Salmonella spp. and E. coli isolated from 515 samples collected from poultry farms at the north Vietnam. The results showed that the presence of E. coli in the poultry farm was 59.4%. The highest positive rate was fecal samples 78.0%; following by sewages samples (77.8%), poultry house floors swap samples (68.0%), drinking water (17.8%), tools samples (16.7%) and none of 45 food samples were E. coli positive isolation. In this study, 37 samples (7.2%) were Salmonella positive isolation including 10.0% fecal samples; 9.3% poultry house floors swap and 6.7% seweages samples. The E.coli isolates were highly resistant to tetracycline (85.3%), streptomycin (83.3%), ampicillin (61.8%), trimethoprim (56.9%) and nalidixic acid (55.9%). They were low resistant to ceftazidime (6.9%) and nitrofurantoin (12.7%). The other antibiotics such as norfloxacin, ciprofloxacin and gentamicin were resisted by E.coli isolates range from 15.7% to 32.4%. In our results, the Salmonella isolates were commonly resistant to streptomycin (89.2%), tetracycline (83.8%) and ampicillin (59.5%). Three antibiotic such as ciprofloxacin, gentamicin and norfloxacin were resisted by the Salmonella isolates with the similar rates (21.6%). Salmonella isolates showed resistance to ceftazidime at the lowest rate (16.2%). Of the isolated trains, 65.7% of the E. coli and 62.2% of the Salmonella isolates showed multi-drug resistance. The data suggest that detection of resistance isolates from chicken, poultry environment, and humans need for one health consideration in the usage of antibiotics in the poultry industry.

Keywords: antibiotic resistance, E. coli, poultry farms, Salmonella Spp, vietnam

Antibiotics have been used widely in in farm animals, especially for poultry production to treat and prevent bacterial infections and as growth promoters in feeds.^1–3 However, it is now generally known that the widespread use of antibiotics is the main risk factor for an increase in the occurrence of bacterial resistant strains.^4,5 The emergence and dissemination of antibiotic-resistant bacterial strains like Salmonella and Escherichia coli from poultry products are reported to be high and are increasing worldwide.^3,6 Beside, antibiotic-resistant Salmonella and E. coli strains involved the human diseases are mostly spread from food and farm animals.^7–9 Therefore, it is necessary to know where the origin sources of antibiotic-resistant bacteria which were contaminated to the food production chains; and any knowledge about that might provide valuable information to reduce the sources of contamination with resistant bacteria during food processing and thus to minimize the risk for the consumer. Thus, given the health risks linked to the presence of E. coli and Salmonella in both poultry production and human health, as well as the antibiotic resistance issue posed by these germs in public health, regular monitoring of their resistance to antibiotics in poultry farming is essential.^1,10

However, as far as we are aware, there have not been any reports about the occurrence of antibiotic-resistant bacteria in commercial poultry farms in Vietnam. The aim of this study is to detect the prevalence and antibiotic resistance rates of Salmonella and E. coli at poultry farms in the North Vietnam in order to provide the useful information for the food safety and public health in Vietnam.

For the samples collection, during three years, from January 2011 to December 2013, 515 samples collected from 45 flocks of 15 poultry farms located in three provinces (Bac Ninh, Hai Duong, Vinh Phuc) and two cities (Ha Noi, Hai Phong) at the north Vietnam including fecal samples (n=200), poultry house floors (n=150), drinking waters (n=45), poultry foods (n=45), sewages (n=45) and tools (n=30); Swab samples (poultry house floors, tools) were sampled by autoclaved cottons in an area approximately 20 cm2 and placed in sterile bags with 90 mL of buffered peptone water (BPW); approximately 100 mL of drinking waters and sewages were taken to 200 mL bottle and then 10 mL was mixed with 90 mL of BPW; approximately 10 gram of fecal samples and 250 gram of poultry food samples were taken to the sterilized plastic bags. All samples were kept on ice box during the transportation and characterized on the arrival day at the laboratory of Department of Veterinary hygiene, National of Institute veterinary research, Vietnam.

