Investigating the Prevalence and Antibiotic Resistance Patterns of Campylobacter Jejuni and Escherichia Coli Among Various Avian SpeciesABSTRACT
Avian species are recognized as reservoirs of bacteria with potential human health risks, highlighting the need for further research into their role in spreading these pathogens, and the associated public health concerns. This study aimed to investigate the prevalence and antibiotic resistance patterns of Campylobacter jejuni and Escherichia coli among various farmed avian species. A total of 5 avian species from different farms in the district of Kasur were sampled, and fecal samples (n=250) were collected for analysis. The samples were processed using standard microbiological techniques to isolate and identify C. jejuni and E. coli. Antibiotic susceptibility testing was performed to determine the resistance patterns of these bacteria against commonly used antibiotics. The results revealed a significant prevalence of C. jejuni (56%) and E. coli (87%) among the avian species tested. Regarding antibiotic resistance, both C. jejuni and E. coli strains showed varying levels of resistance to the tested antibiotics (ciprofloxacin, tetracycline, erythromycin and amoxicillin). The findings suggest that avian species may harbor C. jejuni and E. coli, underscoring the need for surveillance, control, and effective management of antibiotic use. It was concluded that avian species are significant reservoirs for Campylobacter jejuni and Escherichia coli, which exhibited notable antibiotic resistance and multidrug-resistant strains.
Keywords: Antibiotic resistance; avian species; Campylobacter jejuni; Escherichia coli; prevalence
INTRODUCTION
Avian gut is inhabited by thousands species of microbes and is considered a densely populated natural environment (Dipineto et al., 2017), but still has been poorly studied. The GIT (gastrointestinal tract) of avian species harbors different communities of microbes. Birds need rapid bursts of energy to support intensive flying, and the feed passage time through GIT is between 2-3.5 hours; in this context, the presence of microbiota is helpful for the extraction of energy (Wilkinson et al., 2016; Ombugadu et al., 2019). The gut microbiota, primarily comprising bacteria, has a beneficial impact on local and systemic immunity. Recent research has found that the gut microbiota can influence the pulmonary immune system during respiratory disease by influencing the gut-lung axis (Gilbert et al., 2016; Peng et al., 2021).
The bacterial community within the GIT, known as the gut microbiome, is a key determinant for the health and physiology of host birds (Sekirov et al., 2010; Wood et al., 2011). E. coli can infect people and other animals, particularly birds (Machado et al., 2018; Kimura et al., 2021). It shows great diversity and adaptation (Croxen & Finlay, 2010). Physiology of host vertebrates is adversely affected by their inhabiting gut microbes because these microbes impact functions like immunity, intestine morphology and nutrition development (Young, 2012; Neo et al., 2013; Stanley et al., 2014; Vasai et al., 2014). In recent studies, high performance sequencing technology and bioinformatics methods have been used to classify the species and behaviors of microbes that inhabit bird guts.
A lot of research have been conducted to describe the gut microbiota of birds such as the kakapo (Strigops habroptilus) and turkeys (Meleagris gallopavo), showing that immunity and digestive physiology are affected by gut microbes (Waite & Taylor, 2012; Jurado-Tarifa et al., 2016). Furthermore, birds travel long distances due to their migration and foraging behaviors, and thus have a significant impact on the spread of bacteria worldwide (Ryu et al., 2012; Keller & Shriver, 2014; Llarena et al., 2015). Diseases transmitted by birds are of particular concern due to the potential risk they pose not only to avian populations, but also to human health (Literák et al., 2010).
Many sampling methods such as oral, fecal, and gut sampling approaches have been developed to sample bacteria from individuals. Many bacteria can flourish in the intestinal caeca, which has low oxygen and enzyme concentrations (Choi et al., 2014; Cox et al., 2014). Cloacal sampling is widespread in birds since it is simple to do and allows for multiple samples from the same individual. It is often preferred over fecal sampling because the latter can be inefficient, poses difficulties for the precise identification of the specimen of origin, and also leads to problems related to the timing of defecation (Ganz et al., 2017; Wei et al., 2019). The prevalence of C. jejuni and E.coli has been found to be higher among opportunistic feeders, omnivores or scavengers than among insectivores and grainivores (Ramonaitė et al., 2015).
