Multidrug Resistant Bacteria in the Community: An Update

Abstract

Multidrug resistant (MDR) bacteria are one of the most important current threats to public health. Typically, MDR bacteria are associated with nosocomial infections. However, some MDR bacteria have become quite prevalent causes of community-acquired infections. These may be pathogens which are classically community acquired such as Neisseria gonorrhoeae, Shigella, Salmonella and Streptococcus pneumoniae. Indeed, MDR N. gonorrhoeae is now regarded by the CDC as an urgent threat. The community spread of MDR bacteria, more typically associated with healthcare environments, is also a crucial development. Methicillin-resistant S. aureus (MRSA) and extended-spectrum beta-lactamase (ESBL) producing E. coli are the most prevalent of such bacteria. The prevalence of these is driven by person to person transmission in the community and, in the case of ESBL producing E. coli by the use of antibiotics in agriculture. An important global threat on the horizon is represented by production of carbapenemases by community-acquired hypervirulent Klebsiella pneumoniae. Such strains have already been found in Asia, Europe and North America. Prevention of further community spread of MDR bacteria is of the utmost importance, and will require a multi-disciplinary approach involving all stakeholders.

Introduction

Multidrug resistant (MDR) bacteria are well-recognized to be one of the most important current public health problems. More than 2.8 million antibiotic resistant infections occur in the United States each year, accounting for 35,000 deaths¹. Rising rates of antibacterial resistance have an impact on all aspects of modern medicine, and compromise the results of cancer care, transplantation and surgical procedures². Although difficult to accurately calculate, there are also substantial economic costs to antibiotic resistance. This may result from extended duration of hospital stay, the need for greater outpatient follow-up and the higher costs of new drugs needed to treat MDR bacteria¹. Unfortunately the occurrence of specific MDR bacteria is closely linked to the use of broad spectrum antibiotics, both for empiric as well as for definitive therapy³. This increased use in turn leads to even higher rates of MDR bacteria, thus creating a vicious cycle.

Typically, MDR bacteria were associated with nosocomial infections. However, some MDR bacteria have become quite prevalent causes of community-acquired infections. This is an important development as community spread of MDR bacteria leads to a large increase of the population-at-risk, and subsequently an increase in the number of infections caused by MDR bacteria. In addition, when the incidence of a certain resistance pattern in bacteria causing community-acquired infections exceeds a specific threshold, broader spectrum antibacterials and/or combination antibacterial therapy are indicated for the empiric treatment of community-acquired infections. In this review, we will outline the trends in and epidemiology of community prevalence of various MDR bacteria.

Community-associated, health-care associated and nosocomial infections

Infections can be divided into community onset and nosocomial acquisition. The widely used cut-off to distinguish between these two categories is whether the onset of infection was within the first 48 hours of hospitalization (community-onset) or later (nosocomial). Limitations of this division include the arbitrary nature of the 48 hour time point, as well as the dependence on the timing of diagnosis. If cultures are performed earlier during hospitalization, more infections are likely to be labeled as community-onset.

The category of community-onset can then be further subdivided into community-acquired and healthcare-associated, based on work pioneered by Morin et al. and Friedman et al ^{4, 5}. Generally, an infection is deemed to be healthcare-associated if a patient was hospitalized in an acute care hospital for two or more days within 90 days of the infection; resided in a nursing home or long-term care facility; received recent intravenous antibiotic therapy, chemotherapy, or wound care within the past 30 days of the current infection; or attended a hospital or hemodialysis clinic ⁶.

The remaining category includes those patients who have a community-onset infection, and who do not meet any of the above criteria for health-care associated infection. These infections are considered to be community-acquired. However, for the purposes of evaluating MDR bacteria in the community, these definitions may not tell the whole story. Patients tend to get infected with organisms with which they were previously colonized. Therefore, it is the timing of colonization, rather than the timing of diagnosis of infection that is crucially important to determine the origin of the MDR bacteria. Studies that have employed screening of non-infected individuals have addressed these questions for some MDR bacteria in certain populations.

