EVOLUTION O ANTIBIOTIC RESISTANCE BY HUMAN AND BACTERIAL NECHE CONSTRUCTION

Abstract Antibiotic treatment by humans generates strong viability selection for antibiotic‐resistant bacterial strains. The frequency of host antibiotic use often determines the strength of this selection, and changing patterns of antibiotic use can generate many types of behaviors in the population dynamics of resistant and sensitive bacterial populations. In this paper, we present a simple model of hosts dimorphic for their tendency to use/avoid antibiotics and bacterial pathogens dimorphic in their resistance/sensitivity to antibiotic treatment. When a constant fraction of hosts uses antibiotics, the two bacterial strain populations can coexist unless host use‐frequency is above a critical value; this critical value is derived as the ratio of the fitness cost of resistance to the fitness cost of undergoing treatment. When strain frequencies can affect host behavior, the dynamics may be analyzed in the light of niche construction. We consider three models underlying changing host behavior: conformism, the avoidance of long infections, and adherence to the advice of public health officials. In the latter two, we find that the pathogen can have quite a strong effect on host behavior. In particular, if antibiotic use is discouraged when resistance levels are high, we observe a classic niche‐construction phenomenon of maintaining strain polymorphism even in parameter regions where it would not be expected.

[1]  S. Bonhoeffer.  Adaptive Dynamics of Infectious Diseases: Managing Antibiotic Resistance: What Models Tell Us? , 2002 .

[2]  B. Cvjetanović.  The dynamics of bacterial infections , 1982 .

[3]  F. Baquero,et al.  Mutation Frequencies and Antibiotic Resistance , 2000, Antimicrobial Agents and Chemotherapy.

[4]  F. J. Odling-Smee,et al.  Evolutionary consequences of niche construction and their implications for ecology. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[5]  N. Rashevsky,et al.  Mathematical biology , 1961, Connecticut medicine.

[6]  Barry G. Hall,et al.  Predicting the evolution of antibiotic resistance genes , 2004, Nature Reviews Microbiology.

[7]  M. Nowak,et al.  Virus dynamics: Mathematical principles of immunology and virology , 2001 .

[8]  M. Iseman,et al.  Evolution of drug-resistant tuberculosis: a tale of two species. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Marcus W Feldman,et al.  Coevolution of pathogens and cultural practices: a new look at behavioral heterogeneity in epidemics. , 2002, Theoretical population biology.

[10]  M. Swartz,et al.  Hospital-acquired infections: diseases with increasingly limited therapies. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[11]  J. Watmough,et al.  Reproduction numbers and sub-threshold endemic equilibria for compartmental models of disease transmission. , 2002, Mathematical biosciences.

[12]  F. J. Odling-Smee,et al.  Niche Construction: The Neglected Process in Evolution , 2003 .

[13]  John H. Miller,et al.  The standing ovation problem , 2004, Complex..

[14]  O. Diekmann,et al.  On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations , 1990, Journal of mathematical biology.

[15]  D. Livermore.  Bacterial resistance: origins, epidemiology, and impact. , 2003, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[16]  F. M. Stewart,et al.  The population genetics of antibiotic resistance. , 1997, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[17]  Daisuke Nakanishi,et al.  Cost–benefit analysis of social/cultural learning in a nonstationary uncertain environment: An evolutionary simulation and an experiment with human subjects , 2002 .

[18]  M. Lipsitch,et al.  The rise and fall of antimicrobial resistance. , 2001, Trends in microbiology.

[19]  Carl T. Bergstrom,et al.  Ecological theory suggests that antimicrobial cycling will not reduce antimicrobial resistance in hospitals. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  H. Neu,et al.  The Crisis in Antibiotic Resistance , 1992, Science.

[21]  S. Palumbi.  The Evolution Explosion: How Humans Cause Rapid Evolutionary Change , 2001 .

[22]  M. Feldman,et al.  Cultural transmission in a demographic study of sex ratio at birth in China's future. , 2000, Theoretical population biology.

[23]  M A Nowak,et al.  Anti-viral drug treatment: dynamics of resistance in free virus and infected cell populations. , 1997, Journal of theoretical biology.

