Vol. 68, No. 12
Host-Pathogen Interactions: Basic Concepts of Microbial Commensalism, Colonization, Infection, and Disease
Division of Infectious Diseases, Department of Medicine, andDepartment of Microbiology, Albert Einstein College of Medicine, Bronx, New York 10461 Most of the terminology used to deﬁne the host-microbe interaction has been in use for nearly a century. Early in this period, microbes were thought to be primary aggressors that governed the host-pathogen interaction, resulting in disease. Later, new information about the attributes of microbes and their hostsresulted in the understanding that the hostpathogen interaction does not always result in disease. This recognition, in turn, led to the introduction of terms to explain states in which microbes exist within hosts without causing overt disease and why some microbes only cause disease in certain hosts. Commensal, carrier state, and opportunist were terms put forth to account for microbes andconditions that were sometimes associated with disease but for which Koch’s postulates could not be fulﬁlled for one reason or another. Most of these terms were originally proposed to describe the behavior of particular microbes, rather than to deﬁne a more general host-microbe relationship. Recently, we reviewed the concepts of virulence and pathogenicity and described how the deﬁnitions for these termschanged over the years as microbiologists tried to ﬁnd ways to convey that microbial pathogenesis reﬂects an interaction between two entities, host and pathogen (7). Based on the concept that host damage was the most relevant outcome of the host-pathogen interaction, we proposed revisions to the deﬁnitions of the terms pathogen, pathogenicity, and virulence (7). However, the proposed frameworksuggested a need to reexamine the terms used to deﬁne the outcomes of host-microbe interactions. Here, we critically review the origin and historical evolution of key concepts used to describe the outcome of host-microbe interactions, namely, infection, commensalism, colonization, persistence, infection, and disease. We propose that the meaning of these terms can be clariﬁed by placing them in thecontext of the damage framework put forth previously (7). LEXICON OF MICROBIAL PATHOGENESIS Once the germ theory of disease was accepted, microbes were considered to be pathogens if they met the stipulations of Koch’s postulate. However, it rapidly became apparent that (i) although there are many microbes, most human infections were caused by only a few; (ii) some microbes were classiﬁed aspathogens although they did not cause disease in every host; and (iii) some microbes were classiﬁed as nonpathogens, although they did cause disease in certain hosts (for an early review, see reference 56). In addition, it became evident that
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normal individuals harbored, in their mouth, gut, and skin, large numbers of microbes that did not cause disease. New ideas and terminology, heretofore referred to collectively as a lexicon, were devised to accommodate this information. By the early twentieth century, it was apparent that pathogenicity was neither an invariant nor a stable characteristic of most microbesand that the acquisition of pathogenic microbes was not necessarily synonymous with disease. In the laboratory, the successful attenuation of pathogens revealed that virulence could be increased or decreased by animal passage and/or in vitro culture (for a review of early experimentation, see reference 4). This scientiﬁc advance eventually led to the development of vaccines that controlled many of...