Antibacterial cleaning and hygiene products as an emerging risk factor for antibiotic resistance in the community

doi:10.1016/S1473-3099(03)00723-0

The Lancet Infectious Diseases

Volume 3, Issue 8, August 2003, Pages 501-506

https://doi.org/10.1016/S1473-3099(03)00723-0 Get rights and content

Summary

Antibiotic resistance within the community setting is an emerging public-health concern. Infection with antibiotic-resistant organisms in the community among people lacking traditional risk factors has been reported. In addition, prevalence studies have identified individuals carrying antibiotic-resistant organisms in the absence of known risk factors. These studies strongly suggest the presence of contributing factors that have yet to be identified. In this paper we review the burden of antibiotic resistance and known risk factors within the community setting, assess the potential role of antibacterial cleaning and hygiene products containing triclosan in the emergence of resistance, and recommend future research on the assessment of household cleaning and hygiene products containing triclosan.

Section snippets

The public-health burden of antibiotic resistance

There are two important public-health concerns surrounding infection with an antibiotic-resistant organism. First, infection with a resistant organism may cause a delay in treatment because it can take hours or even days to ascertain the resistance pattern of the infecting organism.²⁰ Second, infection with antibiotic-resistant organisms leads to treatment failure and can therefore increase transmission potential since the resistant organism is able to thrive and survive within the host for a

Known risk factors for the emergence of antibiotic resistance in the community

The primary routes by which an individual may become colonised and subsequently infected with an antibiotic-resistant organism in the community setting include person-to-person transmission of the bacteria and selective pressures from direct exposure to antibiotics (figure). For both of these routes there are established or known risk factors, such as attending day-care centres or other crowded settings, antibiotic use, and consumption of food products treated with antibiotics.

Child-care centres/crowded living conditions.

There is increased risk for the transmission of antibiotic-resistant organisms in crowded environments, a problem that is best illustrated in child-care centres. For example, the presence of antibiotic-resistant Streptococcus pneumoniae in day-care centres has been reported worldwide.24, 25, 26, 27, 28, 29 The use of broad-spectrum antibiotics among susceptible day-care age children as therapy for infections and treatment for recurring infections contributes to the presence and transmission of

Outpatient antibiotic use

Antibiotic use has been established as a risk factor for carrying a resistant organism by both individual and ecological study designs. In a study among the urban poor, individuals reporting antibiotic use in the past 12 months were significantly more likely to be colonised with MRSA.⁴ By contrast, prior antibiotic use was not associated with carriage of MRSA versus meticillin-susceptible S aureus (MSSA) in an American Indian community.³⁹ In a study among college-age women attending an

Infection and carriage of antibiotic-resistant organisms without known risk factors

Of major concern is the recent appearance of infections with MRSA in people in the community setting who lack traditional risk factors.3, 47, 48 A review by Salgado et al⁴⁹ reported that for a majority of the caMRSA studies among hospital patients, a case was defined as community-acquired if an MRSA-positive isolate was identified within 48 h of hospital admission, with or without other risk factors for MRSA. Since there are several health-care-related risk factors for carrying MRSA in the

Potential risk from antibacterial cleaning and hygiene products: changes in the susceptibility of microbial flora?

To assess the risk from antibacterial cleaning and hygiene products, it is important to ascertain the baseline prevalence of antibiotic resistance within the home environment. One small survey⁶⁰ of antibiotic resistance in flora isolated from kitchens and bathrooms of 25 households has been reported. There were no isolates of MRSA (n=51 MSSA) and four of 58 (6·9%) enterococcal isolates were resistant to vancomycin. Most (94%) Escherichia coli isolates were susceptible to ten antibiotics tested.

Recommendations

Although there has been recent growth in the use of products—such as soaps and hand lotions—that contain antibacterial ingredients, there are no guidelines or recommendations regarding the use of home hygiene products from any of the major US federal agencies, such as the Environmental Protection Agency, the Centers for Disease Control and Prevention, or Food and Drug Administration (FDA). The American Medical Association (AMA) has recently published a statement with respect to the use of

Search strategy and selection criteria

The Pubmed database was searched and English language studies only were included. Search terms for this review included: “antibiotic resistance”, “antimicrobial resistance”, “hospital”, “day care”, “military”, “agriculture”, “community acquired resistance”, “antibacterial”, “cleaning”, “hygiene”, and “triclosan”

