African Journal of
Microbiology Research

  • Abbreviation: Afr. J. Microbiol. Res.
  • Language: English
  • ISSN: 1996-0808
  • DOI: 10.5897/AJMR
  • Start Year: 2007
  • Published Articles: 5137

Full Length Research Paper

Molecular detection and characterization of Escherichia coli, Salmonella spp. and Campylobacter spp. isolated from broiler meat in Jamalpur, Tangail, Netrokona and Kishoreganj districts of Bangladesh

Md. Kamrul Islam
  • Md. Kamrul Islam
  • Department of Microbiology and Hygiene, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh.
  • Google Scholar
S. M. Lutful Kabir
  • S. M. Lutful Kabir
  • Department of Microbiology and Hygiene, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh.
  • Google Scholar
A. K. M. Ziaul Haque
  • A. K. M. Ziaul Haque
  • Department of Microbiology and Hygiene, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh.
  • Google Scholar
Y. A. Sarker
  • Y. A. Sarker
  • Department of Pharmacology, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh.
  • Google Scholar
M. H. Sikder
  • M. H. Sikder
  • Department of Pharmacology, Bangladesh Agricultural University, Mymensingh-2202, Bangladesh.
  • Google Scholar


  •  Received: 23 July 2018
  •  Accepted: 13 August 2018
  •  Published: 28 August 2018

 ABSTRACT

The study was conducted to isolate, identify and characterize bacterial samples from broiler meat collected from 20 different upazilla markets of Jamalpur, Tangail, Netrokona and Kishoreganj districts of Bangladesh. A total of 20 samples were subjected to bacteriological isolation and identification, and the isolated bacteria were subjected to antimicrobial susceptibility testing using disc diffusion method. Among the samples, 75% (n=15) were contaminated with Campylobacter spp., 70% (n=14) were with Salmonella species and 85% (n=17) were contaminated with Escherichia coli. The Campylobacter spp., Salmonella spp. and E. coli were isolated and identified by culturing on Blood agar, Xylose-Lysine Deoxycholate (XLD) agar, and MacConky and eosin methylene blue (EMB) agar respectively. Isolates of Campylobacter spp., Salmonella spp. and E. coli were biochemically analyzed. Campylobacter specific 16S rRNA genes were amplified from the isolates. Campylobacter spp. and E. coli isolates were positive to 16S rRNA gene based polymerase chain reaction (PCR). Almost all isolates of Campylobacter spp., Salmonella spp. and E. coli showed highest susceptibility to ciprofloxacin, norfloxacin and gentamicin. However, most isolates were resistant to amoxicillin and erythromycin. Some isolates showed susceptibility to tetracycline, streptomycin and azithromycin. The findings of this study revealed that there is presence of multidrug resistant isolates of Campylobacter spp., Salmonella spp. and E. coli in broiler meat. Results of this research project demonstrated the high level of microbial contamination and occurrence of pathogenic bacteria in broiler meat sold in markets of Bangladesh.

 

Key words: Broiler meat, Escherichia coli, Salmonella, Campylobacter, molecular detection, characterization.


 INTRODUCTION

Poultry industry which has started during 1980s is an excellent agribusiness (Haque, 2001) now in Bangladesh. Over the last decades surprising development has occurred in this sector (Rahman,  2003). It has become a
 
vital sector for generating employment, creating additional income and improving the nutritional level of the country. Broiler meat is more popular to the consumers because of its easy digestibility and acceptance by the majority of people, although it could be contaminated with various potential food borne pathogens such as Salmonella, Campylobacter, Escherichia coli (Mulder et al., 1999). Broiler entering slaughter processing is highly contaminated by microorganisms such as Salmonella and Campylobacter and tends to be disseminated during processing (Mead et al., 1994).
 
Particular concern for human health is the inappropriate use of antibiotics in poultry production and the development of antibiotic resistant strains of bacteria (Sarker et al., 2018). Effective control systems are critical in ensuring product safety, and considerable information is available on how to minimize the risks (FAO, 2013). Various pathogenic microbes, such as E. coli, Salmonella spp. and Staphylococcus have been implicated to reduce the growth of poultry including duck.
 
