition, plasmids have also been found among bacteria in clinical and healthcare settings where they carry genes involved in antibiotic resistance (San Millan Citation2018; Kammili et al. Citation2020). Antibiotic resistance is a very serious phenomenon currently causing problems within healthcare systems globally, especially in low- and middle-income countries (LMICs), with attendant increases in the prevalence of infectious diseases, treatment failures, increased hospital stays and an overall increase in the cost of healthcare across the world (Friedman et al. Citation2016; Van Hecke et al. Citation2017). Therefore, the aim of this review is to examine the specific contributions of plasmids to the upsurge of antibiotic resistance in core clinical settings and elucidate the various replicon types or incompatibility groups that have been attributed to specific antibiotic-resistant infections in healthcare settings. This article also gives specific recommendations on possible mitigation measures that can be adopted to reduce the problem of plasmid-mediated antibiotic resistance in healthcare settings, especially in low resource countries.

Plasmids in clinical infections

Plasmid-mediated antibiotic resistance in urinary tract infections (UTIs)

The most serious concern about plasmids in clinical settings appears to be their role in clinical infections which is linked to their ability to spread AR and virulence determinants in both human, animal and clinical settings. A study by Zhou et al. (Citation2021), confirmed the spread of antibiotic resistance in a clinical setting through plasmids. Another similar study linked the outbreak of carbapenemase-producing P. aeruginosa to the presence of plasmids in a clinical setting (Peter et al. Citation2020). Plasmids have been linked with virulence and resistance to different antibiotics among bacterial pathogens implicated in urinary tract infections (UTIs), skin and soft tissue infections (SSTIs), bloodstream infections (BSIs), upper and lower respiratory tract infections (ULRTIs), etc. However, UTIs appear to be the most common infection in healthcare settings, and the role of plasmids in the carriage and spread of antibiotic resistance has been noted (Vorland et al. Citation1985).

According to studies by Ranjan et al. (Citation2021) and Mukherjee and Mukherjee (Citation2019), plasmids that caused resistance to multiple antibiotics were found among bacterial uropathogens within clinical settings. The introduction of whole genome sequencing (WGS) methods have facilitated the characterization and detection of plasmids among bacterial urobiota, and such studies have confirmed that plasmids confer significant traits on bacterial urobiota, including virulence traits and antibiotic resistance (Montelongo Hernandez et al. Citation2021). It has been established that the Gram-negative bacteria occur more frequently than Gram-positive bacteria in UTIs, and Escherichia coli is the most common bacterial uropathogen (Regasa Dadi et al. Citation2018; Bunduki et al. Citation2021; Thangavelu et al. Citation2022). The E. coli is noted for the carriage of specific antibiotic resistance plasmids among other bacterial species recovered from UTIs in clinical settings (Rabbee et al. Citation2016; Thapa Shrestha et al. Citation2020). Although some antibiotic resistance determinants are coded by chromosomes, the bulk of acquired resistance to antibiotics in UTI and other infections in clinical settings are mediated by plasmids (Harris et al. Citation2023). The most common resistance mechanism mediated by plasmids among Gram-negative uropathogens is the extended spectrum beta lactamase (ESBL) production in UTIs and other clinical infections (Thangavelu et al. Citation2022). This is the primary enzyme for the deactivation of penicillins and third-generation cephalosporins. Mahmud et al. (Citation2022), confirmed the use of whole genome sequencing of plasmids carrying ESBL genes to map their presence and confirm their spread in a clinical environment. Another major problem in the management and treatment of UTIs in healthcare settings is the predominance and spread of multidrug-resistant (MDR) strains of Gram-negative uropathogens, which has also been attributed to antibiotic resistance plasmids (Rabbee et al. Citation2016; Thapa Shrestha et al. Citation2020). In a study by (Kammili et al. Citation2020), Gram-negative bacterial pathogens, especially E. coli and Klebsiella pneumoniae were common among women with UTIs and they carried plasmids that conferred resistance to multiple antibiotics. The plasmid-borne antibiotic resistance genes found among the bacteria include ESBL-encoding genes (blaTEM, blaSHV, blaCTX-M) and PMQR genes (qnrA, qnrB, qnrD, qnrS, aac (6’)-Ib-cr). In addition to the specific contributions of uropathogens like E. coli and K. pnumoniae to UTIs, plasmids are also found in other broader range of bacteria which include Proteus mirabilis, Staphylococus aureus (Mores et al. Citation2021; Iheanacho and Antai Citation2023). Plasmids have also been found in the urinary microbiota, where they improve the fitness of the urinary microbiota and contribute to the overall health of the urinary tract (Johnson et al. Citation2022). Some studies in Nigeria have confirmed that the presence of resistance to antibiotics among E. coli and other Gram-negative bacteria are associated with plasmids and most of the bacteria showed resistance to multiple antibiotics (Onwuezobe and Orok Citation2015; Iheanacho and Antai 2023). Some antibiotics to which some uropathogens have shown reduced susceptibility due to the presence of plasmids include tetracycline, streptomycin, sulfhonamides, and quinolones (Bunduki et al. Citation2021).

