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.

In this study, we 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.