For the bacteria isolation, at the laboratory 1 gram of substance from fecal samples; 25 gram of food samples were homologized with BPW following the ratio 1:9; the bags of swap samples, drinking and seweages samples at the samples collection step also incubated at 370C within 18 – 24 hr for pre-enrichment. The next steps for Salmonella isolation were previously described.¹¹ For E. coli isolation, 0.1 mL of the 18 - 24h incubated pre-enrichment cultures was continuously incubated onto eosin methylene blue agar (EMB) at 37°C for 24 hr. Only one typical colony producing metallic sheen on EMB agar were isolated and streaked into the triple sugar iron agar (TSI) tube and incubated at 37°C for 24 hr. The colonies in TSI agar showed typical E. coli behaviors, such as glucose and lactose fermentation with gas production and the absence of H2S, were confirmed by gram staining and a biochemical series based on citrate utilisation, indol production, methyl red and Voges-Proskauer reactions.

For the antibiotic susceptibility testing, in 2021, thirty seven isolated Salmonella and one hundered isolated E.coli strains were randomly selected to characterize the antibiotic susceptibility at the Laboratory of the Faculty of Veterinary medicine, Vietnam national university of agriculture, Hanoi, Vietnam. The antibiotic susceptibility of isolates was determined according to the guidelines of the Clinical and Laboratory Standards Institute.¹² Agar diffusion assays were performed on Muller - Hinton agar with disks containing 10 different antibiotic agents (Oxoid, UK). The tested antibiotics were as follows: ampicillin (Am), 10 μg; ceftazidime (Cf), 30μg; ciprofloxacin (Ci), 5μg; gentamicin (Ge), 10μg; nalidixic acid (Na), 30 μg; norfloxacin (Nor), 10μg; streptomycin (St), 10μg; tetracycline (Te), 30μg; trimethoprim (Tm), 5 μg and nitrofurantoin (Ni), 300μg. The susceptible, intermediate or resistant interpretive categories were used according to CLSI guidelines.¹³ Multi drug-resistant (MDR) strains were defined when it showed the resistance to at least one antibiotic in three or more different categories.¹⁴ In our study, antibiotic classes included: Aminoglycosides (gentamicin, streptomycin); β - Lactams (ampicillin, ceftazidime); Pyrimidine (trimethoprim); Quinolones (ciprofloxacin, norfloxacin, nalidixic acid); Tetracyclines (tetracycline) and Nitrofuran (nitrofurantoin).

Data and statistical analysis, statistical comparison of the prevalence, antibiotic resistance rates between Salmonella and Escherichia coli from different sources was analyzed by the Chi-square test (Microsoft Excel 2016).

The percentage of E.coli and Salmonella positive samples collected from poultry farms shown in the Table 1. Overall, the presence of E. coli in the poultry farm was quite high, 306/515 (59.4%) examined samples. The highest positive rate was fecal samples 156/200 (78.0); following by seweages samples 35/45 (77.8%), then poultry house floors swap samples 102/150 (68.0%); the positive rates of drinking warter and tools samples were 8/45 (17.8%) and 5/30 (16.7%), respectively; and none of 45 food samples were E. coli positive isolation. Thirty seven of 515 (7.2%) samples were Salmonella positive isolation. Among them, Salmonella was detected from 20/200 (10.0%) fecal samples; the prevalence of Salmonella in poultry house floors swap and seweages samples were 14/150 (9.3%) and 3/45 (6.7%), respectively; there were no Salmonella contamination with the tools, poultry food and drinking samples.

