Abstract
Understanding the burden of antibiotic resistance globally is hindered by incomplete surveillance, particularly across low-resource settings. The Antibiotic Resistance in Communities and Hospitals (ARCH) consortium encompasses sites across 6 resource-limited settings and is intended to address these gaps. Supported by the Centers for Disease Control and Prevention, the ARCH studies seek to characterize the burden of antibiotic resistance by examining colonization prevalence at the community and hospital level and to evaluate for risk factors that are associated with colonization. In this supplement, 7 articles present results from these initial studies. Though future studies identifying and evaluating prevention strategies will be critical to mitigate spreading resistance and its impact on populations, the findings from these studies address important questions surrounding the epidemiology of antibiotic resistance.
Keywords: antibiotic resistance, colonization, health outcomes, epidemiologic trends
In 2022, the first global estimate of the burden of antimicrobial resistance (AMR) revealed that AMR is the leading cause of infectious disease-related deaths [1]. Moreover, the report showed that the greatest burden of AMR deaths occurs in low- and middle-income countries (LMICs). Although the report provides key insights into the epidemiology of AMR, the modeled estimates for LMICs are largely based upon sparse data that are highly impacted by variation in utilization of both healthcare and diagnostics, limiting the ability to act locally on AMR data from specific regions or countries. High rates of AMR in LMICs have been attributed to a wide range of factors, including inappropriate use of antibiotics, inadequate sanitation, overcrowding, and insufficient infection prevention and control practices [2, 3]. However, these factors fail to explain variability in AMR colonization risk between individuals living in the same communities.
The US Centers for Disease Control and Prevention (CDC) supports the Antibiotic Resistance in Communities and Hospitals (ARCH) research consortium, a part of the Global Antimicrobial Resistance Laboratory and Response Network (www.cdc.gov/drugresistance/ar-lab-networks/global.html). The ARCH consortium is designed to improve the detection of and response to healthcare-associated AMR in humans. The published ARCH studies represent findings across resource-limited settings in 6 countries: Bangladesh, India, Kenya, Botswana, Chile, and Guatemala [4]. These studies sought to assess colonization with 4 clinically important pathogens: extended-spectrum cephalosporin-resistant Enterobacterales (ESCrE), carbapenem-resistant Enterobacterales (CRE), colistin-resistant Enterobacterales (ColRE), and methicillin-resistant Staphylococcus aureus (MRSA). Using colonization data collected through active surveillance, these studies characterized the burden of AMR across LMICs while overcoming many of the biases that are intrinsic to surveillance systems built around identifying AMR in passively collected clinical isolates [5]. The studies have also begun exploring factors associated with AMR colonization to identify drivers of AMR in community and hospital settings [4].
Understanding risk factors for AMR colonization is important from both a population and an individual healthcare perspective. Colonized individuals can spread resistant organisms to others, challenging population- and healthcare facility-level control. Furthermore, AMR colonization increases risk for subsequent infections with those organisms among hospitalized individuals [6, 7] and community dwellers [8]. This has led to studies targeting decolonization as a risk reduction strategy, employing diverse approaches from topical antimicrobials to fecal microbiota transplantation [9]. Identifying risk factors for colonization provides an opportunity to intervene prior to the widespread development of difficult-to-treat infections.
The ARCH studies provide insight into the prevalence and drivers of AMR colonization, while highlighting unique regional differences. Despite slight differences in methodologies (Table 1), trends were observed along with notable differences by subgroup (Table 2). Surprisingly, colonization with ESCrE was common in both community and hospital settings; prevalence varied widely, ranging from 29% in the community in Chile to 82% in hospitals in India and Bangladesh [10–12]. This contrasts with studies from high-income countries (HICs) showing much lower colonization with extended-spectrum beta-lactamase–producing Enterobacterales, reflecting overall increasing global trends, but a growing dichotomy between HICs and LMICs [13, 14]. Although CRE colonization was less common than ESCrE colonization, the ARCH studies are among the first to demonstrate CRE colonization in communities underscoring the concerning expansion of CRE reservoirs beyond healthcare facilities.
Table 1.
