Characterization and epidemiology of antimicrobial resistance patterns of Salmonella spp. and Staphylococcus spp. in free-ranging rhesus macaque (Macaca mulatta) at high-risk interfaces with people and livestock in Bangladesh

Abstract

IntroductionAntimicrobial resistance (AMR) is a growing global health threat for humans and animals. Environmental contamination of antimicrobials from human and domestic animal feces has been linked to AMR in wildlife populations, including rhesus macaques. This study aimed to describe the eco-epidemiology of AMR within Salmonella and Staphylococcus species isolated from rhesus macaques.MethodsWe followed macaque groups for 4 h per day (2 days) to observe the direct and indirect contact rate and type between macaques and people and livestock. We collected 399 freshly defecated, non-invasive fecal samples from macaques at seven sites in Bangladesh in January–June 2017. Bacterial isolation and identification were conducted using culture, biochemical characteristics, and polymerase chain reaction (PCR). An antimicrobial susceptibility test (AST) for 12 antimicrobials for each organism was conducted using the Kirby–Bauer disc diffusion method.ResultsThe overall prevalence of Salmonella spp. and Staphylococcus spp. in rhesus macaques was 5% (n = 18; 95% CI: 3–7%) and 16% (n = 64; 95% CI: 13–20%), respectively. All the isolated Salmonella spp. and most of the Staphylococcus spp. (95%; 61/64; 95% CI: 86.9–99%) were resistant to at least one antimicrobial. The odds of a fecal sample having antimicrobial-resistant Salmonella spp (OR = 6.6; CI: 0.9–45.8, P = 0.05) and Staphylococcus spp. (OR = 5.6; CI: 1.2–26, P = 0.02) were significantly higher in samples collected at peri-urban sites than those collected at rural and urban sites. Salmonella spp. were most frequently resistant to tetracycline (89%), azithromycin (83%), sulfamethoxazole-trimethoprim (50%), and nalidixic acid (44%). Staphylococcus spp. were found to be highly resistant to ampicillin (93%), methicillin (31%), clindamycin (26%), and rifampicin (18%). Both bacterial species produced colonies with multidrug resistance to up to seven antimicrobials. Direct and indirect contact rates (within 20 m for at least 15 min) and resource sharing between macaques and people were higher in urban sites, while macaque-livestock contact rates were higher in rural sites.DiscussionThe study shows that resistant microorganisms are circulating in rhesus macaque, and direct and indirect contact with humans and livestock might expand the resistant organisms.

Antimicrobial Resistance Profiles, Virulence Determinants, and Biofilm Formation in Enterococci Isolated from Rhesus Macaques (Macaca mulatta): A Potential Threat for Wildlife in Bangladesh?

“…In the same way, different eco and safari parks provide breeding-friendly and natural environments that help them to adapt easily to these areas. Macaques are found in many urban, rural, and forested/protected areas in Bangladesh [4].…”

“…Moreover, the frequency of these interactions has risen due to factors, such as eco-tourism and the expansion of forest areas, potentially resulting in the exchange of bacteria through multiple routes, including the provision of food [5]. It is evident that monkeys, including rhesus macaques, can carry different bacterial agents, including Enterococcus spp., Escherichia coli, Salmonella spp., Staphylococcus spp., Klebsiella spp., Campylobacter spp., Shigella spp., and others [4][5][6][7].…”

“…The excessive use of antibiotics creates selective pressure, which serves as a significant driving force behind the emergence of resistance [20]. In Bangladesh, it is common for people to self-administer antimicrobial drugs without seeking guidance from licensed doctors or veterinarians to treat themselves or others, including animals [4]. The genes responsible for bacterial resistance, commonly found in the microbiota of humans or animals, are now being transmitted to natural environments and wild animals that have not been exposed to antimicrobial agents before [21].…”

Identification of Vancomycin Resistance in Methicillin-resistant Staphylococcus aureus in two macaque species and decolonization and long-term prevention of recolonization in Cynomolgus Macaques (Macaca fascicularis)

“…Methicillin-resistant Staphylococcus aureus (MRSA) has been found in numerous captive and non-captive colonies of macaques ( 1 – 7 ) and is both increasingly prevalent in community settings and a major nosocomial pathogen in human hospitals. Macaques are often imported to the US from regions with high MRSA prevalence in human and nonhuman primate populations, which may be in part from zoonotic and zooanthroponotic transmission of MRSA among other factors ( 1 , 8 – 10 ).…”

“…Methicillin-resistant Staphylococcus aureus (MRSA) has been found in numerous captive and non-captive colonies of macaques ( 1 – 7 ) and is both increasingly prevalent in community settings and a major nosocomial pathogen in human hospitals. Macaques are often imported to the US from regions with high MRSA prevalence in human and nonhuman primate populations, which may be in part from zoonotic and zooanthroponotic transmission of MRSA among other factors ( 1 , 8 – 10 ). MRSA is transmitted through direct contact and fomites with colonization occurring in moist areas, primarily the nares, but additional sites can include skin and other mucosal surfaces, especially in the inguinal, axillary, genital, and rectal areas.…”