Campylobacter is one of the most important pathogen and is regarded major bacterial cause of human gastroenteritis worldwide. Food animals, mainly poultry, cattle, sheep and pigs, may act as asymptomatic intestinal carriers of Campylobacter and animal food products can become contaminated by this pathogen during slaughter and carcass dressing (Berndtson et al., 1996). The abusive use of antimicrobials in food animals has resulted in the emergence and dissemination of antimicrobial resistant bacteria, including antimicrobial resistant Campylobacter, which has potentially serious impact on human health. Moreover, Campylobacter infections pose a serious public health problem for which many countries have monitored their infection and antimicrobial resistance patterns (Kabir et al., 2014). E. coli frequently cause bacterial infections including urinary tract infection, cholangitis, bacterimia and traveler’s diarrhea. Enteropathogenic E. coli (EPEC) are an important cause of diarrhea in humans (Savkovic et al., 2005). Haemolytic uramic syndrome caused by Shiga toxin producing E. coli (STEC) is dependent on release of Shiga toxin during intestinal infection and subsequent absorption into the blood stream. Poultry meat can be contaminated with E. coli during processing. Any food that has been in contact with raw meat can also be contaminated. The bacteria also spread from person to person, usually when infected person does not wash his hands well after using a toilet. E. coli cause different types of public health hazards including cholangitis, bacteremia, traveler’s diarrhea, Shiga toxicity etc. (Savkovic et al., 2005).
 
Salmonella spp. is potentially responsible for various pathogenic processes in man and animal including poultry (Freeman, 1985). It can cause diarrhea, vomition, fever, abdominal cramps in human. Sometimes severe diarrhea     requires medical   interventions such as intravenous fluid therapy. In cases, where bacteria enter into the bloodstream, symptoms include high fever, malaise, pain in the thorax and abdomen, chills and anorexia (Bell, 2002).
 
Antibiotics are extensively used in poultry industry either as growth promoters or to control infectious diseases (Sarker et al., 2018). Concern about antibiotic resistance and its transmission to human is important because these resistant bacteria may colonize the human gastrointestinal tract and may contribute to the development of resistance genes to human through R-factor, conjugative plasmids or chromosomal elements as reviewed by Kabir (2010). Therefore, the disease causing microbes that have become resistant to antibiotic drug therapy are increasing public health importance.
 
Undoubtedly, the poultry slaughtered and dressed under Bangladesh conditions carry extremely high initial contamination loading from the point of slaughtering process to the point at which the consumers are offered the product. There occurs biomagnifications at all levels of handling, poor transport and retailing conditions. Therefore, considering the present perspective, the present research project was designed to detect and characterize the bacteria specifically Campylobacter spp. Salmonella spp. and E. coli and their antimicrobial resistance patterns in broiler meat.

 


 MATERIALS AND METHODS

Collection and transportation of samples
 
A total of 20 apparently healthy dressed broilers were collected randomly from 20 different upazilla live bird markets of Jamalpur, Tangail, Kishoreganj and Netrokona district of Bangladesh. Five upazilla were selected randomly from each district. After collection, samples were immediately brought to Bacteriology Laboratory of the Department of Microbiology and Hygiene, Bangladesh Agricultural University, Mymensingh through maintaining cool chain using ice box.
 
 
Bacterial culture media
 
Solid and liquid culture media were used to isolate the bacteria. Blood agar (BA), MacConkey (MC), Salmonella-Shigella (SS), Eosin Methylene Blue (EMB), Xylose-Lysine Deoxycholate (XLD), Mueller Hinton agars were used as solid culture media for this study. The liquid media used in the study were nutrient broth (NB), peptone broth, methyl-red and voges-proskauer broth (MR-VP), and sugar media, 1% hippurate solution, 3.5% ninhydrin solution, oxidase solution and sugar media.
 