Enrollment Characteristics Across Antibiotic Resistance in Communities and Hospitals (ARCH) Study Sites
| Country | Study Site | Participants | Specimens Collected |
|---|---|---|---|
| Bangladesh (Enrollment: April to October 2019; pre-COVID-19) | |||
| Community | Dhaka (urban) | Adults (≥ 18 y) without fever, diarrhea, or cough | Stool Nasal swab |
| Hospital | Dhaka (1 tertiary public hospital + 2 private hospitals) | Adults (≥ 18 y) without neutropenia or gastrointestinal bleeding | Stool Nasal swab |
| India (Enrollment: November 2020 to March 2022; during COVID-19) | |||
| Community | Chennai (semi-urban) | Adults (≥ 18 y) without fever, diarrhea, or cough | Stool |
| Hospital | Chennai (2 secondary level hospitals) | Adults (≥ 18 y) without diarrhea, neutropenia, or gastrointestinal bleeding | Stool |
| Kenya (Enrollment: January 2019 to March 2020; pre-COVID-19) | |||
| Community |
|
Adults (≥ 18 y) and children (<5 y) without fever, diarrhea, or cough | Rectal swab Nasal swab |
| Hospital |
|
All ages without neutropenia or gastrointestinal bleeding | Rectal swab Nasal swab |
| Botswana (Enrollment: January to September 2020, except April-May; during COVID-19) | |||
| Community |
|
All ages | Rectal swab |
| Hospital |
|
Adults (≥ 18 y) able to consent and undergo rectal swabbing | Rectal swab |
| Outpatient clinic |
|
Adults (≥ 18 y) | Rectal swab |
| Guatemala (Community enrollment: November 2019 to March 2020, July to October 2021; Hospital enrollment: March to September 2021; during COVID-19) | |||
| Community | Quetzaltenango (urban, rural) | All ages without fever, diarrhea, cough, or COVID-19 | Stool |
| Hospital | Quetzaltenango (1 tertiary hospital) | All ages without gastrointestinal bleeding, neutropenia, or COVID-19 | Stool |
| Chile (Enrollment: December 2018 to May 2019; pre-COVID-19) | |||
| Community | Molina (semi-rural) | Adults (38–74 y) without fever, diarrhea, or respiratory symptoms | Stool |
| Hospital |
|
Adults (≥ 16 y) without diarrhea or gastrointestinal bleeding | Rectal swab |
Sources: Chowdhury F, Mah-E-Muneer S, Bollinger S, et al. Prevalence of Colonization with Antibiotic-Resistant Organisms in Hospitalized and Community Individuals in Bangladesh, A Phenotypic Analysis: Findings from the Antibiotic Resistance in Communities and Hospitals (ARCH) Study Clinical Infectious Diseases 2023: 77(Suppl 1):S118–24; Kumar CPG, Bhatnagar T, Narayanan G S, et al. High-level colonization with Antibiotic-Resistant Enterobacterales among individuals in a semi-urban setting in South India: an Antibiotic Resistance in Communities and Hospitals (ARCH) study Clinical Infectious Diseases 2023: 77(Suppl 1):S111–7; Ita T, Luvsansharav UO, Smith RM, et al. Prevalence of colonization with multidrug-resistant bacteria in communities and hospitals in Kenya. Sci Rep 2022; 12(1): 22290; Mannathoko N, Mosepele M, Gross R, et al. Colonization with extended-spectrum cephalosporin-resistant Enterobacterales (ESCrE) and carbapenem-resistant Enterobacterales (CRE) in healthcare and community settings in Botswana: an antibiotic resistance in communities and hospitals (ARCH) study. Int J Infect Dis 2022; 122: 313–20; Ramay BM, Castillo C, Grajeda L, et al. Colonization with antibiotic-resistant bacteria in a hospital and associated communities in Guatemala: An Antibiotic Resistance in Communities and Hospitals (ARCH) Study. Clinical Infectious Diseases 2023: 77(Suppl 1):S82–8; Araos R, Smith RM, Styczynski A, et al. High burden of intestinal colonization with antimicrobial resistant bacteria in Chile: An Antibiotic Resistance in Communities and Hospitals (ARCH) study. Clinical Infectious Diseases 2023: 77(Suppl 1):S75–81.
Abbreviation: COVID-19, coronavirus disease 2019.
Table 2.