Antibiotic susceptibility of the E.coli isolates were shown in the Table 2 and Table 3. The E.coli isolates were highly resistant to tetracycline (85.3%), streptomycin (83.3%), ampicillin (61.8%), trimethoprim (56.9%) and nalidixic acid (55.9%). They were low resistant to ceftazidime (6.9%) and nitrofurantoin (12.7%). The other antibiotics such as norfloxacin, ciprofloxacin and gentamicin were resisted by E.coli isolates range from 15.7% to 32.4%. A total of 29 antibiotypes were obtained from the E. coli isolates, only six strains shown the sensitivity to all of ten antibiotics. And 67/102 (65.7%) of the E. coli strains showed multi drug-resistant (resisted at least three different antibiotic classes). More than half (52/102 – 51.0%) were resistant to at least five antibiotics. Fifty five (14.7%) strain was recorded against five antibiotics belong to five different classes; only one isolate was resistant to all compounds tested. The most commonly found resistance patterns are listed in Table 4. The resistance profile was the most prevalent (14.7%), which was resistant to Na – Tm – Am – St – Te; the patterns Ge – Na – Tm – Am – St – Te, was observed in ten (9.8%) of the E coli isolates.

Antibiotic susceptibility of the Salmonella isolates were presented in the Table 4 and Table 5. The Salmonella isolates were commonly resistant to streptomycin (89.2%), tetracycline (83.8%) and ampicillin (59.5%). Three antibiotic such as ciprofloxacin, gentamicin and norfloxacin were resisted by the Salmonella isolates with the similar rates (21.6%). Salmonella isolates showed resistance to ceftazidime at the lowest rate (16.2%). The antibiotic resistance rates of nalidixic acid and trimethoprim were 43.2% and 54.1%, respectively. There were thirty six Salmonella strains among the thirty seven isolates that showed resistant to at least one antibiotics. And twenty seven different resistance patterns were recorded. In particular, 23/37 (62.2%) of the Salmonella isolates showed the multi drug-resistance. Sixty multi drug-resistant Salmonella isolates predominantly resisted to 3 - 7 antibiotics belong to 3 -5 different antibiotic classes, the predominant MDR profile was Na-Tm-Am-St-Te (10.8%) and No-Ci-Na-Tm-Am-St-Te (8.1%). Interestingly, there were four Salmonella strains could resisted to 8 – 10 antibiotics belong to 6 different antibiotic classes.

Salmonella contamination of poultry and derivative products occurs at different levels. Thirty seven (7.2%) of the 515 poultry farms samples were contaminated with Salmonella. The isolation rate varied according to the origin of the sample, 10.0% for fecal samples, 9.3% for poultry house floor swaps and 6.7% for the seweage samples. The other report in Vietnam¹⁵ shown that, Salmonella was present in the poultry farms samples such as dinking warter, bedding, feed, chicken feces and environmental samples ranged from 0.7% to 7.7%. Around the world, the Salmonella spp. prevalence varied considerably among regions and countries such as in several European countries. The reported prevalence was in France (3.4%), Italy (9.2%), Germany (2.7%), Spain (1.02%), Poland (1.57%) and Sweden (nearly 0%).^16–18 The isolation rate varied from 2.8% to 15.9% according to the origin of the sample at the Afican countries such as Algeria, Ethiopia and Nigeria.^19–21 The prevalence of Salmonella in broiler farms at Colombia²² was higher than that in our research (26.7%). However, Salmonella was only isolated in 6.7% of the poultry litter samples in the southern United States.⁷ The prevalence of non-typhoidal Salmonella can be found in environmental reservoirs, infections from which are challenging to control.10 In chicken farms, Salmonella can be transmitted through feces, vehicles, workers, clothing, footwear, equipment, water, food, garbage, animals, and other factors.²³