 
Isolation and identification of bacteria
 
Pure culture of E. coli and Salmonella spp. were obtained as per the methods described by Krieg et al. (1994). Briefly; 10 g of samples were homogenized with 90 ml of 0.1% peptone water and 50 µl of homogenized sample was poured on to selective agar media and spread with glass spreader and incubated at 37°C for 24 h. Isolation of Campylobacter spp. was carried out by filtration method (0.45 μm filter)  according  to  Shiramaru  et  al. (2012). The collected samples were allowed to prepare meat homogenates and then 50 μl of meat homogenates were spread on the filter papers that were placed on the surface of Blood base agar no.2 and allowed to stand for 30 min at room temperature, after 30 min filter papers were removed from the BA and the plates were incubated at 37°C for 48 h in microaerobic condition (5% O2, 10% CO2 and 85% N2). The colonies of primary cultures were repeatedly sub-cultured by streak plate method (Cheesbrough, 1985) until the pure cultures with homogenous colonies appeared. The representative bacterial colonies were characterized morphologically using Gram's stain according to the method describe by Merchant and Packer (1967). Biochemical characterizations of the E. coli and Salmonella isolates were performed with Sugar fermentation test, Methyl Red test (MR), Voges-Proskauer test (V-P) and indole test (Cheesbrough, 1985). Differentiation of isolated Campylobacter spp. with supporting growth characteristics were subjected to various biochemical tests such as catalase, oxidase and hippurate hydrolysis test according to the procedures followed by Nachamkin (2003) and Foster et al. (2004).
 
Molecular identification by polymerase chain reaction (PCR)
 
DNA template was prepared by boiling method as described by Rawool et al. (2007). All the samples were examined by two pairs of primers (Table 1) to detect 16S rRNA gene of Campylobacter spp., E. coli and Histidine transport operon gene of Salmonella spp. For Campylobacter  spp. the PCR reactions were carried out using a thermocycler (ASTEC, Japan) with the following programme: initial denaturation for 5 minutes at 94°C, followed by 30 cycles of denaturation at 94°C for 30 s, annealing at 47°C for 30 s and extension at 72°C for 1 min and 30 s. The final extension was conducted at 72°C for 10 min. For E. coli, the PCR reactions were carried out using a thermocycler (ASTEC, Japan) with the following programme: Initial denaturation for 5 min at 95°C followed by 30 cycles of denaturation at 94°C for 45 s, annealing at 55°C for 45 s and extension at 72°C for 1 min. The final extension was conducted at 72°C for 5 min. For Histidine transport operon gene identification in Salmonella spp. initial denaturation for 5 min at 94°C, followed by 30 cycles of denaturation at 94°C for 30 s, annealing at 56°C for 30 s and extension at 72°C for 45 s. The final extension was conducted at 72°C for 5 min. 1 and 2% agarose (Invitrogen, USA) gel was used for electrophoresis of the PCR products.
 
 
Antibiotic sensitivity test
 
All isolates randomly selected from the three genera were tested for antimicrobial   drug   susceptibility   against   eight  commonly  used antibiotics by disc diffusion method according to the guidelines of Clinical and Laboratory Standard Institute (CLSI), 2012. The selected antibiotics used were ciprofloxacin (5 μg/disc), azithromycin (30 μg/disc), amoxicillin (30 μg/disc), gentamicin (10 μg/disc), Norfloxacin (10 μg/disc), erythromycin (30 μg/disc), streptomycin (10 μg/disc), and tetracycline (30 μg/disc). The interpretation on susceptibility was done according to the guidelines of Clinical and Laboratory Standard Institute (CLSI, 2007) (Table 1).

 


 RESULTS

Isolation of bacteria from poultry meat
 
A total of 20 samples were collected for isolation of bacteria from broiler meat of different upazilla markets of four districts where three types of bacteria were isolated from the collected meat samples. The isolates were identified as E. coli, Salmonella spp. and Campylobacter spp. on the basis of their morphological, cultural properties, biochemical characteristics with standard reference organisms and molecular methods. Among the isolated bacteria, E. coli were detected in 85% (n=17), Salmonella and Campylobacter in 70% (n=14) and 75% (n=15), respectively of the samples. The highest percentage of E. coli (100%) isolates was observed in Jamalpur and Tangail district. Salmonella isolates were higher (80%) in samples of Jamalpur, Tangail and Kishoreganj. Furthermore, Campylobacter isolates were 100% in samples of Jamalpur District.
 