Prevalence, defined as the proportion of individuals in a population with a disease, is a key measure of disease status. Zoonoses from wildlife reservoirs present significant global health challenges (Hassell et al., 2017). Assessing disease prevalence is effective for understanding the burden on a population, including impacts on life expectancy, morbidity, and quality of life, beyond just economic costs. This information can guide health department investments (Noordzij et al., 2010; Mirsepasi-Lauridsen et al., 2019).
The resistance of bacteria to antimicrobial drugs is now a rising problem in human and animal diseases. Antimicrobial resistance (AMR) is a major problem that adversely affects the clinical treatments of pathogens, resulting in a decrease of the effectiveness of antibiotics and higher medical costs (Hebla et al., 2011; Founou et al., 2017).
The misuse and overuse of antibiotic treatments has led to the antibiotic resistance problem, along with the reduced economic inducements and demanding regulatory requirements causing a deficiency in the development of new drugs by the pharmaceutical industry (Ventola, 2015; de Kraker et al., 2016).
The primary aim of this study was to investigate the prevalence and antibiotic resistance patterns of Campylobacter jejuni and Escherichia coli among various farmed avian species.
MATERIALS AND METHODS
Ethics Statement
The research in this study was conducted in the avian conservation and research center maintained by the Department of Wildlife and Ecology of the University of Veterinary and Animal Sciences (UVAS).
Sample Area
Samples were collected from different avian farms (n=10) in the district of Kasur (Figure 1). The avian farms were selected from four tehsil of the district of Kasur (UVAS Avian Conservation and Research Centre, Arian Avian Farm Pattoki, Pattoki Bird Market, Kashif Bird Farm, Jahanzaib Hassan Private Farm Chunian, Hafiz bird Shop Chunian, WS Aviary Kot Radha Kishan, Shali’s Bird Aviary Kot Radha Kishan, Kasur Bird’s Point, and AS Birds Farm Kasur).
Collection and processing of fecal samples
Freshly deposited fecal samples were collected with the help of a forceps from captive pheasants (Phasianus colchicus), chukar partridges (Alectoris chukar), peafowl (Pavo cristatus) (n=5), quails (Coturnix coturnix) and turkeys (Meleagris gallopavo) reared privately in avian farms in the district of Kasur, Pakistan. Fecal samples were collected from the cages using the methodology described by Garcia-Mazcorro et al. (2017). There was no direct interaction with the birds during the collection of fecal samples. Since birds are often reared in flocks in captivity, a sample of their droppings was collected from each flock.
Fecal samples were collected in autoclaved falcon tubes under hygienic conditions from the tray, and kept at 4°C until processing. Fecal samples were ground into powder form and mixed in phosphate-buffered saline (PBS) solution separately in labelled Eppendorf tubes. The sample mixture was centrifuged in Bio-Rad centrifuge machine at 5000rpm (Murphy et al., 2005), and the supernatant of the sample was taken and diluted serially up to a 10-6 fold.
Isolation and identification of bacterial species E. coli and C. jejuni
Prepared samples were cultured on MacConkey agar and Eosin Methylene Blue agar (EMB agar) for sub-culturing (Ngaiganam et al., 2019). For bacterial growth, the plates were then placed in an incubator for 18-24 hours at a temperature of 37°C. The identification and confirmation of E. coli was based on the characteristics observed in the colonies on the agar plate, following the method described by Habib et al. (2021). Three putative colonies from every plate were independently characterized using Gram staining and various biochemical tests to ensure the presence of E. coli (Divya et al., 2016).
Every sample was examined separately. Both direct plating of the processed sample on modified Charcoal Cefoperazone Deoxycholate agar (mCCDA) with CCDA selective supplement and selective enrichment in Bolton broth were used to isolate thermophilic Campylobacter spp. (Milton et al., 2015). Samples were prepared and homogenized in PBS, bacterial cells were isolated by centrifugation, and the pellet was washed to remove contaminants. For the analysis, purity was confirmed by plating, and then the purified cells were stored at -80°C or further analysis was conducted as needed. The specific colonies were chosen and transferred to Blood agar for further sub-culturing at 37°C for 24 hours. The identification process to confirm the presence of C. jejuni involved a series of methods, such as Gram staining and biochemical tests.