In this study we examined antibiotic resistance in commensal E. coli isolates from chicken farms in some provices and cities in the north of Vietnam. The high level of E. coli resistance in chicken farms is a public health concern, this may also be an indicator of emerging resistance in other gut microflora within the chicken population. The isolates were highly resistant to tetracycline (85.3%), streptomycin (83.3%), ampicillin (61.8%), trimethoprim (56.9%) and nalidixic acid (55.9%). High resistance of E.coli isolated from chicken farms to broad-spectrum antibiotics have been reported in Vietnam.¹⁵ The authors reported that E. coli were highly resistant to tetracycline (93.4%), and ampicillin (86.0%), and Trimethoprim/sulfamethoxazole (69.7%). The significant proportion of resistance against the above antibiotics was also reported from Ghana, Nigeria and China.^24–26 The observed high prevalence of antibiotic resistance reflects the common use of antibiotic products for therapeutic and prophylactic purposes, as found in our survey on antibiotic drug usage.¹⁸ In contrast, in this study, isolated E.coli strains showed relatively lower grade of resistance against third generation cephalosporins (ceftazidime – 6.9%), quinolones group (norfloxacin – 15.7% and ciprofloxacin – 19.6%). This finding is supported by other studies showing lower resistance rates against the above antibiotics.^27–29 However, data from seven European countries suggest a higher prevalence of ciprofloxacin resistance (57.6%), while data from five European countries indicate a higher prevalence of ceftazidime resistance (11.1%) in bacteria isolated from chickens in these countries.^30,31 Although such comparisons should be interpreted with caution because of differences in sampling methods as well as differences in the breakpoints used for interpreting susceptibility test results between studies from different regions.

Antibiotic resistance may arise due to the indiscriminate use of antimicrobials and their use as growth promoters and chemotherapeutic agents to control diseases at farms.¹⁸ Most Salmonella isolates in this study showed relative resistance to streptomycin (89.2%), tetracycline (83.8%) which have been used to treat salmonellosis since many years in Vietnam. The use of antibiotics over long periods thus favors the selection of resistant bacterial strains. The high percentage of Salmonella isolates resisted to the antibiotic above in current research is in line with the previous reports in Bangladesh and Vietnam.^32,33 In curent research, the Salmonella isolates resisted to ampicillin at high level rate (59.5%). Our results were in line with reports from Myanmar, 47.1%; Malaysia, 72.7% and Singapore, 78.8%;^34–36 however, Salmonella spp. resistance to ampicillin was observed at lower rates in Japan, 17.9%; South Korea, 5.6% and Iran, 11.7%.^37–39 Quinolone resistance is a current worldwide problem in human and veterinary medicine. The Salmonella isolates resisted to ciprofloxacin, norfloxacin and nalidixic acid by range from 21.6% to 43.2%. In comparison to the other results, higher rates of quinolones resistance (ciprofloxacin and nalidixic acid) have been reported in Salmonella isolated from poultry in the EU (64.7% and 61.5%), China (25.7% and 46.7%) and Brazil (86.5% and 89%).^30,40,41 However, Salmonella isolated from broilers have shown a low resistance frequency to quinolones in Canada (3% and <1%) and in the USA (0% and <1%), which can be attributed to the restricted use of fluoroquinolones in poultry.^2,42,43

Emergence of MDR bacteria, especially Enterobacteriaceae, has increased in recent years. In this study, 65.7% of the E. coli and and 62.2% of the Salmonella isolates showed MDR. The similar proportions of MDR were also reported for Salmonela isolates from Bangladesh, Nigeria and Malaysia;^44,45,32 and for E. coli isolates from Vietnam, Malaysia and Ghana.^45,24,46 The occurrence of MDR may be linked with indiscriminate use of antimicrobial agents. MDR makes the difficult treatment of infections caused by pathogenic bacteria in both poultry and humans. Thus, the use of antibiotics at poultry farms and households should be controlled to prevent the creation of MDR pathogenic strains.^47-51

