AN ASSESSMENT OF THE ANTIMICROBIAL RESISTANCE PROFILE OF ESCHERICHIA COLI ISOLATED FROM APPARENTLY HEALTHY DOMESTIC LIVESTOCK
Abstract
Background
Antimicrobial resistance (AMR) is a growing concern globally, but the impact is very deleterious in the context of Bangladesh. Recent review article on the AMR issue demonstrates the scenario in human medicine; unfortunately, no attempt was taken to address this as One Health issue. The antimicrobial resistance bacteria or genes are circulating in the fragile ecosystems and disseminate into human food chain through direct or indirect ways. In this systematic review we are exploring the mechanism or the process of development of resistance pathogen into human food chain via the domestic animal, wildlife and environmental sources in the context of One Health and future recommendation to mitigate this issue in Bangladesh.
Results
Tetracycline resistance genes were presenting in almost all sample sources in higher concentrations against enteric pathogen Escherichia coli. The second most significant antibiotics are amino-penicillin that showed resistant pattern across different source of samples. It is a matter of concerns that cephalosporin tends to acquire resistance in wildlife species that might be an indication of this antibiotic resistance gene or the pathogen been circulating in our surrounding environment though the mechanism is still unclear.
Conclusions
Steps to control antibiotic release and environmental disposal from all uses should be immediate and obligatory. There is a need for detailed system biology analysis of resistance development in-situ.
Background
Antimicrobial resistance (AMR) is one of the emerging issues globally including in low and middle-income countries (LMICs) for human health threats [1]. Primarily, AMR is the ability of a microbe to avoid the effects of an antimicrobial even though exposure to recommended doses. AMR in bacteria can be achieved by several ways including the inherent capability of natural resistance by certain bacteria, genetic mutation or acquired resistance through their surroundings [2]. Bangladesh is a developing and middle-income country in Southeast Asia (SEA) with a dense human population. The presence of diverse wildlife as well as a livestock population (cattle, sheep, goat, and poultry etc.) reservoir, has identified Bangladesh as a country where high prevalence of antibiotic resistance is documented against important pathogens in humans [3]. Developing countries such as Bangladesh are vulnerable to AMR issues for their poor surveillance health care facilities [4], unhygienic and unregulated conditions of the agriculture, livestock and aquaculture food production process, poor sanitation, widespread misuse and irrational antibiotics and prophylactics use in poultry, livestock and aquaculture industry [5]. The probiotics used in veterinary feeds contribute to the burden of antibiotic resistance bacteria (ARB) and/or antibiotic resistance genes (ARGs) in the human food chain [6]; therefore, people in the community acquiring resistance pathogens from food, environment, and wildlife sources. People affected with various illnesses (for example urinary tract infection) may not respond to the first line of drugs (such as amoxicillin, amoxiclav, ampicillin, and ciprofloxacin) available for their treatment [3]. This enhances the risk of mortality, longer duration of hospitalization and higher hospital costs. Additionally, physicians may resort to alternative drugs such as fosfomycin, nitrofurantoin, tigecycline, carbapenems [7].
Poultry production system is considered a high risk for AMR emergence in low-income settings, particularly in Bangladesh, where commercial poultry production is rapidly increasing. The majority of antimicrobial classes are used both in humans and animals (such as domestic mammals, birds, and farmed fish etc.) [8]. There are significant differences in the ways of treating companion animals (dog, cat, pet birds) compared to food-producing animals (poultry, cattle). In the case of food animals, entire flocks or pens are treated with antimicrobials through feed and water [9]. In addition, food animals exposed to long term, low dose, mass medication for the purpose of growth promotion create a favorable condition for selection and spread of resistant bacteria within and between groups of animals and humans [10]. Moreover, the non-veterinarian (popularly called Quack) prescribed antibiotics, used unwisely and unprofessionally for treating diseases in animals overwhelmed this resistance pattern.
ARB and ARGs dissemination from food producing animals to the surrounding environment niches, takes place in the excretion of antimicrobials through urine or feces onto surface waters and soils, or the application of animal manure as fertilizer to soil or ponds [11]. Untreated animal waste is used for a variety of purposes in subsistence economies like Bangladesh. Movement of food and animals has also led to the development of global dissemination of AMR.
