Antimicrobial resistance at a community level
Authors: Rodney Dean Adam
Journal: The Lancet Planetary Health (2018)

Antimicrobial resistance is a major problem globally, with levels of resistance in many common bacterial pathogens increasing far more rapidly than the development of new antimicrobial agents. Fortunately, the problem is drawing international attention, and WHO, the US Centers for Disease Control and Prevention, and many other organisations are making major efforts to curtail it. The Article by Mark A Caudell and colleagues1Caudell MA Mair C Subbiah M et al.Identification of risk factors associated with carriage of resistant Escherichia coli in three culturally diverse ethnic groups in Tanzania: a biological and socioeconomic analysis.Lancet Planet Health. 2018; 2: 441-449Google Scholar in this issue of The Lancet Planetary Health is an important contribution to understanding the interaction between humans and domestic animals in the transmission of resistant bacteria. In this study, the authors measured the antimicrobial susceptibilities of 11 470 presumed Escherichia coli (lactose-fermenting Gram-negative rods) isolates from 225 households in 13 villages representing three ethnic groups (Chagga, Arusha, and Maasai) in northern Tanzania. They subsequently sequenced selected isolates from the Maasai community and found that more than 90% of the samples were truly E coli; most of the remainder were Enterobacter cloacae. Because Enterobacter species are inherently resistant to some of the selected antibiotics, this could have led to overestimation of the resistance level of E coli. Human faecal samples were collected from pit toilets, and milk samples were collected from milk containers at the households. A strength of this work is that the sampling was done at the household level, avoiding the bias inherent in using clinical samples. Caudell and colleagues also obtained information about several factors that could be assessed for their effects on antimicrobial resistance levels. Results suggest that antimicrobial resistance patterns are shared among humans and livestock. One of the notable findings of this study was that the prevalence of resistant organisms was associated with sharing water sources with livestock and wild animals. Additionally, the prevalence of resistant organisms in Maasai households was associated with the amount of unboiled milk ingested. The authors correctly point out the importance of an approach to antimicrobial resistance that goes far beyond individual human consumption. A comprehensive approach should control or eliminate the use of antimicrobials for growth promotion in animals raised for human consumption and control therapeutic use in animals and humans.2Van Boeckel TP Glennon EE Chen D et al.Reducing antimicrobial use in food animals.Science. 2017; 357: 1350-1352Crossref PubMed Scopus (279) Google Scholar Additionally, as discussed in this Article, limitation of transmission between humans and their animals could also be an important target to help to curb the spread of resistant organisms. The importance of limitation of the transmission of disease-causing zoonotic organisms has long been recognised, but the transmission of resistant organisms between animals and humans in the absence of disease has been less well researched. However, Caudell and colleagues' claim that improvements in antimicrobial stewardship in low-income countries is unlikely to convey reductions in antibiotic resistance is incorrect. First, this study is a snapshot at a brief point in time that does not allow for extrapolation of changes in resistance levels over time. Some (but certainly not all) studies have shown reduction in the prevalence of resistant bacteria in hospitals that reduce antimicrobial use;3Baur D Gladstone BP Burkert F et al.Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis.Lancet Infect Dis. 2017; 17: 990-1001Summary Full Text Full Text PDF PubMed Scopus (389) Google Scholar others have shown reduced prevalence of resistance bacteria when regional usage is reduced.4Sundqvist M Reversibility of antibiotic resistance.Upsala J Med Sci. 2014; 119: 142-148Crossref PubMed Scopus (27) Google Scholar Antimicrobial agents are overused in people with viral respiratory infections and numerous other self-limiting illnesses. This issue is exacerbated by the ready availability of antibiotics without prescription in many countries. Thus, it remains urgent to emphasise reduced use of antimicrobials by humans. The resistance problem is also too complex to reduce to a single organism, or even group of organisms. For example, other regional studies