Escherichia coli Isolated from Migratory Birds: History
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Subjects: Health Care Sciences & Services
Contributor:
Md. Tanvir Rahman

Antibiotic resistance is a global health crisis. Migratory birds are carriers of various types of pathogens including multidrug  Escherichia coli. However, their roles in the dissemination of these resistant pathogens are still being neglected in Bangladesh. MDR E. coli carried by many of these migratory birds could also be positive for APEC-associated virulence genes, which can seriously contribute to the development of human and animal diseases. 

  • migratory birds
  • E. coli
  • virulence
  • APEC
  • MDR
  • environment
  • public health

1. Introduction

There are over 10,000 known species of birds that are distributed globally [1]. Birds can travel long distances between countries and across continents. Bangladesh is located in the subtropical region and thus has milder winters than in the northern hemisphere. During the winter season, migratory birds travel to Bangladesh, and inhabit suitable water bodies such as ponds, lakes, and rivers. Migratory birds are known to be involved in the transmission and spread of human and animal pathogens such as bacteria, viruses, fungi, archaea, and parasites as healthy carriers or as hosts of infected vectors [2][3]. Several studies revealed the transmission patterns of bacterial pathogens to aquatic environment from migratory birds [4][5]. Importantly, bacterial pathogens can be transmitted to humans, animals, and poultry by ducks and duck-like birds from water bodies contaminated by fecal matter of migratory birds. In addition, people dwelling around water bodies where migratory birds take rest, may come in contact with contaminated water that they may try to use for household or agricultural purposes. Furthermore, when people usually use contaminated water for dairy or poultry farming, bacterial pathogens can be transmitted to other humans and animals.
Among the different bacteria transmitted by migratory birds, Escherichia coli are important commensal avian and human pathogens that exist as part of the microbiota of the intestinal tract of avian species [6]. Pathogenic E. coli can infect the respiratory tract, urinary tract, and bloodstream of humans and animals [7]. Strikingly, more than 80% of urinary tract infections in humans are caused by this microorganism [8].
Avian pathogenic E. coli (APEC) causes avian colibacillosis in poultry, which is an infectious disease that negatively impacts the poultry sector [9]. It causes yolk sac infections, pericarditis, synovitis, peritonitis, osteomyelitis, and salpingitis in poultry [10]. The disease has been associated with several virulence genes, including fimC, fimH, papC, iss, stx1, stx2, tss, cvi, and iucD [10][11][12][13]. Virulence factors include invasins, adhesins, protectins, iron acquisition systems, and toxins and are crucial for invasion, colonization, and adherence of the pathogen to the surface of respiratory tract, its resistance mechanisms, its ability to multiply under iron-restricted situation, and its cytotoxic effects [10][14]. Among virulence genes, fimC (Type 1 fimbriae C) is responsible for adherence and colonization on epithelial cells, iucD (iron-uptake systems of E. coli D) is responsible for iron-acquisition, and papC (pyelonephritis-associated pili C) is responsible for bacterial adhesion [10]. The number and combination of virulence genes associated with APEC determine its overall virulence [15].
APEC infections are zoonotic in nature and have phylogenic similarities with uropathogenic E. coli (UPEC) that causes urinary tract infections and with neonatal meningitis E. coli that causes neonatal meningitis in humans [16][17]. In addition, these strains can share virulence factors by transmitting virulence genes and plasmids [16]. Furthermore, APEC in meat of healthy birds can be transmitted to humans via the food chain leading to extraintestinal diseases and other diseases [18].
Antimicrobial resistance (AMR) is a serious global problem that jeopardizes human, animal, and environmental health. If not contained by 2050, AMR is estimated to cause hundreds of millions of human deaths, severe financial losses, and a significant fall in livestock production [19]. The impact will be severe in low- and middle-income countries (LMICs) in Africa and Asia including Bangladesh. Migratory birds can spread antibiotic resistant pathogens over long distances to remote locations and can act as reservoirs of antibiotic-resistant bacteria [20][21][22]. They have been recognized as an important source for the environmental dissemination of AMR [21][23][24]. Multidrug resistant (MDR) E. coli has been from migratory birds in different parts of the world [25][26][27][28]. Fecal transmission of MDR E. coli from migratory birds to water bodies in different areas has been reported [29][30].
AMR has been extensively studied in humans, livestock, and poultry. There has been less focus on AMR in non-typical hosts such as in migratory birds and significant gaps of knowledge do exist. MDR E. coli has been reported in migratory birds in Bangladesh [25]. However, to the best of our knowledge, there is no data on virulence determinants of MDR E. coli associated with the APEC pathotype in Bangladesh. In this study, we assessed the hypothesis that APEC-associated virulence determinants exist in the microbiota of migratory birds travelling to Bangladesh. In addition to the isolation and identification of the virulence determinants, we assessed multidrug resistance in these migratory birds.