Molecular detection of bacteria
 
Screening of E. coli isolates from meat sample in this study was performed by genus specific (16S rRNA gene) polymerase chain reaction (PCR). The PCR assay was able to amplify 585 bp fragment of the targeted gene from the genomic DNA of E. coli successfully (Figure 1). Specific 496 bp fragment of targeted histidine transport operon gene of Salmonella was amplified successfully (Figure 2). Genus specific (16S rRNA gene) PCR was performed  for  Campylobacter  spp. 1530  bp fragment of targeted gene was amplified successfully. The result of PCR is presented in Figure 3.
 
 
 
Antimicrobial susceptibility of isolated E. coli, Salmonella and Campylobacter spp.
 
A total of 17 E. coli isolates were subjected to antimicrobial susceptibility testing. Most of the isolates were resistant to erythromycin (70.58%) and amoxicillin (88.24%) and few isolates were intermediate. Almost all the isolates of E. coli showed their highest sensitivity to gentamicin (76.47%), norfloxacin (82.35%), ciprofloxacin (82.35%) and azithromycin (64.70%). Some isolates of E. coli were resistant and some were sensitive to tetracycline. The result is presented in Table 2.  A total of 14 Salmonella isolates were subjected to antimicrobial susceptibility testing against eight selected antibiotics. Almost all isolates of Salmonella spp. were resistant to tetracycline (85.71%) and erythromycin (64.28%) whereas most of the isolates of Salmonella spp. were susceptible to gentamicin (92.85%), norfloxacin (78.57%) and ciprofloxacin (78.57%) respectively. 5 (35.71%) were sensitive to streptomycin and 10 (71.42%) isolates were intermediate to amoxicillin. Results are presented in Table 2.
 
 
The result of antimicrobial susceptibility of Campylobacter jejuni and Campylobacter coli are summarized in Table 2. Out of 11 C. jejuni isolates, 10 (90.90%) isolates were susceptible to gentamicin, 9 (81.81%) were sensitive to  norfloxacin,  8  (72.72%)  were sensitive to ciprofloxacin and 7 (63.63%) were susceptible to streptomycin. Most of the isolates were resistant to amoxicillin (81.81%) and 9 (81.81%) isolates were intermediate resistant to erythromycin. On the other hand, out of four C. coli isolates, all (100%) were sensitive to both ciprofloxacin and norfloxacin. 3 (75%) were sensitive to gentamicin, and 4 (100%) were resistant to amoxicillin, 2 were resistant to streptomycin.
 
Antimicrobial resistance pattern
 
Antimicrobial resistance pattern of E. coli
 
The results of the antimicrobial resistance pattern by disk diffusion method with 8 chosen antimicrobial agents are presented in Table 3. Out of 17 isolates, 6 (35.29%) were resistant to 1 antimicrobial agent. Each 1 (5.88%) was resistant to each of 2 antibiotics. Moreover, 2 (11.76%) were resistant to 2 antibiotics. Furthermore, each 1 (5.88%) was resistant to each of 3 antibiotics.
 
Antimicrobial resistance pattern of Salmonella spp.
 
The results of the antimicrobial resistance pattern by disk diffusion method with 8 chosen antimicrobial agents are presented in Table 4. Out of 14 isolates no resistance observed in 1 isolate. 1 (7.14%) was resistant to 1 antibiotics. Furthermore, each 2 (14.28%) were resistant to each of 2 antibiotics. Moreover, 1 (7.14%), 2 (14.28%), 1 (7.14%) and 1 (7.14) were resistant to each of 3 antibiotics respectively. Furthermore, 1 (7.14%) and 1 (7.14%) were resistant to each of 4 antimicrobial agents. On the other hand, 1 was resistant to 5 antimicrobial agents.
 
Antimicrobial resistance pattern of Campylobacter spp.
 
