Prevalence and risk factors of antimicrobial resistance patterns of Staphylococcus spp. and E. coli in rodents and shrews at human-animal interfaces in Chattogram, Bangladesh

Abstract

Antimicrobial resistance (AMR) poses a significant threat to human and animal health worldwide. Wild rodents and shrews may serve as bioindicators of environmental health. They may serve as a potential source of the transmission of AMR bacterial infections to humans and domestic animals, despite not directly consuming antibiotics. We conducted a cross-sectional study aimed to estimate the prevalence and factors associated with the AMR patterns in Staphylococcus spp. and Escherichia coli (E. coli) isolated from rodents and shrews. We trapped and collected throat and rectal/urine swab samples from 200 wild rodents (n = 115) and house shrews (n = 85) across different locations in Chattogram, Bangladesh. The collected samples were then evaluated for the isolation of both bacterial organisms using culturing and biochemical properties. We performed culture sensitivity (CS) tests of the isolates using the Kirby-Bauer disc diffusion method for 14 antimicrobials. The overall prevalence of Staphylococcus spp. was 26.5% (95% CI: 0.20-0.33; n = 53), and E. coli was 56% (95% CI: 0.49-0.63; n = 112) in the sampled rodents and Asian house shrews. Staphylococcus spp. isolates were 100% resistant to oxacillin, oxytetracycline, metronidazole, and cefixime. Again, E. coli isolates were 100% resistant to metronidazole followed by ampicillin and cefixime (98.0%), sulfamethoxazole + trimethoprim (97.0%), amoxicillin and doxycycline (96.0%), streptomycin (95.0%). Only gentamycin was sensitive against both bacterial isolates. Statistical modeling revealed a higher risk of resistant bacterial infection in rodents from agricultural interfaces compared to other habitats. Rodents and Asian house shrews with poor body condition were more prone to resistant Staphylococcus spp. infection, while rodents were more susceptible to resistant E. coli infection. Our findings indicate a significant prevalence of AMR Staphylococcus spp. and E. coli in urban rodents and house shrews, suggesting their potential role as reservoirs and disseminators of AMR, hence posing a risk to human and animal health.

Fig 1. Capturing sites of the rodents and Asian house shrews in Bangladesh.

The inset shows the study district in Bangladesh. The triangular shape represents the capturing sites. The map was created using a shapefile from the freely accessible GADM database (GADM; www.gadm.org) [34].

Fig 2. Percentage of identified bacteria in rodents and shrews in the study sites with 95% confidence interval.

Fig 3. Forest plot of odds ratios for Staphylococcus spp. compared to the reference category for each independent variable (intercept and reference category not shown) with 95% confidence intervals and significance markers (*).

The red line at the vertical intercept represents no effect (where the odds ratio equals 1 on the x-axis).

Fig 4. Estimated marginal means and 95% confidence intervals for Staphylococcus spp. across independent variables as a function of their respective explanatory variables.

Fig 5. Forest plot of odds ratios for E. coli compared to the reference category for each independent variable (intercept and reference category not shown) with 95% confidence intervals and significance markers (*).

The red line at the vertical intercept represents no effect (where the odds ratio equals 1 on the x-axis).

Fig 6. Estimated marginal means and 95% confidence intervals for E. coli across independent variables as a function of their respective explanatory variables.

Fig 7. Resistance pattern of Staphylococcus spp. and E. coli isolated from the rodents and Asian house shrews.

Note: SXT = Sulphamethoxazole+Trimethoprime, AMP = Ampicillin, CRO = Ceftriaxone, OX = Oxacillin, AZM = Azithromycin, CIP = Ciprofloxacin, S = Streptomycin, DO = Doxycycline, CFM = Cefixime, AML = Amoxicillin, E = Erythromycin, CN = Gentamycin, MTZ = Metronidazole, OT = Oxytetracycline.

Fig 8. Resistance pattern of Staphylococcus spp. isolated from the rodents and Asian house shrews.

Note: SXT = Sulphamethoxazole + Trimethoprime, AMP = Ampicillin, CRO = Ceftriaxone, OX = Oxacillin, AZM = Azithromycin, CIP = Ciprofloxacin, DO = Doxycycline, CFM = Cefixime, AML = Amoxicillin, E = Erythromycin, CN = Gentamycin, MTZ = Metronidazole, OT = Oxytetracycline.

Fig 9. Resistance pattern of E. coli isolated from the rodents and Asian house shrews.

Note: SXT=Sulphamethoxazole + Trimethoprime, AMP=Ampicillin, CRO=Ceftriaxone, AZM= Azithromycin, CIP=Ciprofloxacin, S=Streptomycin, DO=Doxycycline, CFM=Cefixime, AML=Amoxicillin, CN=Gentamycin, MTZ=Metronidazole, OT=Oxytetracycline.