Plasmid-mediated antibiotic resistance in respiratory tract infections (RTIs)

Compared with UTIs, there are fewer confirmed incidences of plasmid-borne antibiotic resistance among bacterial pathogens that cause RTIs. The most common bacterial pathogens implicated in respiratory tract infections are Streptococcus pneumoniae, Haemophilus influenzae, K. pneumoniae and E. coli (Gong et al. Citation2020). Penicillin and third-generation cephalosporins have been the drugs of choice for the treatment of bacterial respiratory tract infections. However, the use of carbapenems has become more prominent in the past decade (Yang et al. Citation2022; Liu et al. Citation2023). The extensive use of these antibiotics for treatment and prevention of RTIs has led to a surge in bacterial pathogens with reduced susceptibility to these drugs, especially the third-generation cephalosporins and newer generation carbapenems (Thonda et al. Citation2021). Most cases of antibiotic resistance among bacteria recovered in RTIs have also been linked with the plasmids that carry some of the genes that confer the resistance (Guitor and Wright Citation2018). Acinetobacter baumanii, commonly found on respiratory devices in intensive care units (ICUs) carry plasmids that mediate resistance against third-generation cephalospirins, carbapenems and colistin (Patwardhan et al. Citation2008; Hameed et al. Citation2019). A similar study in China reported the presence of two plasmid-borne New Delhi metallo-beta-lactamase genes among K. pneumoniae recovered from patients with RTIs (Y. Liu et al. Citation2019). Another study in China screened 156 ventilated patients and reported infection caused by K. pneumoniae, A. baumanii and P. aeruginosa. The bacteria carried plasmids that spread of ESBLs within the clinical setting (Wang et al. Citation2018). Majewski et al. (Citation2021) reported plasmid-mediated colistin resistance in a clinical setting in Poland. Instances of plasmid-mediated carbepenem resistance among different categories of patients including the critically ill have been reported (Schweizer et al. Citation2019). Plasmids are also responsible for resistance to multiple antibiotics, especially carbapenems and colistin, in pets and such plasmids were found to carry carbapenemases and mcr genes that can be transmitted to humans (Khalifa et al. Citation2020; Liu et al. Citation2022). The emergence of plasmid-borne resistance to colistin and carbapenems poses a more serious concern in core healthcare settings due to the critical importance of such antibiotics for last resort use in respiratory wards and intensive care units (ICUs). There are reports that the mcr genes variants are increasingly carried by plasmids with increased transmissibility within intensive care units (ICUs) (Liu et al., Citation2023b). Fluoroquinolones are also drugs of choice for treatment of RTIs and genes that code for resistance to these classes of antibiotics are carried by plasmids (Alvi et al. Citation2018). In Nigeria, plasmid-borne AmpC beta-lactamase was found among K. pneumoniae strains recovered from the sputum of patients with lower respiratory tract infections in a hospital complex (Thonda et al. Citation2021). Furthermore, the presence of resistance genes on plasmids and other mobile genetic elements raises the risk of the transmission of antibiotic resistant bacterial pathogens, as confirmed by an index case of respiratory tract infection contaminating a whole hospital ward with plasmid-borne antibiotic resistant bacteria (Gerding et al. Citation1979). The genomic characterization of some plasmid-carrying bacterial pathogens recovered from respiratory tract infections has provided more insight into the structure and characteristics of plasmids responsible for antibiotic resistance and such genomic studies are currently gaining attention to elucidate the genetic context, replicon, resistance genes and dynamics of spread of such antibiotic resistance plasmids in clinical environments (Moglad et al. Citation2022).