Antibiotic resistance in bacteria typically regarded as community-acquired

Antibiotic resistant sexually transmitted infections

Multidrug resistant bacteria that cause sexually transmitted infections (STIs) have become increasingly prominent in recent years. Drug resistant Neisseria gonorrhoeae is now regarded by the CDC as an urgent threat (Table 1) and is estimated to infect 550,000 Americans annually ¹. While antibiotic resistance in Chlamydia trachomatis and Treponema pallidum does occasionally occur, these organisms are not renowned as being MDR. In contrast, an emerging pathogen, drug resistant Mycoplasma genitalium, is on the CDC’s “watch list” due to its propensity for multidrug resistance. It should also be noted that bacteria that cause gastrointestinal illness may be sexually transmitted – MDR shigellosis is increasingly recognized as an issue for men who have sex with men ⁷.

Table 1.

Multidrug resistant bacteria observed in the community, classified according to CDC threat level.

MDR Phenotype	Epidemiologic setting of community-onset infections
Urgent Threats
CR-AB	Extremely rare
Candida auris	Extremely rare
Clostridioides difficile	Prior antibiotic exposure; nursing homes
CRE	Rare at present; emerging in India and China
Drug-resistant Neisseria gonorrhoeae	Exclusively community-onset
Serious threats
Drug-resistant Campylobacter	Exclusively community-onset
Drug-resistant Candida	Rare at present; prior azole exposure typical
ESBL + Enterobacterales	Endemic in most parts of the world
VRE	Rare except in nursing home residents
CR-PA	Extremely rare, except in those with suppurative lung disease and extensive antibiotic use
Drug-resistant nontyphoidal Salmonella	Exclusively community-onset
Drug-resistant Salmonella serotype Typhi	Exclusively community-onset
Drug-resistant Shigella	Exclusively community-onset
MRSA	Household colonization; farm animal exposure
Drug-resistant Streptococcus pneumononiae	Almost exclusively community-onset
Drug-resistant tuberculosis	Predominantly community-onset

There are a number of reasons why MDR in bacteria that cause STIs has become so prominent. This includes availability of antibiotics without a prescription in many parts of the world and reliance of treatment that is typically empiric, either based on symptoms or culture independent methods for laboratory diagnosis. In recent years, molecular methods for rapid diagnosis of antibiotic resistance genes in N. gonorrhoeae and M. genitalium have been developed ^{8, 9}. This could improve surveillance and may allow more targeted treatment choices.

Antibiotic resistant gastrointestinal infections

Clostridioides difficile is regarded by the CRC as an urgent AMR threat. Further discussion on this pathogen is beyond the scope of this article. Drug resistant Campylobacter, nontyphoidal Salmonella and Shigella are all serious AMR threats. They infect more than 700,000 people in the United States annually. The use of antibiotics in agriculture with subsequent entry of AMR pathogens (or genes) into human food is the usual means by which these MDR pathogens infect humans. In contrast, in the United States and Western Europe, patients with drug-resistant Salmonella serotype Typhi have typically traveled internationally.

One of the key challenges associated with treatment of antibiotic resistant gastrointestinal infections and STIs is provision of alternatives to orally administered fluoroquinolones and macrolides when resistance is present. Some new antibiotic options are now under development which are hoped to address this need.

Antibiotic resistant respiratory infections

Streptococcus pneumoniae is the most common cause of community-acquired pneumonia and drug-resistant S. pneumoniae infects more than 900,000 Americans annually. In response to this threat, new antibiotics, including delafloxacin, omadacycline, lefamulin, solithromycin, nemonoxacin, and ceftaroline, have recently been approved or are in clinical development¹⁰. Drug-resistant tuberculosis, an enormous global health problem, is beyond the scope of this article.

Antibiotic resistant organisms classically described in hospitals but now found in the community

MRSA

Methicillin-resistant S. aureus (MRSA) is probably the best example of a prevalent and important MDR bacterium that has successfully transitioned from an almost exclusively nosocomial setting to being widespread in the community. The epidemiology of community-associated MRSA (CA-MRSA) has been extensively reviewed elsewhere^{11, 12}. Here, we will give a brief overview of MRSA in the community as it may be predictive of the behavior of other MDR bacteria.