Prevalence of E. coli and C. jejuni
The plate count method was used to calculate the number of C. jejuni and E. coli colonies per mL of the fecal matter sample using 200 µL of every dilution on blood agar and MacConkey agar, respectively (Jahan et al., 2018). For the calculation of CFU, culture plates containing colonies within the range of 30 and 300 were considered (Sutton, 2011).
Antimicrobial Susceptibility by Disk diffusion method
Resistance to antimicrobials was tested using the Kirby-Bauer disk diffusion method. The antibiotics used in this study were ciprofloxacin, enrofloxacin, gentamicin, nalidixic acid, tetracycline, chloramphenicol, streptomycin, erythromycin, doxycycline, and amoxicillin, and the results were based on the Clinical and Laboratory Standards Institute (CLSI) breakpoints (Wayne, 2020). These antibiotics were chosen because of their widespread use in poultry feed and their effectiveness in treating colibacillosis and other avian infections.
Statistical analysis
Prevalence was calculated as CFU and shown as Mean ± SD. One way ANOVA was applied for comparison of prevalence depending upon the sampling sites and bacterial species (E. coli and C. jejuni). The zone of inhibition was mentioned in percentages, indicating the proportion of total isolates resistant to a specific antibiotic.
RESULTS
The specific colonies were chosen and transferred to Blood agar for further sub-culturing at 37°C for 24 hours, and the identification process involved a series of methods, such as Gram staining to confirm the presence of C. jejuni. The results are shown in Table 1
The descriptive statistics showed that the observed mean value of the CFU of E. coli was greater in turkeys as compared to other birds (i.e., 186.6), and the lowest CFU value of E. coli was observed in chukar partridges (i.e., 107.1), as shown in Table 2 and Figure 2. The one way analysis of variance (ANOVA) showed that there was no statistically significant effect on the E. coli CFU/ml of fecal samples of these species (p=0.086) (p> 0.05) (Table 3).
The descriptive analysis showed the mean value of CFU of C. jejuni among different avian species. The highest mean value for the CFU of C. jejuni was observed in quails and peafowl, with means of 164.9 and 164.6, respectively, as shown in Table 4 and Figure 3. One way ANOVA showed that there is no statistically significant effect on the C. jejuni CFU/ml of fecal samples of these species, since p=0.951 (p>0.05) (Table 5). C. jejuni prevalence was almost the same in all avian species.
The ANOVA results indicate that there were no statistically significant differences in C. jejuni CFU means among the different bird species.
Antibiotics susceptibility tests against ten antibiotics were conducted. E. coli and C. jejuni from peafowl, pheasants, turkeys, chukar partridges and quail fecal samples showed resistance against ciprofloxacin, enrofloxacin, gentamicin, nalidixic acid, tetracycline, chloramphenicol, streptomycin, erythromycin, doxycycline and amoxicillin. The zone of inhibition was mentioned in percentages, indicating the proportion of total isolates resistant to a specific antibiotic, as shown in Figures 4 and 5.
DISCUSSION
The findings of this study enhance our understanding of the prevalence and antibiotic resistance patterns of Campylobacter jejuni and Escherichia coli among various avian species across farms in the Kasur district. The isolation methods for E. coli and C. jejuni from pheasants and turkeys, as suggested by Mushtaq et al. (2021) and Good et al. (2019) respectively, were applied in this study. Notably, the prevalence of E. coli and C. jejuni in turkeys and pheasants was significantly lower, reaching 30% and 39.2%, respectively, compared to higher rates observed in quails, peafowl, and partridges. These findings are consistent with previous research, such as that by Hughes et al. (2009), which reported similar differences in the prevalence of C. jejuni among wild birds of different taxonomic families. However, the reasons behind the varying prevalence of C. jejuni across different wild bird species remain unclear and warrant further investigation.