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Exploring the resistome, virulome, mobilome and microbiome along pork production chain using metagenomics
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In order to understand and minimize microbial contaminants spread from animal to raw pork products, we explored the diversity of antibiotic resistance genes (ARGs), virulence factors (VFs), mobile genetic elements (MGEs) and the bacterial community composition in feces of pigs, processing areas as well as the end pork products in a large-scale pig slaughterhouse in China using metagenomics. The abundance and diversity of microbial community was higher in arrival and slaughtering room area and decreased sharply in the end pork products. Furthermore, the relative abundance of some clinically relevant pathogens and opportunity pathogens were greater in the end pork products and cutter samples. We identified 1412 subtypes of ARGs related to 30 antibiotic classes, in which ARGs related to multidrug resistance and β-lactamase were dominant. Resistance determinants to clinically critical important antibiotics, including sequences related to mcr, optrA, poxtA, tetX and β-lactamase genes (i.e. bla_OXA, bla_VIM, bla_IMP, bla_GES, bla_NDM, bla_KPC and bla_SME) were detected. More than 42 general virulence features, mainly adherence, secretion system, iron uptake, toxin, antiphagocytosis and immune evasion, were identified. A total of 1922 types of MGEs, mainly plasmids were observed. Most of the ARGs are predicted to be associated with MGEs. The prevalence of ARGs, VFs and MGEs decreased over subsequential processing steps. Most of the remaining ARGs, VFs and MGEs in end pork products were also present on other samples, indicating the flow of these genes through the production line. These results broaden our understanding of the global ARGs, VFs and MGEs diversity along the pork production chain, with the suggestion of implementing improved control measures to reduce the risk of spread of pathogenic bacteria and their associated resistome, virulome and mobilome from animal to the food chain and the surrounding environment.
Association of antimicrobial usage with faecal abundance of aph(3’)-III, ermB, sul2 and tetW resistance genes in veal calves in three European countries
2020, International Journal of Antimicrobial Agents
High antimicrobial use (AMU) and antimicrobial resistance (AMR) in veal calves remain a source of concern. As part of the EFFORT project, the association between AMU and the abundance of faecal antimicrobial resistance genes (ARGs) in veal calves in three European countries was determined.
In 2015, faecal samples of veal calves close to slaughter were collected from farms located in France, Germany and the Netherlands (20 farms in France, 20 farms in the Netherlands and 21 farms in Germany; 25 calves per farm). Standardized questionnaires were used to record AMU and farm characteristics. In total, 405 faecal samples were selected for DNA extraction and quantitative polymerase chain reaction to quantify the abundance (16S normalized concentration) of four ARGs [aph(3’)-III, ermB, sul2 and tetW] encoding for resistance to frequently used antimicrobials in veal calves. Multiple linear mixed models with random effects for country and farm were used to relate ARGs to AMU and farm characteristics.
A significant positive association was found between the use of trimethoprim/sulfonamides and the concentration of sul2 in faeces from veal calves. A higher weight of calves on arrival at the farm was negatively associated with aph(3’)-III and ermB. Lower concentrations of aph(3’)-III were found at farms with non-commercial animals present. Furthermore, farms using only water for the cleaning of stables had a significantly lower abundance of faecal ermB and tetW compared with other farms.
A positive association was found between the use of trimethoprim/sulfonamides and the abundance of sul2 in faeces in veal calves. Additionally, other relevant risk factors associated with ARGs in veal calves were identified, such as weight on arrival at the farm and cleaning practices.
Efficient multiresidue determination method for 168 pharmaceuticals and metabolites: Optimization and application to raw wastewater, wastewater effluent, and surface water in Beijing, China
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New analytical methods are needed to efficiently measure the growing list of priority pharmaceuticals in environmental samples. In this regard, a rapid, sensitive, and robust method was developed for quantitation of 168 pharmaceuticals and pharmaceutical metabolites using solid-phase extraction (SPE) and liquid chromatography with tandem mass spectrometry. The extraction protocol and instrumental efficiency were specifically addressed to increase analytical workload and throughput. The optimized protocols, which are five times more efficient than US EPA Method 1694, enabled analyte recoveries that ranged from 77% to 117% for 162 analytes with method quantitation limits (MQLs) as low as 0.1 ng L⁻¹. To verify the suitability of the improved analytical method for environmental samples, 24-h composite samples of raw wastewater and wastewater effluent, along with downstream surface water, were analyzed. Overall, 143/168 target compounds were identified in at least one of the samples, and 130/168 analytes were present at concentrations above their MQLs. The total mass concentration of the measured analytes decreased by 93% during wastewater treatment. The analyte concentrations in the wastewater effluent were comparable to those measured in surface water 1 km downstream of the wastewater discharge point. Ultimately, the comprehensive method will serve as an important tool to inform the occurrence, fate, transport, and toxicity of a large suite of priority pharmaceuticals and pharmaceutical metabolites in natural and engineered systems.
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Aquatic ecosystems harbor a vast pool of antibiotic resistance genes (ARGs), which can suffer mutation, recombination and selection events. Here, we explored the diversity of ARGs, virulence factors and the bacterial community composition in water samples before (surface raw water, RW) and after (disinfected water, DW) drinking water conventional treatment, as well as in tap water (TW) and ultrafiltration membranes (UM, recovered from hemodialysis equipment) through metagenomics. A total of 852 different ARGs were identified, 21.8% of them only in RW, which might reflect the impact of human activities on the river at the sampling point. Although a similar resistance profile has been observed between the samples, significant differences in the frequency of clinically relevant antibiotic classes (penam and peptide) were identified. Resistance determinants to last resort antibiotics, including sequences related to mcr, optrA and poxtA and clinically relevant beta-lactamase genes (i.e. bla_KPC, bla_GES, bla_IMP, bla_VIM, bla_SPM and bla_NDM) were detected. 830 coding sequences (CDSs - related to 217 different ARGs) were embedded in contigs associated with mobile genetic elements, specially plasmids, of which 68% in RW, DW and TW, suggesting the importance of water environments in resistance dissemination. Shifts in bacterial pathogens genera were observed, such as a significant increase in Mycobacterium after treatment and distribution. In UM, the potentially pathogenic genus Halomonas predominated. Its draft genome was closely related to H. stevensii, hosting mainly multidrug efflux pumps. These results broaden our understanding of the global ARGs diversity and stress the importance of tracking the ever-expanding environmental resistome.
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ReviewAntibacterial cleaning and hygiene products as an emerging risk factor for antibiotic resistance in the community