As early as 1982 an outbreak of CA-MRSA was reported in Detroit¹³. In this outbreak, more than half of patients were intravenous drug users, and the remaining patients had several comorbidities that put them at risk. Importantly, various different strains were found in this outbreak¹³. It was not until the early 1990’s that more genuine CA-MRSA outbreaks began to be reported. These outbreaks occurred in populations without specific risk factors. The MRSA strains involved were generally monoclonal or oligoclonal and rather than being extensively multidrug resistant such as nosocomial MRSA strains at that time, these CA-MRSA strains were susceptible to many non-β-lactam antibiotics. In the early 2000’s, a new strain of CA-MRSA – USA300 – became the predominant CA-MRSA in the United States, effectively replacing the previous USA400 CA-MRSA strain¹¹. This USA300 strain is characterized by the presence of the staphylococcal cassette chromosome mec (SCCmec) type IV as well as of genes encoding for Panton-Valentine leucocidin (PVL) toxins¹⁴. Households are an important reservoir for the USA300 strain. In a recent study that utilized whole genome sequencing data, USA300 MRSA was shown to persist in households between 2 and 8 years prior to admission of a symptomatic patient from that household, and to continue to persist for at least another year after that¹⁵. This and other evidence shows conclusively that this specific strain of MRSA has been able to become entrenched in a community setting in the absence of ongoing antibiotic pressure. In addition, specific strains of CA-MRSA have been shown to be associated with exposure to lifestock; so-called lifestock-associated (LA) MRSA. The ST398 LA-MRSA is predominantly found in Europe and America, whereas ST9 LA-MRSA is encountered in Asia¹⁶.

Vancomycin-resistant Enterococci (VRE)

Vancomycin-resistant enterococci (VRE) emerged in the late 1980’s, and became a common cause of nosocomial infections in the 1990’s¹⁷. Studies in the 1990’s did not detect the presence of vancomycin resistance in enterococci isolated from subjects without healthcare exposure in the United States^{18, 19}. In contrast, in European studies from the same time period, VRE was detected in the stool of healthy volunteers²⁰. In addition, VRE was commonly found in European food animals^{21, 22}. The underlying reason for this difference between Europe and the United States is the use of avoparcin – a glycopeptide antibiotic – for the purpose of promoting growth in food animals. Avoparcin was never approved for use in the United States or Canada, but its use was widespread in Europe up to 1997²². After a ban on avoparcin in animal husbandry, rates of VRE in both animal samples, as well as in samples from human volunteers started to decrease^{20, 22}. These important data illustrate the critical link between antibiotic use in the food industry and antimicrobial resistance rates in humans. It also indicates that it is never too late to make a change and that banning antimicrobials from our food chain may have an almost instantaneous positive – and cost-saving – effect.

Around 2000, community-associated VRE began to appear in the US. In a screening study of patients attending an ambulatory care clinic in Nashville, Tennessee, 3 patients tested positive for VRE out of 100 patients screened. One of these patients came in for her annual check-up and had no prior healthcare exposures²³. Also, VRE was found in wastewater from a semi-closed “agri-food” system²⁴. Nonetheless, VRE remains an uncommon pathogen in community-associated infections. In 289 patients with community-onset VRE, 85% of patients had been hospitalized, and 71% had antimicrobial exposure in the last 3 months, respectively²⁵. In another study that included 81 patients with community-onset VRE bacteremia, 79% of patients had prior hospitalizations²⁶. These data indicate that even in those patients where VRE is detected on admission or early during hospitalization, acquisition likely occurred in the healthcare setting. This acquisition was driven by traditional risk factors of antimicrobial exposure, healthcare exposure, chronic illness, indwelling devices, malignancies and immunosuppression^{25, 26}.

The discrepancy between the community spread of MRSA and VRE is notable, as both S. aureus and enterococci are common human colonizers. However, overall colonization with enterococci is much more universal than with S. aureus, and S. aureus is not truly a commensal. Apparently – in contrast to MRSA – high prevalence of current strains of VRE in the community requires either an ongoing incoming supply of VRE into the shared community gut microbiome through the food chain, or a high level of antibiotic pressure. Fitness cost of maintaining a vancomycin resistant phenotype would be an intuitive explanation for the relative lack of true community-associated VRE infections. However, the fitness cost of vancomycin resistance appears to be minimal for enterococci, especially in the context of inducible resistance^{27, 28}. A recent study suggests that pheromone-mediated killing of VRE may account for why vancomycin-susceptible commensal enterococci outcompete VRE in the human gut²⁹. In this study, the prototype multidrug-resistant clinical isolate strain E. faecalis V583 was killed by human fecal flora, whereas commensal antibiotic-susceptible E. faecalis was able to survive in the presence of flora. The killing effect was traced to pheromone production by commensal E. faecalis strains²⁹.