In this study, the prevalence of E. coli and Salmonella spp. detected in chicken farms in the north Vietnam was 59.4% and 7.2%, respectively. The isolates showed high resistance rates to tetracycline, ampicillin, strepmycin and trimethoprim; and its were fairly susceptible to ceftazidime, norfloxacin, ciprofloxacin. This varying degree of resistance shown by E. coli and Salmonell spp. supports the assertion that the poultry environment is a potential reservoir for antibiotic-resistant trains that can spread from the animals to the human population using poultry liter for farming purposes. In Vietnam, like in other developing countries, the indiscriminate and widespread use of antimicrobials in veterinary practice and the easy access to antimicrobials by farmers who can purchase them without any prescription should be addressed. These findings provide evidence for the emergence for the antimicrobial resistance of Salmonella spp. and E. coli in poultry farms in Vietnam. Future studies should focus on detection of resistance isolates from chicken, poultry environment, and humans to demonstrate the need for one health consideration in the usage of antibiotics in the poultry industry.

This study was supported by the Ministry of Agriculture and Rural Development, Vietnam. We thank the staff of the Department of Veterinary Hygiene, National Institute of Veterinary Research, Hanoi, Vietnam, for their technical assistance and the isolates providing. The authors would like to thank the students, technicians, and other individuals who helped us in sampling and processing.

Author declares there is no conflict of interest in publishing the article.

None.