show high prevalence of resistant Gram-negative species in clinical isolates from East Africa.5Brander RL Walson JL John-Stewart GC et al.Correlates of multi-drug non-susceptibility in enteric bacteria isolated from Kenyan children with acute diarrhea.PLoS Negl Trop Dis. 2017; 11: e0005974Crossref PubMed Scopus (20) Google Scholar, 6Maina D Omuse G Revathi G Adam RD Spectrum of microbial diseases and resistance patterns at a private teaching hospital in kenya: implications for clinical practice.PLoS One. 2016; 11: e0147659Crossref PubMed Scopus (27) Google Scholar By contrast, the prevalence of resistant Gram-positive species was low (eg, the prevalence of meticillin-resistant Staphylococcus aureus was 6%) 6Maina D Omuse G Revathi G Adam RD Spectrum of microbial diseases and resistance patterns at a private teaching hospital in kenya: implications for clinical practice.PLoS One. 2016; 11: e0147659Crossref PubMed Scopus (27) Google Scholar. Factors leading to antimicrobial resistance vary among organisms with different ecological niches. Some organisms primarily colonise or infect humans,7Clemens JD Nair GB Ahmed T Qadri F Holmgren J Cholera.Lancet. 2017; 390: 1539-1549Summary Full Text Full Text PDF PubMed Scopus (213) Google Scholar, 8Crump JA Sjölund-Karlsson M Gordon MA Parry CM Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections.Clin Microbiol Rev. 2015; 28: 901-937Crossref PubMed Scopus (547) Google Scholar so resistance is based on human exposure to antimicrobial agents (eg, Vibrio cholerae, typhoidal Salmonella). By contrast, resistance in organisms that are primarily zoonotic, such as many of the non-typhoidal Salmonella species,8Crump JA Sjölund-Karlsson M Gordon MA Parry CM Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections.Clin Microbiol Rev. 2015; 28: 901-937Crossref PubMed Scopus (547) Google Scholar is affected by animal exposure to antimicrobial agents. In between these categories are species that are known to colonise humans but for which the relative importance of zoonotic transmission is not well understood. For example, enterohaemorrhagic E coli is generally recognised as a zoonotic infection,9Croxen MA Law RJ Scholz R Keeney KM Wlodarska M Finlay BB Recent advances in understanding enteric pathogenic Escherichia coli.Clin Microbiol Rev. 2013; 26: 822-880Crossref PubMed Scopus (845) Google Scholar and a zoonotic origin has even been suggested for urinary tract infections caused by E coli.10Jakobsen L Garneau P Bruant G et al.Is Escherichia coli urinary tract infection a zoonosis? Proof of direct link with production animals and meat.Eur J Clin Microbiol Infect Dis. 2012; 31: 1121-1129Crossref PubMed Scopus (52) Google Scholar However, the frequency of zoonotic transmission of E coli is not known, and could vary between different microbial or human populations. The work reported by Caudell and colleagues is a step towards the understanding of this cycle for E coli, but further research is required to establish when these transmitted organisms result in human disease. This complex relationship between antimicrobial use in humans and animals requires detailed regional understanding as pointed out by Caudell and colleagues.1Caudell MA Mair C Subbiah M et al.Identification of risk factors associated with carriage of resistant Escherichia coli in three culturally diverse ethnic groups in Tanzania: a biological and socioeconomic analysis.Lancet Planet Health. 2018; 2: 441-449Google Scholar A great burden of antimicrobial resistance is in low-income and middle-income countries, so it is crucial that these countries develop an internal capability for understanding the factors contributing to resistance—eg, development of clinical diagnostics11Sayed S Cherniak W Lawler M et al.Improving pathology and laboratory medicine in low-income and middle-income countries: roadmap to solutions.Lancet. 2018; 391: 1939-1952Summary Full Text Full Text PDF PubMed Scopus (92) Google Scholar with microbiological capability, whole-genome sequencing, and active anticrobial resistance surveillance systems. I declare no competing interests. Identification of risk factors associated with carriage of resistant Escherichia coli in three culturally diverse ethnic groups in Tanzania: a biological and socioeconomic analysisWhen cultural and ecological conditions favour bacterial transmission, there is a high likelihood that people will harbour antimicrobial-resistant bacteria irrespective of antimicrobial use practices. Public health interventions to limit antimicrobial resistance need to be tailored to local practices that affect bacterial transmission. Full-Text PDF Open Access