Carbapenem-resistant Acinetobacter baumannii (CRAB)

Acinetobacter baumannii infections are commonly encountered in hospitalized patients, especially in the intensive care³⁰. However, community-associated A. baumannii infections have been well-described especially in (sub-) tropical climates, including Asia and Australia³¹. These are generally associated with pharyngeal carriage and are linked to alcohol abuse and smoking³¹. These are serious infections and the attributable mortality in 80 patients with bacteremia and/or pneumonia from various case series was reported at 56%³¹. Community reservoirs for A. baumannii include environmental sources such as soil and vegetables, as well as human and animal skin and throat carriage. Furthermore, A. baumannii has also been recovered from human lice³².

A. baumannii is intrinsically resistant to several antibiotic classes. In addition, carbapenem resistance may occur through acquisition of carbapenemases such as IMP-like carbapenemases and/or oxacillinases (OXA)³³. The rate of carbapenem resistance in clinical isolates of A. baumannii rose sharply from 9% to 40% between 1995 and 2004 in the US³⁰. More recent studies suggest that this rate has remained around 40%^{34, 35}. In contrast, the rate of carbapenem resistance in Acinetobacter infections isolated from community-dwelling patients has remained around 4%³⁴. Similarly, resistance to carbapenems was detected in only one out of 23 community-dwelling volunteers who had A. baumannii isolated from their hands³⁶. In an Australian study on 36 patients with community-onset bacteremic Acinetobacter pneumonia, all tested isolates were susceptible to carbapenems³⁷. A more worrisome report from China described 32 patients with community-acquired pneumonia caused by A. baumannii. Three and 6 isolates were non-susceptible to meropenem and imipenem, respectively. In addition, bla_OXA-23 found in 12 of 15 tested isolates, some of which tested susceptible to both meropenem and imipenem³⁸. Of note, 87% of patients with MDR A. baumannii had a “hospitalization history”, suggesting that these did not truly represent community-associated infections³⁸.

In summary, community-associated CRAB appears to remain uncommon, likely reflecting the natural habitats of Acinetobacter species, and the differences between true community strains found to cause infections in Asia and Australia and hospital-associated strains. Of concern is the potential for acquisition of carbapenemases by such a community strain, especially in high antibiotic use areas in Asia.

Multi-drug resistant Pseudomonas aeruginosa

P. aeruginosa is a common cause of nosocomial infections, including bloodstream infections and pneumonia. It prefers moist environments and can be found in a large variety of places in the hospital, including sink traps and aerators, various equipment such as scopes and respiratory gear and contaminated solutions³⁹. In addition, P. aeruginosa may be present on fresh fruit and vegetables as well as on the fingernails of healthcare providers³⁹.

Similar to A. baumannii, P. aeruginosa is intrinsically resistant to many antibiotic classes. Furthermore, additional acquired antibiotic resistance arises relatively easily and quickly after antibiotic exposure. Some patients have chronic biofilm-mediated pseudomonal colonization; patients with cystic fibrosis (CF) are an important example⁴⁰. In these patients, repeated antibiotic courses are the rule, as is the subsequent development of MDR strains. While these patients are often community-dwelling, these infections are clearly healthcare-associated. Nonetheless, spread of MDR isolates between patients with CF has been well described and is an important infection control risk⁴¹.

True community-associated infections with MDR P. aeruginosa fortunately remain very uncommon^{42, 43}. In a cohort of 60 patients with community-acquired bloodstream infections with P. aeruginosa, 100% of isolates were meropenem susceptible, and 95% were susceptible to piperacillin/tazobactam and ceftazidime⁴⁴. A case report from Turkey describes a young man without healthcare exposure who presented with a pyogenic liver abscess caused by a P. aeruginosa strain that was only susceptible to imipenem, amikacin, and colistin ⁴⁵.

Enterobacteriaceae that produce extended spectrum β-lactamases

Enterobacteriaceae are very common causes of community-associated infections, including urinary tract infections and bacteremia. Unfortunately – in contrast to the situation described above with P. aeruginosa and A. baumannii – there is widespread resistance in community-associated enterobacteriaceae isolates mediated by extended spectrum β-lactamases (ESBL) ⁴⁶. This is a global phenomenon and involves patients of all ages including pediatric populations. In a multicenter, prospective US study over a one year period in 2009-2010, 4% of E. coli community-onset isolates were ESBL producers⁴⁷. The majority reflected urinary tract infections such as cystitis or pyelonephritis. The most common ESBL encountered were of the CTX-M group (91%), the remaining ESBLs were either SHV (8%) or CMY-2 (1%). Most isolates (54%) belonged to the ST131 clonal group⁴⁷. E. coli ST131 is a globally disseminated MDR clone, and is characterized by resistance to fluoroquinolones in addition to production of CTX-M type ESBL⁴⁸.