1. Bonardi S. Salmonella in the pork production chain and its impact on human health in the European Union. Epidemiol Infect. 2017;145(8):1513–1526.
2. Caffrey N, Agunos A, Gow S, et al. Salmonella spp. prevalence and antimicrobial resistance in broiler chicken and Turkey flocks in Canada from 2013 to 2018. Zoonoses Public Health. 2021;68(7):719–736.
3. Costa PM, Loureiro L, Matos AJ. Transfer of multidrug-resistant bacteria between intermingled ecological niches: the interface between humans, animals and the environment. Int J Environ Res Public Health. 2013;10(1):278–294.
4. Looft T, Johnson TA, Allen HK, et al. In-feed antibiotic effects on the swine intestinal microbiome. Proc Natl Acad Sci USA. 2012;109(5):1691–1696.
5. Love D, Davis M, Bassett A, et al. Dose imprecision and resistance: Free-choice medicated feeds in industrial food animal production in the United States. Environ Health Perspect. 2011;119(3):279–283.
6. Schwaiger K, Huther S, Hölzel C, et al. Prevalence of antibiotic-resistant enterobacteriaceae isolated from chicken and pork meat purchased at the slaughterhouse and at retail in Bavaria, Germany. Int J Food Microbiol. 2012;154(3):206–211.
7. Dunn LL, Sharma V, Chapin TK, et al. The prevalence and concentration of Salmonella Enterica in poultry litter in the southern United States. PLoS One. 2022;17(5):e0268231.
8. Hammerum AM, Heuer OE. Human health hazards from antimicrobial-resistant Escherichia coli of animal origin. Clin Infect Dis. 2009;48(7):916–921.
9. Vieira AR, Collignon P, Aarestrup FM, et al. Association between antimicrobial resistance in Escherichia coli isolates from food animals and blood stream isolates from humans in Europe: An ecological study. Foodborne Pathog Dis. 2011;8(12):1295–1301.
10. EFSA. The European Union summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks in 2014. EFSA Journal. 2015;13:4329.
11. Thai TH, Hirai T, Lan NT, et al. Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol. 2012;156(2):147–151.
12. CLSI. Performance standards for antimicrobial susceptibility testing. 30th edn. CLSI supplement M100. Wayne, PA; 2020.
13. CLSI. Performance standards for antimicrobial disk susceptibility tests. 13th edn. CLSI standard M02. Wayne, PA; 2018.
14. Magiorakos AP, Srinivasan A, Carey RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–281.
15. Nguyen VT, Carrique-Mas JJ, Ngo TH, et al. Prevalence and risk factors for carriage of antimicrobial-resistant Escherichia coli on household and small-scale chicken farms in the Mekong Delta of Vietnam. J Antimicrob Chemother. 2015;70(7):2144–2152.
16. EFSA. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2001. EFSA Journal. 2013;11:3129.
17. Lamas A, Fernandez-No IC, Miranda J, et al. Prevalence, molecular characterization and antimicrobial resistance of Salmonella serovars isolated from Northeastern Spanish broiler flocks (2011-2015). Poult Sci. 2016;95(9):2097–2105.
18. Wibisono FM, Wibisono FJ, Effendi MH, et al. A review of salmonellosis on poultry farms: Public health importance. Sys Rev Pharm. 2020;11(9):481–486.
19. Dagnew B, Alemayehu H, Medhin G, et al. Prevalence and antimicrobial susceptibility of Salmonella in poultry farms and in contact humans in Adama and Modjo towns, Ethiopia. Microbiologyopen. 2020;9(8):e1067.
20. Dibner J, Richards J. Antibiotic growth promoters in agriculture: History and mode of action. Poult Sci. 2005;84(4):634–643.
21. Jibril AH, Okeke IN, Dalsgaard A, et al. Prevalence and risk factors of Salmonella in commercial poultry farms in Nigeria. PLoS One. 2020;15(9):e0238190.
22. Rodríguez-Hernández R, Bernal JF, Cifuentes JF, et al. Prevalence and molecular characterization of Salmonella isolated from broiler farms at the Tolima region - Colombia. Animals (Basel). 2021;11(4):970.
23. Witkowska D, Kuncewicz M, Żebrowska JP, et al. Prevalence of Salmonella spp. in broiler chicken flocks in northern Poland in 2014–2016. Ann Agric Environ Med. 2018;25(4):693–697.
24. Mensah GI, Adjei VY, Vicar EK, et al. Safety of retailed poultry: Analysis of antibiotic aesistance in Escherichia coli From raw chicken and poultry fecal matter from selected farms and retail outlets in Accra, Ghana. Microbiol Insights. 2022;15:11786361221093278.
25. Omoya FO, Ajayi KO. Antibiotic resistance pattern of pathogenic bacteria isolated from poultry droppings in Akure, Nigeria. Futa J Res Sci. 2016;12:219–227.
26. Yassin AK, Gong J, Kelly P, et al. Antimicrobial resistance in clinical Escherichia coli isolates from poultry and livestock, China. PLoS One. 2017;12(9):e0185326.