Plasmid-mediated antibiotic resistance in bloodstream infections (BSIs)

Plasmids are also involved in antibiotic resistance and virulence among bacteria isolated from bloodstream infections in different clinical settings (Corkill et al. Citation2005; Abbassi et al. Citation2008; Ahmed et al. Citation2021). The fluoroquinolones are common antibiotics for the treatment of BSIs, partly due to the enhanced pharmacokinetics of this family of antibiotics. Resistance to fluoroquinolones among bacteria causing BSIs has been on the increase, and some of these bacteria carry plasmids that contain genes that confer resistance to fluoroquinolones (Abd ElSalam et al. Citation2018). Septicamia is a serious problem among children and neonates in developing countries, and bacteria responsible for infection carried plasmids that conferred resistance to multiple antibiotics, according to a clinical report from Nigeria (AbdulAziz et al. Citation2017). Similarly, the E. coli and K. pneumoniae recovered from bloodstream infections among pediatric patients carried plasmids with genes that encode ESBLs and carbapenemases. The carbapenems are drugs of last resort for treatment of BSIs and reports have also indicated that resistance to carbapenems has emerged and that blaNDM genes that encode carbapenemases are mostly found on plasmids in bacteria (Abouelfetouh et al. Citation2020; Ahmed et al. Citation2021; Shi et al. Citation2022). Acinetobacter baumanii is emerging as a leading bacterial pathogen in healthcare-associated BSIs. The large genome of this pathogen has been considered as one of its pathogenic adaptations, and most strains of this bacterium carry plasmids that code for ESBLs, carbapenemases, and virulence determinants (Abouelfetouh et al. Citation2020). Klebsiella pneumoniae has also emerged as the most common bacterial pathogen in BSIs and the hypermucoidity of this bacterium has been attributed to plasmids that carry multiple genes, which also code for resistance to cephalosporins and carbapenems (Ramirez et al. Citation2014; Ahmed et al. Citation2021). This is closely followed by E. coli as a common agent of BSIs (Akova Citation2016; Goswami et al. Citation2020). Among E. coli strains found in BSIs, plasmids were found that contain the blaCTX-M, blaTEM and the ampC β lactamase genes. The plasmids also encode resistance to other antibiotic classes including fluoroquinolones, chloramphenicol, tetracyclines etc. (Ibrahim et al. Citation2023). The genetic analysis of some K. pneumoniae strains revealed that the EBSI036 strain carried 20 antibiotic resistance genes and was identified as a CR-HvKP strain: it harbored four plasmids, namely, pEBSI036-1-NDM-VIR, pEBSI036-2-KPC, pEBSI036-3, and pEBSI036-4. The two carbapenemase genes blaNDM-1 and blaKPC-2 were located on plasmids pEBSI036-1-NDM-VIR and pEBSI036-2-KPC, respectively. The IncFIB:IncHI1B hybrid plasmid pEBSI036-1-NDM-VIR also carried some virulence factors, including the regulator of the mucoid phenotype (rmpA), the regulator of mucoid phenotype 2 (rmpA2), and aerobactin (iucABCD and iutA) (Ahmed et al. Citation2021). Whole genome sequencing (WGS) and the pulsed field gel electrophoresis have been employed to study plasmids among bacteria in bloodstream infections, and a study by Ai et al. (Citation2021) revealed that the p1575-1 plasmid was conjugative and possessed the rare coexistence of bla SFO-1, bla NDM-1, mcr-9 genes and a complete conjugative system. The plasmids in bloodstream and other healthcare infections have proven to be extremely versatile so that a single plasmid can code for resistance to multiple antibiotics including third-generation cephalosporins, aminoglycosides, tetracyclines, sulfonamides and trimethoprim (Akova Citation2016). Typhoid fever is an endemic bacterial disease in Nigeria and Africa, with Salmonella ser. Typhi as the leading bacterial pathogen. Occasionally, this bacterium has also been recovered from BSIs and recent report in Nigeria revealed that Salmonella strains carry plasmids with genes that encode for resistance to fluoroquinolones, which are the first line of treatment for most infections caused by Salmonella (Ikhimiukor et al. Citation2022). A similar study revealed that certain Salmonella typhi strains carried plasmids with genes that encoded resistance to chloramphenicol, trimethoprim, and ampicillin resistance, and further identified as chloramphenicol acetyltransferase type I, dihydrofolate reductase type VII, and TEM-1 β-lactamase, respectively (Shanahan et al. Citation1998). In another study in Ghana, S. typhi strains recovered from BSIs were found to contain resistance genes that were found on conjugative plasmids (Mills-Robertson et al. Citation2003). A novel bacterial pathogen Corynebacterium resistens has been detected among immunocompromised patients and WGS carried out on the organisms revealed that it carried a 28,312-bp plasmid pJA144188 that carries tetW gene that codes for resistance to tetracycline (Schröder et al. Citation2012). Another novel bacterial pathogen Pseudocitrobacter faecalis was recovered from a patient with BSI in China and the bacteria was found to carry a 55,148-bp-long IncX3 type plasmid that carried blaOXA-181 and qnrS1 genes which code for resistance to carbapenems and fluoroquinolones respectively (Shi et al. Citation2022). P. aeruginosa is another less common bacterial pathogen and also contains plasmids that confer resistance to multiple antibiotics (Igumbor et al. Citation2000).