In Asia, the Middle East, South America and some parts of Europe, community-onset infection with ESBL-producing E. coli is extraordinarily frequent. Lower prevalence regions include North America, some parts of Northern Europe, Australia and New Zealand. Specific risk factors for community-onset ESBL-producing E. coli infections have been found in these low prevalence regions. Reported risk factors from a Chicago-based study for ESBL-producing E. coli included travel to India (OR 14.4), increasing age (OR 1.04 per year), and prior use of ciprofloxacin (OR 3.92)⁴⁹. In a German survey-based study, risk factors for ESBL-positive E.coli colonization included an Asian language being the primary language spoken in the household (OR 13.4) and frequent pork consumption (OR 3.5)⁵⁰. A population-based study in London also suggested South-Asian ethnicity and older age as risk factors for ESBL-positive E. coli bacteriuria⁵¹. A study performed in Australia and New Zealand also found that birth on the Indian subcontinent or travel to SouthEast Asia, China, India, Africa or the Middle East were risk factors for community-onset third generation cephalosporin resistant E. coli infections⁵².

A significant problem in Asia is disseminated infection with hypervirulent Klebsiella pneumoniae strains. These “hypermucoviscous” strains have a propensity to cause community-onset pyogenic liver abscess and sometimes metastatic infections, including meningitis⁵³. While these strains were typically susceptible to multiple antibiotics, community-onset ESBL-producing strains are now well described and appear to be increasing⁵⁴.

Community-associated ESBL-producing enterobacteriaceae are of specific concern as treatment requires broad-spectrum antibiotics. A randomized controlled trial to address the question of comparative efficacy of piperacillin-tazobactam vs. meropenem to treat bloodstream infections caused by ceftriaxone non-susceptible E. coli and Klebsiella sp., showed that carbapenems were the more reliable choice⁵⁵. Whether carbapenems are always indicated for infections caused by ESBL-producing organisms remains controversial. Tamma and colleagues in a recent observational study showed that piperacillin/tazobactam was as effective as carbapenems for complicated urinary tract infection in the absence of bloodstream infection⁵⁶. A number of trials of “carbapenem-sparing” options for ESBL producing organisms are now planned or underway⁵⁷.

Carbapenemase-producing Enterobacteriaceae

Carbapenem-resistant enterobacteriaceae (CRE) represent an immediate public health threat that requires urgent and aggressive action^{58, 59}. CRE are resistant to most antibiotics and clinical outcomes after CRE infections are generally poor^60-65. While less frequent than carbapenem-resistant Klebsiella pneumoniae (CRKP), carbapenem resistant E. coli (CREC) constitute an important subset of CRE, and are on the rise globally and outbreaks have been reported in the US^{66, 67}. To date, most CRE infections in the United States and Europe are health-care associated, with patients from long term care facilities at especially high risk⁶⁸. Although data from Asia are somewhat sparse, carbapenemases have been found in bacteria recovered from drinking water in India and in food-producing animals in China^{69, 70}.This raises the spectre of huge numbers of people in these large countries being colonized with CRE. It is now clear that hypervirulent Klebsiella can be carbapenem-resistant. This has been found in both Asia and elsewhere in the world, and has been associated both with KPC and other carbapenemase types ^71-76. A worrying development has been the finding of a transmissible plasmid which augments virulence in K. pneumoniae ⁷⁷. Disturbingly, this plasmid could be conjugated to carbapenem resistant strains, enabling them to simultaneously express carbapenem resistance and hypervirulence.

Given the rapid global spread of ESBL-producing E. coli ST131, another obvious concern is for this highly successful clone to acquire a carbapenemase. Indeed, several reports of carbapenemase-producing E. coli ST131 have been published^78-80. In a study from India, ST131 clinical isolates were compared to non-ST131 clinical isolates. Overall 20% of clinical isolates were positive for metallo-β-lactamases such as bla_NDM-1, which was evenly distributed between ST131 and non-ST131 E. coli⁷⁹. As the epidemiology of ESBL is estimated to be about 10 years ahead of that of the carbapenemases, it is likely that community-associated carbapenem-resistant ST131 E. coli will become a major threat in the near future.