27. Braykov NP, Eisenberg JN, Grossman M, et al. Antibiotic resistance in animal and environmental samples associated with small-scale poultry farming in Northwestern Ecuador. mSphere. 2016;1(1):e00021–15.
28. Ngai DG, Nyamache AK, Ombori O. Prevalence and antimicrobial resistance profiles of Salmonella species and Escherichia coli isolates from poultry feeds in Ruiru Sub-County, Kenya. BMC Res Notes. 2021;14(1):41.
29. WHO. Mapping educational opportunities and resources for health-care workers to learn about antimicrobial resistance and stewardship. Geneva, World Health Organization. Human Resources for Health Observer Series No. 21: Licence: CC BY-NC-SA 3.0 IGO. 2017.
30. EFSA and ECDC. European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2018/2019. EFSA Journal. 2021;19.
31. EFSA and ECDC. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2019–2020. EFSA Journal. 2022;20(3):7209.
32. Mahmud MS, Bari ML, Hossain MA. Prevalence of Salmonella serovars and antimicrobial resistance profiles in poultry of Savar area, Bangladesh. Foodborne Pathog Dis. 2011;8(10):1111–1118.
33. Nguyen TK, Nguyen LT, Chau TTH, et al. Prevalence and antibiotic resistance of Salmonella isolated from poultry and its environment in the Mekong Delta, Vietnam. Vet World. 2021;14(12):3216–3223.
34. Moe AZ, Paulsen P, Pichpol D, et al. Prevalence and antimicrobial resistance of Salmonella isolates from chicken carcasses in retail markets in Yangon, Myanmar. J Food Prot. 2017;80(6):947–951.
35. Thung TY, Mahyudin NA, Basri DF, et al. Prevalence and antibiotic resistance of Salmonella enteritidis and Salmonella typhimurium in raw chicken meat at retail markets in Malaysia. Poult Sci. 2016;95(8):1888–1893.
36. Zwe YH, Tang VCY, Aung KT, et al. Prevalence, Sequence types, antibiotic resistance and, gyrA mutations of Salmonella isolated from retail fresh chicken meat in Singapore. Food Control. 2018;90:233–240.
37. Iwabuchi E, Yamamoto S, Endo Y, et al. Prevalence of Salmonella isolates and antimicrobial resistance patterns in chicken meat throughout Japan. J Food Prot. 2011;74(2):270–273.
38. Kim MS, Lim TH, Jang JH, et al. Prevalence and antimicrobial resistance of Salmonella species isolated from chicken meats produced by different integrated broiler operations in Korea. Poult Sci. 2012;91(9):2370–2375.
39. Sodagari HR, Mashak Z, Ghadimianazar A. Prevalence and antimicrobial resistance of Salmonella serotypes isolated from retail chicken meat and giblets in Iran. J Infect Dev Ctries. 2015;9(5):463–469.
40. Kuang X, Hao H, Dai M, et al. Serotypes and antimicrobial susceptibility of Salmonella spp. isolated from farm animals in China. Front Microbiol. 2015;6:602.
41. Rau RB, Ribeiro AR, dos Santos A, et al. Antimicrobial resistance of Salmonella from poultry meat in Brazil: results of a nationwide survey. Epidemiology & Infection. 2021;149:E228.
42. FDA. Extralabel use and antimicrobials. U.S. Department of health and human services, Rockville, MD, USA. 2018.
43. Rothrock MJ, Guard JY, Oladeinde A. Salmonella diversity along the farm-to-fork continuum of pastured poultry flocks in the southeastern United States. Frontiers in Animal Science. 2021;2:761930.
44. Ahmed AO, Raji MA, Mamman PH, et al. Salmonellosis: Serotypes, prevalence and multi-drug resistant profiles of Salmonella enterica in selected poultry farms, Kwara State, North Central Nigeria. Onderstepoort J Vet Res. 2019;86(1):e1–e8.
45. Ibrahim S, Wei Hoong L, Lai Siong Y, et al. Prevalence of antimicrobial resistance (AMR) Salmonella spp. and Escherichia coli isolated from broilers in the East Coast of Peninsular Malaysia. Antibiotics (Basel). 2021;10(5):579.
46. Nhung NT, Cuong NV, Campbell J, et al. High levels of antimicrobial resistance among Escherichia coli isolates from livestock farms and synanthropic rats and shrews in the Mekong Delta of Vietnam. Appl Environ Microbiol. 2015;81(3):812–820.
47. Dione MM, Ikumapayi UN, Saha D, et al. Clonal differences between non-typhoidal Salmonella (NTS) recovered from children and animals living in close contact in the Gambia. PLoS Negl Trop Dis. 2011;5(5):e1148.
48. Djeffal S, Mamache B, Elgroud R, et al. Prevalence and risk factors for Salmonella spp. contamination in broiler chicken farms and slaughterhouses in the northeast of Algeria. Vet World. 2018;11(8):1102–1108.
49. EFSA. Scientific opinion of the panel on biological hazards on a request from the European food safety authority on foodborne antimicrobial resistance as a biological hazard. The EFSA Journal. 2008;765:1–87.
50. Marshall BM, Levy SB. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev. 2011;24(4):718–733.
51. Tollefson L, Karp B. Human health impact from antimicrobial use in food animals. Med Infect Dis. 2004;34(11):514–521.