INTRODUCTION
Bacteria are present both inside and on the surface of the human body, especially on the skin and the mucous membranes. Most of these bacteria are innocuous, many are beneficial, and some are even necessary. However, other bacteria, which are categorized as pathogens, are able to colonize, invade, and damage the host and thus cause illness. Pathogenicity is an ability of an agent to cause disease, and the pathogenic bacteria possess several factors that enable them to enhance their virulence (i.e., the degree of pathogenicity). Most pathogens make use of a combination of two properties to cause disease: (i) toxicity, the degree to which a substance causes harm, and (ii) invasiveness, the ability to penetrate into the host and spread (1). The final balance of an infectious disease process will depend on the virulence or pathogenicity of the microbe as well as the host status in relation to risk factors such as immune status, age, diet, and stress, which determine the host susceptibility to infection. Hosts and bacteria have coevolved over millions of years, during which pathogenic bacteria have modified their virulence to adapt to the host defense systems. This contrasts with the relatively recent evolution of antimicrobial resistance (defined as the ability of an organism to resist the action of an antimicrobial agent to which it was previously susceptible). Although medical practice has limited the development and spread of pathogens, this has led to a global increase in antibiotic resistance. The evolution and spread of resistance are relatively recent and have occurred mainly in the last 50 years, i.e., since antibiotics were first used. Therefore, virulence and resistance have evolved over very different timescales.
Despite the difference in the evolution of these processes, they share some common characteristics. (i) From a biological point of view, both processes are necessary for bacteria to survive under adverse conditions. Virulence mechanisms are necessary to overcome host defense systems, and the development of antimicrobial resistance is essential to enable pathogenic bacteria to overcome antimicrobial therapies and to adapt to and survive in competitive and demanding environments (new niches). Immune defense systems and antibiotic pressure represent bottlenecks for survival of the bacterial population, as they greatly limit the capacity for growth and lead to decreased microbial diversity (2, 3). (ii) Virulence and resistance factors are similar in that most of the determinants have been transmitted between species or genera by horizontal gene transfer (HGT); the transfer of DNA fragments (mobile genetic elements [MGEs]) is probably the main genetic mechanism of dissemination and coselection of virulence and resistance genes, although other mechanisms such as compensatory or adaptive mutations may also be involved (4, 5), as will be discussed below. (iii) Antibiotic resistance is often associated with infection and is therefore also related to virulence, as in the cases of biofilm-producing microorganisms or intracellular infections (6, 7). (iv) Other characteristics that are common to virulence and resistance include the direct involvement of efflux pumps (8), porins (9), cell wall alterations (10), and two-component systems that activate or repress the expression of various genes, such as those involved in resistance and virulence (11).
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In healthy individuals, opportunistic pathogens are not able to produce infection because they lack the necessary mechanisms of toxicity and invasiveness that enable primary pathogens to overcome the host immune system. However, in some individuals, such as immunocompromised patients, opportunistic pathogens can produce infection, which can be prevented mainly by the use of antimicrobial therapies. Certain multiresistant opportunistic species, such as Pseudomonas aeruginosa and Acinetobacter baumannii, can colonize niches where many other species cannot survive (environments with high antibiotic pressure) and can even displace the commensal flora. This is one example of how antimicrobial resistance can increase the virulence or fitness of certain species in some environments, often helping these species to colonize new niches. Therefore, although antibiotic resistance is not in itself a virulence factor, in certain situations it is a key factor in development of infection, and it may be considered a virulence-like factor in specific ecological niches which antibiotic-resistant bacteria are able to colonize. This is especially true in the hospital environment (intensive care units, burn units, etc.), in which if a opportunistic pathogen is drug resistant, it can cause disease more readily (12). In environments where selective antibiotic pressure prevails, some opportunistic pathogens are able to colonize new ecological niches because of their plasticity and ability to adapt through the acquisition or development of mechanisms of resistance and persistence.
The use of antibiotics has changed the natural evolution of bacteria by reducing susceptible pathogenic populations and increasing resistant populations. Resistance is often associated with a fitness cost because the genetic burden required for resistance may be deleterious in antibiotic-free environments. In this case, restriction of the use of antibiotics has been proposed, with the aim of eradicating resistant bacteria (13). However, the genetic background of resistant pathogens allows them to persist in the presence of minimal concentrations of antibiotics or even in the absence of these, as discussed throughout this review (14). Hypermutation, compensatory mutations, and cross coselection are a few of the many mechanisms that favor the persistence of resistant pathogens and even, in some cases, selection of the most virulent and most resistant pathogens.
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This review considers the relationship between virulence and resistance, including the role of increasing resistance in relation to fitness costs. Increased resistance is associated in most cases, either directly or indirectly, with decreased virulence and fitness. However, evidence also shows the opposite, and it is increasingly evident that the relationship is often of greater benefit to the pathogen, resulting in a growing public health problem.
This review also considers the impacts of resistance to the main antimicrobial agents used in clinical practice as well as the genetic events associated with evolution of pathogens on virulence and/or fitness costs. In vivo and in vitro laboratory examples and clinical studies of specific pathogens are presented, and the interplay between both of these important bacterial characteristics is analyzed in detail. Because of the importance of the interactions between resistance and virulence, these aspects are always considered together. Partial analyses that consider aspects of resistance and/or virulence separately were disregarded for the purposes of this review.
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