Prevalence of Colonization With Multidrug-Resistant Organisms
| Site | Target Organism | Prevalence Estimate, % (95% CI)a | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Bangladesh | India | Kenya | Botswana | Guatemala | Chileb | |||||
| Community | ESCrE | 78 (73–83) | 72 (68–75) | Urban | 52 (48–56) | Adults | 24 (21–28) | Adults | 50 (44–56) | 29 (24–34) |
| Rural | 45 (41–49) | Children | 26 (23–30) | Children | 37 (28–48) | |||||
| CRE | 9 (6–13) | 15 (13–18) | Urban | 1 (1–3) | Adults | 0 (0–1) | … | 1 (0–2) | 6 (3–8) | |
| Rural | 1 (0–2) | Children | 1 (0–2) | |||||||
| CoIRE | 11 (8–14)c | 1 (1–2)d | … | … | … | … | … | … | … | |
| MRSA | 22 (19–26) | … | Urban | 2 (1–3) | … | … | … | … | … | |
| Rural | 1 (0–2) | |||||||||
| Hospital | ESCrE | 82 (79–85) | 82 (78–85) | Urban | 70 (65–74) | … | 43 (38–47) | Adults | 72 (65–78) | 41 (38–45) |
| Rural | 63 (58–67) | Children | 65 (56–75) | |||||||
| Infants | 60 (51–68) | |||||||||
| CRE | 37 (34–41) | 23 (19–26) | Urban | 17 (13–21) | … | 7 (5–10) | Adults | 40 (32–47) | 15 (12–17) | |
| Rural | 7 (5–9) | Children | 29 (19–38) | |||||||
| Infants | 37 (28–46) | |||||||||
| ColRE | 7 (6–10)c | 1 (0–2)d | … | … | … | … | … | … | … | |
| MRSA | 21 (18–24) | … | Urban | 3 (2–5) | … | … | … | … | … | |
| Rural | 3 (2–5) | |||||||||
| Outpatient clinic | ESCrE | … | … | … | … | … | 31 (28–34) | … | … | … |
| CRE | … | … | … | … | … | 1 (0–2) | … | … | … | |
Sources: Chowdhury F, Mah-E-Muneer S, Bollinger S, et al. Prevalence of Colonization with Antibiotic-Resistant Organisms in Hospitalized and Community Individuals in Bangladesh, A Phenotypic Analysis: Findings from the Antibiotic Resistance in Communities and Hospitals (ARCH) Study Clinical Infectious Diseases 2023: 77(Suppl 1):S118–24; Kumar CPG, Bhatnagar T, Narayanan G S, et al. High-level colonization with Antibiotic-Resistant Enterobacterales among individuals in a semi-urban setting in South India: an Antibiotic Resistance in Communities and Hospitals (ARCH) study Clinical Infectious Diseases 2023: 77(Suppl 1):S111–7; Ita T, Luvsansharav UO, Smith RM, et al. Prevalence of colonization with multidrug-resistant bacteria in communities and hospitals in Kenya. Sci Rep 2022; 12(1): 22290; Mannathoko N, Mosepele M, Gross R, et al. Colonization with extended-spectrum cephalosporin-resistant Enterobacterales (ESCrE) and carbapenem-resistant Enterobacterales (CRE) in healthcare and community settings in Botswana: an antibiotic resistance in communities and hospitals (ARCH) study. Int J Infect Dis 2022; 122: 313–20; Ramay BM, Castillo C, Grajeda L, et al. Colonization with antibiotic-resistant bacteria in a hospital and associated communities in Guatemala: An Antibiotic Resistance in Communities and Hospitals (ARCH) Study. Clinical Infectious Diseases 2023: 77(Suppl 1):S82–8; Araos R, Smith RM, Styczynski A, et al. High burden of intestinal colonization with antimicrobial resistant bacteria in Chile: An Antibiotic Resistance in Communities and Hospitals (ARCH) study. Clinical Infectious Diseases 2023: 77(Suppl 1):S75–81.
Abbreviations: CI, confidence interval; ColRE, colistin-resistant Enterobacterales; CRE, carbapenem-resistant Enterobacterales; ESCrE, extended-spectrum cephalosporin-resistant Enterobacterales; MRSA, methicillin-resistant Staphylococcus aureus.
All sites used selective agars followed by confirmatory identification and antibiotic susceptibility testing. Slight variations in definitions were applied between the sites.
Prevalence estimates from Chile are based on resistance to extended-spectrum cephalosporins and carbapenems among all recovered gram-negative bacteria, not just Enterobacterales.
Identified based only on Vitek results.
Identified based on broth microdilution for isolates with Vitek minimum inhibitory concentrations (MICs) ≥4 and a subset with MICs ≤2.