The result of antimicrobial resistance patterns of C. jejuni and C. coli are summarized in Table 5. Out of 11 C. jejuni isolates,   each    1    (9.09%)     was     resistant    to    each   1 antimicrobial agent. Furthermore, 3 (27.27%) and 1 (9.09%) were resistant to each of 2 antibiotics respectively. Moreover, 1 (9.09%) and 1 (9.09%) were resistant to each of 3 antibiotics. On the other hand, 1 (9.09%) and 1 (9.09%) were resistant to each of 3 and 4 antibiotics respectively. Out of 4 C. coli isolates, each 1 (25%) were resistant to each of 1 antibiotic. Furthermore, 2 (50%) were resistant to 3 antibiotics.
 
 
 

 


 DISCUSSION

Meat  products  are  important  not  only   from  nutritional  point of view, but also as an item of international trade and foreign exchange for a number of countries. However, they can also function as carriers of several microbial and other health hazards. The greatest risk to human health is due to the consumption of raw or contaminated meat and meat products.
 
In this study, E. coli, Salmonella and Campylobacter were found in the poultry meat, which was similar to the reports by Zhao et al. (2001), Ahmed et al. (2009), Awad-Alla et al. (2010), Torok et al. (2011), Voidarou et al. (2011), Sudershan et al. (2012), Malmuthuge et al. (2012) and Hossain et al. (2015). Several selective culture media were used simultaneously in this study to culture the organism. The media used in this study were selected considering the experience of the past researcher worked in various fields relevant to the present study by Kabir et al. (2014). The colony characteristics of Campylobacter spp. were gray color spreading colony which was supported by (Doyle, 1990; Rowe and Madden, 2000). In Gram's staining, the morphology of the isolated Campylobacter spp. was also supported by Doyle (1990). The colony characteristics of E. coli observed in Mac conkey, EMB agar were similar to the findings of Sharada et al. (1999). And in gram staining isolated bacteria showed pink color small rod shaped organism which was reported by others previously Sharada et al. (1999) and Merchant and Packer (1967). The colony morphology of Salmonella spp. was similar to that of Sarker et al. (2009) and Khan et al. (2005). In Gram's staining, the morphology of the isolated bacteria exhibited Gram negative small rod arranged in single or paired and motile which was supported by Sharada et al. (1999).
 
In catalase test, all the isolates (n = 15) produced bubbles those indicated positive for Campylobacter. In oxidase test, a purple color change was observed within ten seconds in all the isolates (n=15). In hippurate hydrolysis test, some of the isolates (n=4) develop a faint purple to no color change that indicated the isolates were C. coli and some of the test isolates (n=11) developed deep purple color that indicated the isolates were C. jejuni. These findings are similar to the findings of Kabir et al. (2014) and Jamshidi et al. (2008).
 
The E. coli isolates revealed a complete fermentation of 5 basic sugars by producing both acid and gas which was supported by Thomas (1998) and Beutin et al. (1991). The isolates also revealed positive reaction in MR test and Indole test but negative reaction in VP test (Honda et al., 1982). The antimicrobial susceptibility of most of the isolates was sensitive to ciprofloxacin; gentamicin and all the isolates were resistant to amoxycillin. Some of the isolates were multidrug resistant which was similar to the result of Kabir et al. (2014). In this study, it was observed that the E. coli isolates were sensitive to ciprofloxacin, norfloxacin and gentamicin. The results strengthen the earlier observations of Akond et al. (2009) and Islam et al. (2004). Resistance  of  E.  coli  was  observed  against erythromycin, amoxycillin. The result was supported by Akond et al. (2009). The cause of such resistance by the E. coli might be for the fact that the organisms might have gained the resistance property due to the indiscriminate use of antibiotics.
 
The occurrence of isolation of bacterial pathogens from broiler should be considered as hazardous to health and advocate the preventing risk factors. However, in the present study ciprofloxacin were proved to be the best antibiotics to treat E. coli infection since they were highly effective. The results agreed with those reported by several investigations of Islam et al. (2004) and Ozaki et al. (2011) who also obtained similar resistant patterns of E. coli isolated from broiler. It was revealed that Salmonella spp. were sensitive to ciprofloxacin, gentamicin and norfloxacin. This result was supported by Jahan et al. (2013) and Khan et al. (2005) where isolates were sensitive to ciprofloxacin and chloramphenicol. The result is also consistent with Wouafo et al. (2010). The isolates were resistant to erythromycin, and amoxycillin which is similar to report of Hyeon et al. (2011) and Khan et al. (2005).