Plasmid-mediated antibiotic resistance in skin and soft tissue infections (SSTIs)

Skin and soft tissue infections (SSTIs) within healthcare settings also have the involvement of plasmids as contributory factors to virulence and antibiotic resistance among bacterial pathogens implicated in such infections (Beige et al. Citation2014; Goel et al. Citation2023). The most common bacterial pathogens in SSTIs include methicillin-resistant S. aureus, P. aeruginosa, A. baumanii and K. pneumoniae (Bergogne-Bérézin and Joly-Guillou Citation1991; Halem et al. Citation2006). Other rare organisms include the Mycobacteria, Cutibacterium spp. and ESBL-producing E. coli (Buchanan et al. Citation2014; Uzunović et al. Citation2015; Hendrix et al. Citation2021; Koizumi et al. Citation2023). Surgical wounds and burns are some of the risks that predispose individuals to SSTIs and the various routine surgical procedures in most healthcare settings require the use of antibiotics for the prevention of pre- and post-surgical infections in core clinical settings (Alsaeed et al. Citation2022; Goel et al. Citation2023; Seidelman et al. Citation2023). SSTIs are also a risk factor for bloodstream infection (Kaliyeva et al. Citation2022). According to a study by Beige et al. (Citation2014), several Gram-negative bacteria were recovered from patients with wounds, and the organisms carried plasmids that likely conferred resistance to ceftazidime and amikacin. Some antibiotic resistance determinants like blaZ, erm(A), erm(C), msr(A), mph(C), aacA-aphD, aadD were detected among plasmids (Schiller et al. Citation1983). Serwold-Davis and Groman (Citation1986) screened some erythromycin resistant and sensitive Corynebacterium spp. found on skin samples and found that most of the erythromycin-resistant Corynebacteria carried plasmids. It has been noted that the incidence of plasmid-borne of ESBL and carbapenemase producing A. paumanii in SSTIs is attaining an increasing trend in clinical settings (Ramirez et al. Citation2014).