Summary

Section snippets

The public-health burden of antibiotic resistance

Known risk factors for the emergence of antibiotic resistance in the community

Child-care centres/crowded living conditions.

Outpatient antibiotic use

Infection and carriage of antibiotic-resistant organisms without known risk factors

Potential risk from antibacterial cleaning and hygiene products: changes in the susceptibility of microbial flora?

Recommendations

Search strategy and selection criteria

Am J Infect Control

Am J Infect Control

Am J Infect Control

Prog Lipid Res

J Hosp Infect

Curr Opin Microbiol

J Biol Chem

J Biol Chem

FEMS Microbiol Lett

Am J Infect Control

FEMS Microbiol Lett

Am J Infect Control

Lancet

J Hosp Infect

Clin Microbiol Infect

J Hosp Infect

Lancet Infect Dis

Epidemiological factors influencing the emergence of antimicrobial resistance

Ciba Found Symp

Introduction

Clin Infect Dis

Methicillin-resistant Staphylococcus aureus in two child care centers

J Infect Dis

Population-based community prevalence of methicillin-resistant Staphylococcus aureus in the urban poor of San Francisco

Clin Infect Dis

Community-acquired methicillin-resistant Staphylococcus aureus colonisation in healthy children attending an outpatient pediatric clinic

Pediatr Infect Dis J

Methicillin-resistant and borderline methicillin-resistant asymptomatic Staphylococcus aureus colonisation in children without identifiable risk factors

Pediatr Infect Dis

Antibiotic and antiseptic resistance: impact on public health

Pediatr Infect Dis J

Antibacterial household products: cause for concern

Emerg Infect Dis

Triclosan and antibiotic resistance in Staphylococcus aureus

J Antimicrob Chemother

Triclosan targets lipid synthesis

Nature

A triclosan-resistant bacterial enzyme

Nature

Isoniazid affects multiple components of the type II fatty acid synthase system of Mycobacterium tuberculosis

Mol Microbiol

Inhibition of InhA, the enoyl reductase from Mycobacterium tuberculosis, by triclosan and isoniazid

Biochemistry

Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ

Antimicrob Agents Chemother

The MexJK efflux pump of Pseudomonas aeruginosa requires OprM for antibiotic efflux but not for efflux of triclosan

J Bacteriol

Epidemiology of drug resistance: implications for a post-antimicrobial era

Science

Interactions among strategies associated with bacterial infection: pathogenicity, epidemicity, and antibiotic resistance

Clin Microbiol Rev

Containing antimicrobial resistance: review of the literature and report of a WHO Workshop on the Development of a Global Strategy for the Containment of Antimicrobial Resistance$. $WHO/CDS/CSR/DRS/99.2

Excess mortality associated with antimicrobial drug-resistant Salmonella typhimurium

Emerg Infect Dis

Drug-resistant Streptococcus pneumoniae in day–care centres in Stockholm County

J Infect

Marked differences in pneumococcal carriage and resistance patterns between day care centers located within a small area

Clin Infect Dis

Colonization with penicillin-nonsusceptible Streptococcus pneumoniae in urban and rural child-care centers

Pediatr Infect Dis J

The spread of multiply resistant Streptococcus pneumoniae at a day care center in Ohio

J Infect Dis

Previous antibiotic consumption and other risk factors for carriage of penicillin-resistant Streptococcus pneumoniae in children

Eur J Clin Microbiol Infect Dis

Prevalence of carriage of antimicrobial resistant strains of Streptococcus pneumoniae in primary school children in Hong Kong

Epidemiol Infect

High rates of multiple antibiotic resistance in Streptococcus pneumoniae from healthy children living in isolated rural communities: association with cephalosporin use and intrafamilial transmission

Pediatrics

National Department of Defense Surveillance for Invasive Streptococcus pneumoniae: antibiotic resistance, serotype distribution, and arbitrarily primed polymerase chain reaction analyses

Review
Antibacterial cleaning and hygiene products as an emerging risk factor for antibiotic resistance in the community