 CONCLUSION

In this study, bacteria were isolated from only 20 samples of 20 different upazila of Bangladesh. The findings of the present study revealed the presence of multidrug resistant bacteria in broiler meat sold in markets of Bangladesh. Most of the isolates showed resistance to amoxycillin but sensitive to ciprofloxacin and gentamicin. Some isolates showed multidrug resistance.

 


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.

 


 ACKNOWLEDGEMENTS

This study was performed in partial fulfillment of the requirements of a M.S. thesis for Md. Kamrul Islam from the Department of Microbiology and Hygiene, Bangladesh Agricultural University, Mymensingh, Bangladesh. We would also like to thank the Food and Agriculture Organization of the United Nations (FAO) for giving financial and logistic support to the present research project and management of this research.

 



 REFERENCES

Ahmed AM, Shimabukuro H, Shimamoto T (2009). Isolation and molecular characterization of multidrug-resistant strains of E. coli and Salmonella from retail chicken meat in Japan. Journal of Food Science 74:405-410.
Crossref

 

Akond MA, Hassan SMR, Alam S, Shirin M (2009). Antibiotic resistance of E. coli isolated from poultry and poultry environment of Bangladesh. American Journal of Environmental Science 5:47-52.
Crossref

 
 

Awad-Alla ME, Abdien HM, Dessouki AA (2010). Prevalence of bacteria and parasites in White Ibis in Egypt. Veterinaria Italians 46: 277-86.

 
 

Bell C (2002). Foodborne pathogens: Hazards, risk analysis and control. Woodhead Publishing and CRC Press pp. 307-335.

 
 

Berndtson E, Emanuelson U, Engvall A, Danielsson-Tham ML (1996). A 1-year epidemiological study of Campylobacters in 18 Swedish chicken farms. Preventive Veterinary Medicine 26:167-185.
Crossref

 
 

Beutin L, Geier D, Zimmeronann S, Aleksic S, Gillespie HA, Whittarn TS (1991). Epidemiological relatednes and clonal types of natural populations of E. coli strains producing shiga toxin between stx genotype and Stx2 expression level in Shiga 96 toxin-producing E. coli 0157 strain in separate population of cattle and sheep. Applied and Environmental Microbiology 63:2175-2180.

 
 

Cheesbrough M (1985). Medical laboratory manual for tropical countries. Microbiology 2:400-480.

 
 

Clinical and Laboratory Standards Insitute (CLSI) (2007). M100-S17. Performance standards for antimicrobial susceptibility testing; 16th informational supplement. Clinical and Laboratory Standards Institute, Wayne, PA.

 
 

Clinical and Laboratory Standards Insitute (CLSI) (2012). Performance Standards for Antimicrobial Susceptebility Testing: Twenty-second Informational Supplement M100-S22. CLSI, Wayne, PA, USA.

 
 

Cohen ND, Neibergs HL, McGruder ED, Whitford H, Behle RW, Ray PM, Hargis BM (1993). Genus-specific detection of salmonellae using the polymerase chain reaction (PCR). Journal of Veterinary Diagnostic Investigation 5:368-371.
Crossref

 
 

Doyle MP (1990). C. jejuni, p. 217-222. In D. O. Cliver (ed.), Foodborne diseases. Academic Press, Inc., Boston, MA.

 
 

FAO (2013). Food and Agricultural Organization of the United Nation report on Poultry and Human Health. Publication on Veterinary Public Health.

 
 

Foster G, Holmes B, Steigerwalt AG, Lawson PA, Thorne P, Byrer DE, Ross HM, Xerry J, Thompson PM, Collins MD (2004). Campylobacter insulaenigrae sp. nov., isolated from marine mammals. International Journal of Systematic and Evolutionary Microbiology 54: 2369-2373.
Crossref

 
 

Freeman BA (1985). Burrows Textbook of Microbiology. In: W. B. Saunders company, philadephia, London, Toronto, Mexico city, Rio de Janerio, Sydney, Tokyo. 22: 464-475.