Plasmid-mediated antibiotic resistance among diarrhea pathogens

Diarrhea and other related gastrointestinal infections remain a global priority due to the huge economic burden in morbidity and mortality, especially in LMICs (Ingle et al. Citation2018; Alhaji et al. Citation2022). It is a major problem among children under five years, and this has been considered one of the core health indices over the past decades (Uma et al. Citation2009; Yah et al. Citation2010; Afum et al. Citation2022). In commensal bacteria, plasmids have been discovered that carry antibiotic resistance genes including blaCTX-M1, blaTEM, blaCMY-2, tetA, tetB, sul1, sulII, ipaH, est, elt and aggR (Tawfick et al. Citation2022). Various bacterial pathogens that are commonly isolated from patients with diarrhea include E. coli, V. cholerae, Salmonella spp. and Shigella spp as the common ones considered the core diarrheagenic bacteria (Alhaji et al. Citation2022). Although different groups of pathogens, including viruses, Entamoeba histolytica have been linked with diarrhea and gastrointestinal tract infections, bacteria are the most common group of pathogens. This has necessitated the use of antibiotics like ampicillin, gentamicin, erythromycin, co-trimoxazole and other related antibacterial agents for the treatment of most cases of diarrhea (Tribble Citation2017; Rhee et al. Citation2019). Unfortunately, the increase in the prevalence of diarrhea in LMICs has been attributed to antibiotic resistant pathogens (Lima et al. Citation1997; Falbo et al. Citation1999; Dimitriu Citation2022). Many bacteria confirmed in diarrhea cases carry plasmids with genes that code for specific resistance determinants (Bakkeren et al. Citation2021; Kessler et al. Citation2023). According to Adekunle and Onilude (Citation2015), some Campylocacter spp carrying plasmids were recovered from selected cases of diarrhea among infants in Osun State, Nigeria. Similarly, some diarrheagenic strains of K. pneumoniae isolated from stools in Nigeria were found to carry plasmids containing the astA and senB genes (Ogbolu et al., n.d.). Another major concern is the global rise in cases of colistin resistance among bacterial pathogens causing diarrhea, and some plasmids carry the mcr gene series that inactivates colistin (Li et al. Citation2021; Binsker et al. Citation2022). E. coli and Klebsiella spp. have emerged as the most common bacterial pathogens in diarrhea, a vast majority of which produce ESBLs that are mostly coded by plasmids carrying ESBL genes (Bush and Bradford Citation2020; Dela et al. Citation2022). The incidence of multiple drug resistance is a common phenomenon and this has been attributed to the ability of some of these plasmids to carry multiple genes that code for resistance to antibiotics in E. coli, K. pneumoniae, Salmonella spp. and Shigella spp. (Lima et al. Citation1997; Chigor et al. Citation2010; Suh Yah Citation2010). In addition, some bacteria like Salmonella, Shigella and E. coli can also carry multiple plasmids, which further enhances the spread of antibiotic resistance determinants (Adeleye and Adetosoye Citation1993). Strains of V. cholera that showed resistance to tetracycline, streptomycin, spectinomycin and trimethoprim were found to harbor conjugative plasmids (Falbo et al. Citation1999). In Bangladesh, a study by Iqbal et al. (Citation2014) confirmed that strains of Shigella spp carried plasmids harboring the sul2 gene that confer resistance to sulfamethoxazole – a common antibiotic for the treatment of diarrhea. The vast majority of plasmids carrying antibiotic resistance genes in diarrhea and other types of infections are conjugative, and such plasmids spread antibiotic resistance genes by HGT (McInnes et al. Citation2020; Liu et al. Citation2023).

Horizontal gene transfer in transfer of antibiotic resistance genes

The major mechanism of transfer of antibiotic resistance genes within clinical environments is the horizontal gene transfer (Lerminiaux and Cameron Citation2019). It is also the primary mechanism through which bacteria that coexist in the same environment exchange genetic entities among themselves to improve their fitness and adaptability to their respective hosts (Pilla et al. Citation2017). The plasmids, however, are components of a broader family of mobile genetic elements which include insertion sequences, transposons, transposable elements gene cassettes and bacteriophages, and these elements equally play some role in the emergence of antibiotic resistant bacteria and dissemination of antibiotic resistance genes (Partridge et al. Citation2018).