[24]  R. Anderson,et al.  The relationship between the volume of antimicrobial consumption in human communities and the frequency of resistance. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Palumbi,et al.  Humans as the world's greatest evolutionary force. , 2001, Science.

[26]  H J Bremermann,et al.  A competitive exclusion principle for pathogen virulence , 1989, Journal of mathematical biology.

[27]  B. Levin,et al.  The biological cost of antibiotic resistance. , 1999, Current opinion in microbiology.

[28]  Kaleda K. Denton,et al.  Cultural niche construction with application to fertility control: A model for education and social transmission of contraceptive use. , 2023, Theoretical population biology.

[29]  Fernando Baquero,et al.  Interactions among Strategies Associated with Bacterial Infection: Pathogenicity, Epidemicity, and Antibiotic Resistance , 2002, Clinical Microbiology Reviews.

[30]  B. Galef.  Approaches to the study of traditional behaviors of free-living animals , 2004, Learning & behavior.

[31]  B. Levin,et al.  Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. , 2000, Genetics.

[32]  M. Lipsitch,et al.  Antimicrobial Use and Antimicrobial Resistance: A Population Perspective , 2002, Emerging Infectious Diseases.

[33]  D. Livermore.  Can better prescribing turn the tide of resistance? , 2004, Nature Reviews Microbiology.

[34]  J. Weinberg.  Is resistance futile? , 2005, Cutis.

[35]  M Kakehashi,et al.  The transmission dynamics of antibiotic–resistant bacteria: the relationship between resistance in commensal organisms and antibiotic consumption , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  C. Castillo-Chavez,et al.  To treat or not to treat: the case of tuberculosis , 1997, Journal of mathematical biology.

[37]  M. Feldman,et al.  Cultural niche construction and the evolution of small family size. , 2004, Theoretical population biology.

[38]  David L. Smith,et al.  Persistent colonization and the spread of antibiotic resistance in nosocomial pathogens: resistance is a regional problem. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[39]  P. Kaye.  Infectious diseases of humans: Dynamics and control , 1993 .

[40]  M. Feldman,et al.  Gene-culture coevolution: toward a general theory of vertical transmission. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[41]  S. Blower,et al.  Control Strategies for Tuberculosis Epidemics: New Models for Old Problems , 1996, Science.

[42]  C. Walsh.  Opinion — anti-infectives: Where will new antibiotics come from? , 2003, Nature Reviews Microbiology.

[43]  Carl T. Bergstrom,et al.  The epidemiology of antibiotic resistance in hospitals: paradoxes and prescriptions. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Swartz Mn.  Hospital-acquired infections: diseases with increasingly limited therapies. , 1994 .

[45]  J. Blázquez,et al.  Hypermutation as a factor contributing to the acquisition of antimicrobial resistance. , 2003, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[46]  S Bonhoeffer,et al.  Evaluating treatment protocols to prevent antibiotic resistance. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[47]  E. Rogers,et al.  Diffusion of innovations , 1964, Encyclopedia of Sport Management.

[48]  Mitchell L. Cohen.  Epidemiology of Drug Resistance: Implications for a Post—Antimicrobial Era , 1992, Science.

[49]  F. J. Odling-Smee,et al.  The evolutionary consequences of niche construction: a theoretical investigation using two‐locus theory , 1996 .

[50]  Troy Tassier,et al.  A model of fads, fashions, and group formation , 2004, Complex..

[51]  S. Levin,et al.  Disease transmission dynamics and the evolution of antibiotic resistance in hospitals and communal settings. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[52]  F. Baquero,et al.  Antibiotic-selective environments. , 1998, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[53]  S. Frost,et al.  Quasispecies dynamics and the emergence of drug resistance during zidovudine therapy of HIV infection , 1994, AIDS.

[54]  F. M. Stewart,et al.  The population genetics of antibiotic resistance. II: Analytic theory for sustained populations of bacteria in a community of hosts. , 1998, Theoretical population biology.

[55]  M W Feldman,et al.  Cultural and biological evolutionary processes: gene-culture disequilibrium. , 1984, Proceedings of the National Academy of Sciences of the United States of America.