 
 

Haque QMF (2001). Poultry industry in Bangladesh and strategies for its improvement. In Proceedings of 2nd International Poultry Show and Seminar, February 2001, held in IDB Bhaban, Dhaka, Bangladesh. pp. 34-39.

 
 

Honda T, Arita M, Takela Y, Miwatani T (1982). Further evaluation of the Biken Test (Modified Eleck Test) for deletion of enterotoxigenic E. coli producing heat stable enterotoxin and application of the test to sampling of heat stable enterotoxin. Journal of Clinical Microbiology 16:60-62

 
 

Hossain M, Hoda N, Hossen MJ, Hassan MM, Rahman SME, Kabir SML (2015). Assessment of bacterial load of poultry meat used at dining hall of Bangladesh Agricultural University campus. Asian Journal of Medical and Biological Research 1:9-16.
Crossref

 
 

Hyeon JY, Chon JW, Hwang IG, Kwak HS, Kim MS, Kim SK, Choi IS, Song CS, Park C, Seo KH (2011). Prevalence, antibiotic resistance, and molecular characterization of Salmonella serovars in retail meat products. Journal of Food Protection 74:161-6.
Crossref

 
 

Islam MT, Islam MA, Samad MA, Kabir SML (2004). Charachterization and antibiogram of Eshcherechia coli associated with mortality in broilers and duckling in Bangladesh. Bangladesh Journal of Veterinary Medicine 2:9-14.

 
 

Jahan F, Kabir SML, Amin MM (2013). Identification and antimicrobial resistance profiles of Salmonellae isolated from the broiler dressing plants associated with their environments. Advanced Research Journal of Microbiology 1:001-009.

 
 

Jamshidi A, Bassami MR, Farkhondeh L (2008). Isolation and identification of Campylobacter spp. and C. coli from poultry carcasses by conventional culture method and multiplex PCR in Mashhad, Iran. Iranian Journal of Veterinary Research 9:132-137.

 
 

Kabir SML (2010). Avian Colibacillosis and Salmonellosis: A closer look at Epidemiology, pathogenesis, Diagnosis, Control and Public Health Concerns. International Journal of Environmental Research and Public Health 7:89-114.
Crossref

 
 

Kabir SML, Sumon MH, Amin MM, Yamasaki S (2014). Isolation, Identification and Antimicrobial Resistance Patterns of Campylobacter Species from Broiler Meat Sold at KR Market of Bangladesh Agricultural University Campus, MymensinghJournal of Agriculture and Food Technology 4:15-21.

 
 

Khan MFR, Rahman MB, Sarker SK (2005). Seroprevalence of Mycoplasma gallisepticum infection in poultry in some selected farms of Mymensingh. Journal of Bangladesh Society for Agricultural Science and Technology 2:1-4.

 
 

Krieg NR, Holt JG, Sneath PHA, Staley JT, Williams ST (1994). Bergey's Manual of Determinative Bacteriology, Williams & Wilkins, Baltimore, Md, USA, 9th edition.

 
 

Malmuthuge N, Li M, Chen Y, Fries P, Griebel PJ, Baurhoo B, Zhao X, Guan LL (2012). Distinct commensal bacteria associated with ingests and mucosal epithelium in the gastrointestinal tracts of calves and chickens. FEMS Microbiology Ecology 79:337-47.
Crossref

 
 

Mead GC, Hudson WR and Hiton MH (1994). Use of a marker organism in poultry processing to identify sites of cross-contamination and evaluate possible measures. British Poultry Science 35:345-354.
Crossref

 
 

Merchant IA, Packer RA (1967). Veterinary Bacteriology and Virology. Lowa State University Press, Ames. Lowa USA. 7:286- 306.

 
 

Mulder RWAW, Schlundt J (1999). Safety of poultry meat: from farm to table. In: International Consultative Group on Food Irradiation (ICGFI), FAO/IAEA/WHO.

 
 

Nachamkin I (2003). Campylobacter and Arcobacter, pp. 902-914. In: P. R. Murray, E. J. Baron, J. H. Jorgensen, M. A. Pfaller, and R. H. Yolken (ed.), Manual of Clinical Microbiology, ASM Press, Washington, D.C.