Horizontal gene transfer is an intensive biological process in clinical infections and hospital environments that facilitates the transfer of plasmids and other mobile genetic elements (Partridge et al. Citation2018). The type of resistance mediated by plasmids is called acquired resistance, which is different from intrinsic resistance that is chromosomally mediated and not transferable (Munita and Arias Citation2016). The major processes of horizontal gene transfer are conjugation, transduction and transformation (Partridge et al. Citation2018). However, the most pronounced molecular process of horizontal gene transfer is conjugation while the role of the other processes in the transfer of antibiotic resistance genes in clinical settings is less pronounced (Lerminiaux and Cameron Citation2019). Conjugation is the transfer of plasmids and other mobile genetic elements through close contact especially among related bacteria. Transformation is the uptake of genetic entities directly from the environment while transduction is the transfer of genetic elements through the agency of bacteriophages (Lerminiaux and Cameron Citation2019). These biological processes cumulatively promote the transfer of antibiotic resistance genes and spread of infection in clinical environments.

There is increasing scientific and genomic evidence of horizontal gene transfer of antibiotic resistance genes carried on plasmids in different healthcare settings. A study by Evans et al. (Citation2020) revealed that plasmid-borne multidrug resistance genes were transferred across different patients in a healthcare facility. Certain bacterial clones and plasmids have been linked with specific antibiotic resistance genes e.g. the plasmid pOXA-48 carries the carbapenemase gene blaOXA-48 among clinical Klebsiella pneumoniae, while the IncFII plasmids are noted for carrying the extended spectrum beta lactamase genes blaCTX-M among Escherichia coli of clinical origins. Further details of carriage of antibiotic resistance genes by specific replicon types of plasmids are shown in Table . Biofilms are particularly serious problems in different healthcare settings due to their ability to withstand high concentrations of antibiotics contributing to antibiotic resistance. Such biofilms have formed a pool of plasmid-borne antibiotic resistance genes that have been found to spread through horizontal gene transfer (Michaelis and Grohmann, Citation2023). The presence of plasmids among biofilms promote their spread in different environments.

Table 1. Plasmid replicon types and antibiotic resistance genes carriage.

Most plasmids that carry antibiotic resistance genes in clinical and environmental settings are conjugative. This implies that such plasmids carry genetic sequences called the fertility factor that facilitate the replication and subsequent transfer to other related bacteria (Partridge et al. Citation2018). Ideally, most conjugative plasmids carry one or more antibiotic resistance genes and such genes are transferred simultaneously when such conjugative plasmids replicate and spread within the clinical and other environments (Cook and Dunny Citation2014). This is the major reason why plasmids carrying antibiotic resistance genes are easily disseminate in clinical environments, contributing immensely to the problem of antibiotic resistance.

Molecular epidemiology of antibiotic resistance plasmids

The innate ability of most antibiotic resistance plasmids to replicate and spread resistance determinants to other bacteria and environments makes them suitable for tracking the spread of antibiotic resistant bacteria (Goswami et al. Citation2020). Antibiotic resistance phenotypes of resistant bacteria in clinical infections have been used for tracking the spread of such bacteria, but this method has proven grossly unreliable over the years due to the fluctuations of resistance phenotypes with changing environmental conditions (Anjum Citation2015). Some molecular methods used for the characterization of plasmids are gradually replacing the phenotypic methods and have become gold standard for surveillance and for investigating the spread of plasmids in epidemic outbreaks of infections in hospitals. They are also useful for tracking infections in the endemic spread of antibiotic resistant bacteria within population and community settings (Anjum Citation2015; Negeri et al. Citation2023).