2. Current Insights

Migratory birds contribute to the circulation and dissemination of different bacteria including E. coli. As an enteric microorganism, pathogenic E. coli can cause both human and animal diseases and is known to develop antimicrobial resistance [31]. Since migratory birds can spread antibiotic-resistant E. coli during migration, we investigated fecal matter of migratory birds to identify APEC-associated virulence genes.
The 83.33% (55/66) prevalence rate of E. coli in migratory birds was close to the prevalence rate of a study in Portugal (85.7%) [23], but higher than prevalence rates reported in other studies in Bangladesh [25][32], Czech Republic [33], Egypt [34], Northern Italy (33.9%) [35], and Italy (24.31%) [36]. On the other hand, the prevalence rate was lower than the prevalence rate reported in a study in Saudi Arabia (94%) [26]. These variations can be due to the variations in detection methods, geographical and seasonal distribution, sample sizes, and types and species of migratory birds. In addition, stressful conditions that migratory birds experience during migration may impact the shedding rate of bacteria [37]. The detection of E. coli in the fecal samples of the migratory birds is not unusual because of commensal nature of this organism in the intestines of humans, animals, and avian species. In addition, migratory birds usually occupy variegated ecological niches and adapt varying feeding patterns during their different forms of migration. During these migrations, birds can host E. coli and contribute to its transmission from one place to another.
This is the first study to detect virulence determinants of MDR E. coli associated with the APEC pathotype from migratory birds in Bangladesh. Virulence genes are pivotal for the detection of any pathogenic microorganisms [38]. In the present study, 69.09% (38/55) E. coli isolates were positive for at least one or more virulence genes. Among them, the three tested virulence genes (fimC, iucD, and papC) were present together in only three isolates. However, the prevalence of the fimC (67.27%) gene was higher than iucD (29.09%) and papC (5.45%) genes. In addition, there was a significant correlation between fimC and iucD genes; but none with the papC gene. Previous studies reported the detection of APEC-associated virulence genes from migratory birds in Italy and Slovakia [39][40]. Both fimC (a chaperone-like periplasmic protein) and papC allow E. coli to adhere to host cells [41]. The iucD gene contributes to APEC pathogenesis through an iron-acquisition system and the mediation of aerobactin synthesis [42]. As APEC colonizes its avian hosts, it can spread through the fecal route to the environment potentially threatening humans, animals, and other avian hosts [14]. Furthermore, biological and environmental stress factors can compound the APEC’s threat to the livestock and human population [43].
It is noteworthy that APEC-associated virulence genes isolated from migratory birds in this study have been previously detected in humans and wild mammals [44]. Thus, migratory birds can act as potential reservoirs for antibiotic-resistant APEC which, due to its zoonotic nature, can spread from these birds to the human population [17][22][45]. In line with earlier studies [45][46], we detected multidrug resistance in the isolated E. coli. All the E. coli isolates exhibited very high resistance against ampicillin and erythromycin, in addition to different levels of resistance against streptomycin, tetracycline, ciprofloxacin, and chloramphenicol. Previous studies reported resistance in E. coli isolated from migratory birds against ampicillin, ciprofloxacin, chloramphenicol, tetracycline, streptomycin, gentamicin [26][28][33][36][47]. Notably, colistin-resistant and meropenem-resistant E. coli have also been detected in this study. Colistin is in the reserve group of antibiotics and its detection in isolated E. coli is alarming. In addition, meropenem is from the carbapenem group which is typically used for the treatment of serious infections in humans only. Migratory birds might have obtained these resistant isolates from an environment contaminated with human secretions or excretions. Further studies at the molecular level need to be conducted to follow up on this finding.
This study reported significant positive correlations (p < 0.05) between the resistance profiles of ciprofloxacin and tetracycline, chloramphenicol and ciprofloxacin, chloramphenicol and tetracycline, and streptomycin and tetracycline; significant inverse correlations were observed in between colistin and ciprofloxacin, colistin and tetracycline, meropenem and ciprofloxacin, chloramphenicol and colistin, and streptomycin and colistin. The significant correlations observed between antimicrobials might be related to the haphazard use of antibiotics in animals and poultry in areas inhabited by the migratory birds. Cross-contamination of the environment, such as the water bodies, might also have played a role.
It is worth mentioning that all the E. coli isolates from migratory birds in this study were MDR in nature. The detection of MDR E. coli from the migratory birds is not uncommon. Previously, Hasan et al. [25] reported MDR E. coli in fecal samples of migratory birds in Bangladesh. Similar observations have also been made in other parts of the world [26][28]. Our findings leave open the possibility of long-distance transmissions of MDR bacteria from their original habitats to far locations, which can be very alarming, especially if the transmission was to areas in which the public has not been educated about infectious disease control and prevention [48]. The transmission of resistant E. coli from livestock to wild birds has previously been reported [49]. It is likely to occur in Bangladesh as people tend to keep their animals and poultry near water bodies where interaction with migratory birds is possible. Antimicrobial resistant E. coli has also been detected in wild mammals [50][51].
Aquatic environments are considered to be hotspots for the transmission of antibiotic-resistant bacteria such as E. coli [52]. Along this line, previous studies reported that ducks, which live near water bodies, can transmit antibiotic-resistant bacteria [53][54]. Since migratory birds carrying antibiotic-resistant E. coli inhabit water bodies, they might be contributing to the dissemination of antibiotic-resistant E. coli through fecal matter to the surrounding aquatic environments, which can jeopardize human and animal health directly or indirectly. One major area of concern is if the resistant bacteria gain entry into the human food chain. Given all the above, it will be important to control and prevent the spread of antibiotic-resistant bacteria from migratory birds to humans, animals, and other poultry.

This entry is adapted from the peer-reviewed paper 10.3390/antibiotics10020190

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