Prevalence of colonization with both ESCrE and CRE was generally found to be higher in hospitals than communities across ARCH sites. Similarly, multidrug resistance among ESCrE and CRE isolates was more commonly observed in hospital participants. This may be expected given the greater intensity of antibiotic use and risk for nosocomial transmission within hospitals. However, in both Bangladesh and India, ESCrE colonization was similar among hospital and community participants, demonstrating a blurring of the community-hospital divide [11, 12]. This may be in part related to enrollment early during hospitalization demonstrating the need to explore colonization over longer hospital stays. Additionally, there was substantial variation between hospitals in Chile, Kenya, and Botswana, demonstrating that both population- and facility-level factors impact AMR [10, 15, 16]. Given the extent of colonization among community participants, researchers and public health practitioners should focus on community risk factors and mitigation measures along with those in healthcare facilities to truly combat the scourge of AMR.
The coronavirus disease 2019 (COVID-19) pandemic led to worldwide increases in AMR among clinical infections [17–20]. The longitudinal nature of enrollment in the ARCH studies gave investigators in Botswana and Guatemala the ability to assess the impact of the COVID-19 pandemic on AMR colonization. In Botswana, ESCrE and CRE colonization decreased in the early months of the pandemic, following a country-wide lockdown [15]. No changes in colonization prevalence were observed later in the pandemic in Guatemala; however, there were significant decreases in self-reported illness and antibiotic use among participants enrolled during the pandemic [21]. Established research consortia, like ARCH, provide the infrastructure to evaluate critical population-level changes and can be leveraged when large secular changes that disrupt public health mitigation measures occur. This allows for natural experiments regarding the spread of AMR that would be difficult to recreate in a purely research environment.
Risk factor analyses detected notable commonalities across ARCH sites. In Kenya and Botswana, animal contact and healthcare exposure were both risk factors for community colonization [22, 23]. Contact with poultry in Kenya and larger livestock in Botswana were associated with ESCrE colonization. These exposures are likely related to antibiotic use in animal husbandry and animal colonization. Kenya and Botswana also identified increased risk of colonization across a range of inpatient and outpatient healthcare exposures [23, 24]. Although inpatient healthcare facilities are well-described amplifiers of AMR, how outpatient healthcare contact contributes to exposure to AMR organisms and acquisition of colonization is less understood. Given these observations and the alarming prevalence of AMR across settings, additional investigations to elucidate transmission pathways at the healthcare-community interface are warranted.
In addition to raising questions around the risk of outpatient healthcare contact, these studies reveal interesting insights into the relationship between antibiotic use and AMR colonization. All sites recorded antibiotic use in the prior 14 days for hospitalized participants and 3 months for community participants (except for Guatemala, which recorded only the prior 30 days for the community), although the association between antibiotic use and colonization has only been explored in Botswana and Kenya to date [22, 23]. The lack of association between ESCrE colonization and antibiotic exposure in the community, seen in both Botswana and Kenya, may suggest 1 or more possible explanations: (1) organisms with specific resistant phenotypes are overcoming “evolutionary hurdles,” attaining the ability to colonize individuals in the community without antibiotic-mediated microbiome disruption; (2) abundant selective pressures are present, such as subtherapeutic antibiotic and biocide residues in the environment, that persistently perturb the human microbiome, reducing colonization resistance; or (3) frequent exposures from a highly contaminated environment lead to successive, transient colonization. Exploring similar relationships across the other ARCH sites may provide further insights into how antibiotic use is or is not mediating colonization across low-resource settings where other factors may be exerting greater selective pressures.
In summary, these initial findings provide insights into the burden of AMR in LMICs and generate urgent questions about the molecular ecology that leads to the emergence and circulation of antibiotic resistance genes between populations at local, regional, and global levels. The consortium’s work will continue to address these questions with studies utilizing whole genome sequencing to further characterize microbial dynamics. Additional investigations are underway to elucidate the interplay between the microbiome and colonization and to capture longitudinal data on persistence/transience of colonization. However, 1 aspect missing from the current landscape of colonization research is similar population-based community prevalence estimates from western HICs. Much could be learned if such studies were performed using similar methods and compared to ARCH data. Additionally, although ARCH-like studies of colonization are resource intensive and most frequently done in research settings, incorporating estimates of colonization into existing global efforts to surveil for AMR, such as those spearheaded by the World Health Organization Global Antimicrobial Resistance and Use Surveillance System, could provide support for routine evaluation of colonization as a metric by which to measure AMR burden and emergence.
Footnotes
Disclaimer. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.
Supplement sponsorship. This article appears as part of the supplement “The Evolving Challenges of Antibiotic Resistance in Low- and Middle-Income Countries: Priorities and Solutions,” sponsored by the U.S. Centers for Disease Control and Prevention, and Health Security Partners.
Potential conflicts of interest. The authors: No reported conflicts of interest. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.
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