However, plasmid replicon typing and whole genome sequencing (WGS) have currently formed the major technologies in epidemiological investigations (Mutai et al. Citation2019; Oliveira et al. Citation2020; Moglad et al. Citation2022; Al-Trad et al. Citation2023; Liu et al. Citation2023). Replicon typing determines the incompatibility groups of antibiotic resistance plasmids, with some specific replicon types showing higher potential to transfer resistance genes than others. The WGS give a global genetic information, including plasmids, of an infectious organism with high discriminatory power (Liu et al., Citation2023). The plasmid replicon typing is based on the standard polymerase chain reaction and sequencing of the ori sequence and their subsequent grouping into incompatibility (Inc) groups. Plasmids of the same incompatibility groups are not compatible and cannot co-exist in the same bacterial host, while plasmids of different compatibility groups can co-exist in the same bacterial host. Plasmids have been categorized into 18 different replicon types (or incompatibility groups) that can be used as a basis for surveillance of spread of antibiotic resistance genes in hospital and community settings (Mutai et al. Citation2019). Similar incompatibility groups of plasmids in clinical environments are commonly used to indicate the clonal spread of such plasmids, while the same principle is applicable to such clonal spread in community and endemic settings (AbdulAziz et al. Citation2017). The WGS appears to be gradually replacing replicon typing due to its high resolution and accuracy. Standard bioinformatics workflows and databases have now been established to extract specific plasmid sequences from bacterial WGS, and this has simplified the use of WGS in surveillance of antibiotic resistance plasmids in many clinical environments (David et al. Citation2020; Sengeruan et al. Citation2022).

Different antibiotic resistance genes have been located on plasmids with specific replicon types. These different replicon types show different characteristics and have been associated with the carriage of different AR genes. The IncFI plasmids for example possess the enhanced ability to carry antibiotic resistance genes (Rafaï et al. Citation2015; Puangseree et al. Citation2022). In a study among humans and animals in Nigeria, Salmonella carrying plasmids with the following replicon types were detected – FIA, FIB, Frep and W (Adedokun et al. Citation2023). Conventional replicon typing and WGS have revealed that the carbapenem-resistant K. pneumoniae in different clinical infections has been found to carry plasmids, especially in the FIA, FIB, FII, A/C HI1B and IncC replicon types (Elrahem et al. Citation2023; Kuzina et al. Citation2023). In a clinical surveillance study to track the spread of antibiotic resistance plasmids in Iraq, some plasmids belonging to the following replicon types: FII, FIA, FIB, B/O, K, I1 and N were spread extensively and they carried ESBL and aminoglycoside resistance genes (Huang et al. Citation2012). Multidrug-resistant Salmonella isolated from cases of typhoid fever and other environments carry genes that code for fluoroquinolones and ESBLs on plasmids in the replicon groups IncHI1 and IncI1 (Mutai et al. Citation2019). The beta-lactamase resistance genes found in most Enterobacteriaceae in different clinical settings are carried by IncF plasmid (Negeri et al. Citation2023; Ogbolu et al., n.d.; Rozwandowicz et al. Citation2018; Rocha-Gracia et al. Citation2022). More recently, the beta-lactamase resistance genes blaKPC and blaNDM have been found among IncHI1B plasmids and are known to be conjugative (Oliveira et al. Citation2020). In addition to the IncF plasmids being the most prominent carriers of antibiotic resistance genes, they also offer other selective advantages to the bacteria (Mahérault et al. Citation2019; Pitout and Chen Citation2023). Interestingly, plasmid replicon typing has been used to establish the clonality of antibiotic resistance plasmids among humans and animals, with the following replicon groups matching in the different hosts: IncI1, IncN, IncHI1B, IncF, IncFIIS, IncFIB, and IncB/O (Zurfluh et al. Citation2014). Some plasmid incompatibility groups have also been shown to simultaneously carry antibiotic resistance and virulence genes, especially among E. coli and K. pneumoniae (Ahmed et al. Citation2021). The presence of the colistin resistance gene variants mcr among certain replicon groups has emerged as a serious concern in clinical settings (Ai et al. Citation2021).