Similar differences in the prevalence of C. jejuni in wild birds of different taxonomic families have been observed in other studies (Hughes et al., 2009). Islam et al. (2021) reported that out of 66 samples, 55 samples were detected to have E. coli, amounting to 83.33% of positive samples. Results of that investigation (83.33%) are close to the values observed in the present study. However, the reason for the different prevalence of C. jejuni in fecal samples of different wild bird species remains unclear. The results showed that prevalence of E. coli and C. jejuni were independent of the avian species.
Descriptive statistics showed that the mean value of CFU of E. coli observed was greater in turkeys than other birds (i.e, 186.6), and the lowest value of CFU of E. coli was observed in chukar partridges (i.e, 107.1). Different prevalences of E. coli and Campylobacter jejuni among wild birds have been obtained in previous studies and varied from 1.4 to 72.7%, depending on the countries and wild species (Colles et al., 2011). The ANOVA results indicate that there were no statistically significant differences in E. coli CFU means among the different bird species.
The Order of prevalence of E. coli was as follows:
Turkeys>Peafowl>Pheasants>Quails>Chukar Partridges
The CFU of C. jejuni per collected sample was calculated by counting pour plates with 30-300 colonies. The descriptive analysis showed the mean value of CFU of C. jejuni among different avian species. The highest mean value for the CFU of C. jejuni was observed in quails (164.9) and peafowl (164.6). The ANOVA results indicated that there were no statistically significant differences in C. jejuni CFU means among the different bird species.
The order of prevalence of C. jejuni was as follows:
Quails>Peafowl>Pheasants>Turkeys>Chukar Partridges
A study conducted by Díaz-Sánchez et al. (2012) confirmed that farmed partridges had higher prevalence of E. coli and Campylobacter sp. Prevalence of E. coli was significantly higher in farm-reared (45%, p=0.01) and restocked partridges (60%, p<0.001). A study investigated wild birds for the presence of enteric pathogenic bacteria in their environment, specifically identifying Campylobacter spp., which showed tolerance to ampicillin and ciprofloxacin(Beata et al., 2022). Our findings align with this, indicating that while fecal samples were favorable for detecting C. jejuni, cloacal samples were not suitable.
. A recent study indicated that 100% of studied turkey isolates were resistant to tetracycline (Kürekci et al., 2012). Our findings are also in line with the conclusion of Martín-Maldonado et al. (2019) that there was a low frequency of resistance to quinolones and macrolides.
Birds are frequently believed to be Campylobacter repositories since the growth temperature range of these bacteria resembles the internal temperatures of birds more than mammals. The present study was an attempt to compare the Campylobacter prevalence in three important captive avian species, as well as investigate the seasonal effect on this prevalence. Du et al. (2019) investigated a wild bird species as a potential carrier of enteric pathogenic bacteria in its environment, specifically focusing on the presence of Campylobacter species. The study revealed that the bacteria were tolerant to ampicillin and ciprofloxacin.
Our findings align with theirs, showing that fecal samples are conducive to detecting C. jejuni, whereas cloacal samples are not suitable for this purpose. The presence of pathogenic Campylobacter in captive avian species highlights the need for protective measures in their housing. The significance of this study lies in understanding the role of avian species as reservoirs for pathogenic bacteria such as Campylobacter jejuni and Escherichia coli. The findings provide crucial insights into the prevalence and antibiotic resistance patterns of these bacteria across different avian species, which has direct implications for both animal and human health.
CONCLUSION
In conclusion, our study reveals a high prevalence of Campylobacter jejuni and Escherichia coli among farmed avian species, along with significant antibiotic resistance, which could pose a serious threat to both human and animal health. We stress the need for further research to assess the role of farmed avian species in the epidemiology of these pathogens.
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DATA AVAILABILITY STATEMENT
Data will be available upon request.
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DISCLAIMER/PUBLISHER’S NOTE
The published papers’ statements, opinions, and data are those of the individual author(s) and contributor(s). The editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions, or products referred to in the content.
Data availability
Data will be available upon request.
Publication Dates
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Publication in this collection
16 Dec 2024 -
Date of issue
2024
History
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Received
21 Feb 2024 -
Accepted
22 Oct 2024