Environmental contamination with antibiotic residues and resistant organisms/genes due to human activity has been demonstrated from pharmaceutical plants, hospital effluents and untreated wastewater, and may be a leading driver of ABR in low-resource settings [12].
Little is known about the ecology of AMR outside human and animal hosts; however, we increasingly understand that by focusing only two of these One Health compartments of the transmission circle, will result in an incomplete epidemiological background of resistance mechanism [9]. Bacterial populations are significantly diverse, both originating from aquatic and soil habitats. This poses the serious possibility of acquiring resistance capability through selection pressure from their environment which can be transmitted to humans either by direct contact with animals or food products, or indirectly via environmental pathways [9]. Recently a review article entitled “Antibiotic resistance in Bangladesh: A systemic review” has been published by AMR regarding issues in human medicine [3]. Unfortunately, no attempts have yet been made regarding the AMR issue in domestic animals, wildlife and the environment. Additionally, the human food chain is the major route of transmission of ARB and ARGs from other sources [9]. In this review, we discuss this issue systematically. The goal was to generate reference for future works and provide a recommendation to negotiate the AMR through implementing a One Health program.
Result
Demographic characteristics of different studies utilised in this review
We reviewed 45 articles that described AMR in different samples from domestic animals, wildlife, food sources (mainly originated from animal sources), environmental and insects. The majority of the articles published (53%) during the recent period (2015–2019), highlights the importance of the AMR issue in Bangladesh (Table 1). Most of the research work is based in Dhaka and surrounding cities (Mymensingh, Savar), due to the ease of both collecting samples and access to laboratories for testing.
Table 1 Characteristics of the studies included in the review (N = 45)
There are also good number of articles published based on the samples collected from other two cities (Rajshahi and Chittagong) (Table 1). The prominent source of samples were collected from live birds markets, scavenging poultry farming, commercial poultry farms and super shops or street food or restaurant (Table 1). If we consider the sample category, the most number of samples were collected from poultry including layer and broilers, pigeon [11]. There are several wildlife species that were sampled including deer, brown headed gulls, house crow, open bill stork and wild duck. There are a few studies that included wildlife environmental samples such as water bodies under the roosting site of wild birds (open bill storks) and hospital effluent wastage (house crow). Several food sources including vegetables, eggs and milk were included in several articles, in order to determine the resistance pattern against major zoonotic pathogen. Overall; 15 articles described the resistance patterns against Escherichia coli isolated from different sources of samples and there were also 12 articles for Salmonella spp. We observed that in 45 papers, they described 48 sample sources and we divided these into 5 categories. The highest number of samples (31.3%) was from food sources and 29.2% were from environmental sources. We also found similar percentages (12–15%) of samples were from domestic animals, wildlife and insect species.
Meta-analysis revealed the prevalence ofE. coli and Salmonella spp. isolated from different source of samples.
From meta-analysis, the estimated prevalence of E. coli ranged from 16.67% (95% CI: 7.24–26.1) to 95.68% (95% CI: 95.68 -89.53-101.58) with substantial heterogeneity (I2: 96.2%) in different sample categories (Fig. 1). The random effect estimated pooled prevalence was 59.24% (95% CI: 49.97–68.59). Overall, the highest prevalence of E. coli was recorded from food sources 61.77% (95% CI: 40.97–82.57) followed by insects (61%), wildlife (59.51%), environment (57.93%) and domestic animals (51.58%) (Fig. 1). Again, the estimated prevalence of Salmonella spp. ranged from 10% (95% CI: 2.41–17.59) to 91.11% (95% CI: 82.8-99.43); whereas, the heterogeneity varied from 21.07–47.06% in different sampled categories (Fig. 2). Moreover, the prevalence of salmonellosis varied from 21.07% in domestic animals and 42.36%, 45% and 47.06% in environmental, wildlife and food sources respectively.
Fig. 1
Forest plot of E. coli prevalence isolated from different samples (the center dot representing point estimates where as Gray Square representing the weight of each study to the meta-analysis)