The clinical significance of the various replicon plasmid types harboring several antibiotic resistance genes is apparent in the ease with which such genes spread through plasmid replicon types in their respective clinical environments. The increased consumption of antibiotics in clinical settings cumulatively increases the selective pressure that allows those clinical bacteria carrying antibiotic resistance plasmids to thrive within the clinical setting (Tello et al. Citation2012; Willmann et al. Citation2015). Activities of the plasmids is further enhanced through other genetic elements like transposons and insertion sequences (Lipszyc et al. Citation2022). Such insertion sequences can carry antibiotic resistance genes that transverse between the chromosome and plasmids. Antibiotic resistant bacteria can later dominate the clinical environments leading to surge of antibiotic-resistant infections and increased burden on healthcare.

Conclusion and recommendation

The majority of infections spread by antibiotic resistance plasmids that are conjugative (Singh et al. Citation2022). While there are a deluge of reports regarding plasmid-mediated antibiotic resistance genes in bloodstream and urinary tract infections, there appears to be fewer reports on plasmid-mediated antibiotic resistance among bacterial pathogens that cause SSTIs. It is therefore necessary to focus more studies on the roles that plasmids play in skin and soft tissue infections.

The majority of studies that detail the spread of antibiotic-resistant pathogens in clinical and community settings are focused more on developed countries, with fewer studies carried out in LMICs. This contrasts with the underlying fact that LMICs may have a higher burden of antibiotic resistant infections, driven by the COVID-19 pandemic, increased poverty and burden of infectious diseases (Sulis et al. Citation2022). More population-wide studies and molecular surveillance needed to ascertain the burden of antibiotic resistant bacterial infections and how they are spread in low resource settings. Molecular typing for plasmids is one of the best approaches to achieve this aim and provide some mitigating measures to curb the spread of antibiotic resistant bacteria in LMICs (Sulis et al. Citation2022).

It should also be noted that plasmid replicon typing is the gold standard for the identification of antibiotic resistance and virulence plasmids in many clinical environments. However, fewer replicon typing methodologies to track the spread of antibiotic resistance plasmids are reported in LMICs. This could be due to the costly technicalities involved in replicon typing procedures, which may be outside the affordability range of most laboratories in LMICs. More expertise and infrastructure are needed to assist in molecular surveillance of plasmid-mediated antibiotic resistance in clinical and community settings, especially for LMICs.

The WGS is gradually gaining more acceptability in the surveillance of antibiotic resistant bacteria and will eventually replace plasmid replicon typing. This is due to its higher accuracy and power of discrimination. Unfortunately, most studies that report plasmid-mediated antibiotic resistance infections in humans do not utilize this technique because of the relatively increased cost of sequencing (although the overall cost has reduced drastically in developed countries), which is still beyond the reach of laboratories in LMICs. In addition, there seems to be a lack of standardized bioinformatics workflow for the analysis and assembly of whole genome sequencing for LMICs. Funding should be provided immediately to assist laboratories, especially in LMICs to develop their expertise and manpower in WGS. This will enable infectious diseases researchers to carry out innovative surveillance studies. This will also inform other critical efforts to reduce the risk of the emergence of plasmid-mediated antibiotic-resistant infections among humans in clinical and community settings (Karikari Citation2015).

In addition to the molecular strategies already highlighted as one of the measures to mitigate the spread of antibiotic resistant bacteria and antibiotic resistance plasmids, hospitals in low resource settings should place priority on antimicrobial stewardship as one of the measures to curtail the spread of plasmid-borne antibiotic resistant bacteria (Majumder et al. Citation2020). Antimicrobial stewardship is expected to reduce empirical antibiotic treatment which has increased selective pressure on clinical bacteria and increased antibiotic resistance. Furthermore, emphasis should also be placed on hand washing in clinical settings as a means to curtail the spread of antibiotic resistant bacteria in clinical infections and settings.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Authors’ contributions statement

Conceptualization and design of the work was made by A. A. O.; Drafting of paper A. A. O. and A. O. J.; Critical revision of paper, O. A. T and O. A. O. All authors agree to be accountable for all aspect of the work.

Data availability statement

Data sharing is not applicable to this article as no new data were created or analyzed in this study.

Additional information

Funding

The author(s) reported there is no funding associated with the work featured in this article.

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