Prevention

Prevention of further spread of MDR bacteria in the community is one of the most urgent public health challenges. Unfortunately, national or even regional data on antibiotic susceptibilities are often limited. In addition, when these data are available in some form, the accompanying epidemiologic metadata is usually too restricted to determine which isolates are truly community-associated. Furthermore, clinical infections are generally the tip of the proverbial iceberg and once a signal is generated that is sufficient in amplitude to get the attention of policy-makers, subclinical spread has already occurred.

Any successful prevention strategy will have to consist of a multi-pronged approach and involve all stakeholders. In addition to human clinical antimicrobial stewardship, we need to remove antibiotics from the food chain. Furthermore, we need to limit the amount of xenobiotics such as quaternary ammonium compounds that reach the environment⁸¹. Another challenging step in limiting exposure of bacteria to antibiotics is the treatment of contaminated wastewater such as that generated by pharmaceutical factories and medical facilities. For instance, a study evaluated samples collected from a wastewater treatment plant in India that received water from 90 regional bulk drug manufacturers containing – amongst other compounds – higher concentrations of ciprofloxacin than are generally found in the blood of patients who are being treated with this agent. Bacteria recovered from this water were tested against 39 antibiotics. Approximately 30% of bacteria were resistant 29-32 antibiotics tested, and another ~20% were resistant to 33-36 antibiotics⁸². The magnitude of this effect, combined with the knowledge that soil-dwelling bacteria will pass on resistance genes to more clinically relevant bacteria, illustrates the importance of limiting this contamination⁸³.

Antimicrobial stewardship is developing rapidly as a hospital specialty. Stewardship teams often will combine strengths from Infectious Disease medical specialist and doctors of pharmacy to evaluate the appropriateness of choice and duration of antibiotic strategies⁸⁴. However, most antibiotics are prescribed in ambulatory care and more attention is needed in this realm to really impact overall community antibiotic exposure⁸⁵. This will not only require a paradigm shift in the behavior of prescribers, but also a cultural shift in the public on the risks and benefits of antibiotics. Rapid diagnostic testing to identify MDR bacteria more quickly and thus limit the empiric use of unnecessarily broad antibiotics will be of great significance. Also, rapid testing to diagnose alternative, non-bacterial etiologies is important.

An important question is whether any interventions can address the issue of chronic colonization with MDR bacteria. Obviously, decolonizing these patients would decrease the risk of transmission. Also, the burden on the individual patient of this condition should not be underestimated. In many healthcare systems, patients with MRSA or CRE are “labeled” as carriers for life, resulting in the institution of isolation precautions whenever they are admitted to the hospital. This has multiple adverse effects and leads to decreased patient satisfaction⁸⁶. For these reasons, decolonization is a theoretically attractive option. However, most decolonizing strategies involve the use of antibiotics. For MRSA decolonization, most strategies involve some combination of intranasal mupirocin with topical chlorhexidine⁸⁷. This approach has been shown to be effective in decreasing infections after surgery⁸⁸. However, the effect is generally short-lived and recurrence of colonization is the rule. For enteric bacteria, no good options are currently available. Various selective gut decontamination strategies have been described, but none have shown true promise. In addition, with growing knowledge of the role of the gut microbiome in the defense against MDR bacteria, it would seem counter-intuitive to give even more antibiotics. Modulating the gut microbiome either through probiotics or through fecal microbiota transplantation is a promising, but as of yet experimental method of decolonizing patients.

Summary

In conclusion, antibiotic resistance is clearly increasing in bacterial pathogens typically regarded as community acquired. Additionally there is community spread of common nosocomial MDR pathogens. The success of these pathogens in the community is likely secondary to a number of factors that include the natural habitats of the bacteria, and the competition present in those niches. In addition, certain strains of bacteria appear to be much more able to maintain their MDR phenotype and spread throughout the community. This is most likely secondary to additional genetic content that compensates for the relative fitness cost of the expression of genes associated with antibacterial resistance. Community spread of MDR bacteria is an important public health threat that should be approached urgently and pro-actively.