 
 

Ozaki H, Esaki H, Takemoto K, Ikeda A, Nakatani Y, Someya A, Hirayama N, Murase T (2011). Antimicrobial resistance in fecal E. coli isolated from growing chickens on commercial broiler farms. Journal of Veterinary Microbiology 150:13-2¬9.

 
 

Rahman MM (2003). Growth of poultry industry in Bangladesh, poverty alleviation and employment opportunity. Proceeding of 3rd international poultry show and seminar, Bangladesh china friendship conference centre, Dhaka, Bangladesh, 28th February - 2nd March 2003.

 
 

Rawool DB, Malik SVS, Barbuddhe SB, Shakuntala I, Aurora R (2007). A multiplex PCR for detection of virulence associated genes in Listeria monocytogenes. International Journal of Food Safety 9:56-62.

 
 

Rowe MT, Madden RH (2000). Campylobacter: Introduction, In: Robinson, R. K.; Batt, C. A. and Patel, P. D. (eds.), Encyclopedia of food microbiology. Academic Press, San Diego, CA. pp. 335-341.

 
 

Samosornsuk W, Asakura M, Yoshida E (2007). Evaluation of a cytolethal distending toxin (cdt) gene-based species-specific multiplex PCR assay for the identification of Campylobacter strains isolated from poultry in Thailand. Microbiology and Immunology 51:909-917.
Crossref

 
 

Sarker SK, Rahman MB, Rahman M, Khan MFR, Akand MSI, Rahman MS (2009). Seroprevalence study, isolation and identification of Salmonella in chickens selected model breeder poultry farms of Bangladesh. International Journal of Bio Research 2:25-29.

 
 

Sarker YA, Hasan MM, Paul TK, Rashid SZ, Alam MN, Sikder MH (2018). Screening of antibiotic residues in chicken meat in Bangladesh by thin layer chromatography. Journal of Advanced Veterinary and Animal Research 5(2):140-145.
Crossref

 
 

Savkovic SD, Villanueva J, Turner JR, Matkowskyj KA, Hecht G (2005). Mouse model ofbenteropathogenic E. coli infection. Infectious and Immunity 73:1161-1170.
Crossref

 
 

Schippa S, Iebba V, Barbato M, Nardo GD, Totino V, Checchi MP, Longhi C, Maiella G, Cucchiara S, Conte MP (2010). A distinctive 'microbial signature' in celiac pediatric patients. BMC Microbiology 10:175.
Crossref

 
 

Sharada R, Krishnappa G, Raghavan R, Sreevinas G, Upandra HA (1999). Isolation and serotyping of E. coli from different pathological conditions in poultry. Indian Journal of Poultry Science 34:366-369.

 
 

Shiramaru S, Asakura M, Inoue H, Nagita A, Matsuhisa A, Yamasaki S (2012). A cytolethal distending toxin gene-based multiplex PCR assay for detection of Campylobacter spp. in stool specimens and comparison with culture method. The Journal of Veterinary Medical Science 74:857-862.
Crossref

 
 

Sudershan RV, Naveen Kumar R, Kashinath L, Bhaskar V, Polasa K (2012). Microbiological hazard identification and exposure assessment of poultry products sold in various localities of Hyderabad, India. Scientific World Journal 12:736-40.
Crossref

 
 

Thomas CGA (1998). Gram negative bacilli. Medical Microbiology 6:273-274.

 
 

Torok VA, Hughes RJ, Mikkelsen LL, Perez-Maldonado R, Balding K, MacAlpine R, Percy NJ, Ophel-Keller K (2011). Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials. Applied and Environmental Microbiology 77:5868-5878.
Crossref

 
 

Voidarou C, Vassos D, Rozos G, Alexopoulos A, Plessas S, Tsinas A, Skoufou M, Stavropoulou E, Bezirtzoglou E (2011). Microbial challenges of poultry meat production. Anarobe 17:341-343.
Crossref

 
 

Wouafo M, Nzouankeu A, Kinfack JA, Fonkoua MC, Ejenguele G, Njine T, Ngandjio A (2010). Prevalence and antimicrobial resistance of Salmonella serotypes in chickens from retail markets in Yaounde (Cameroon). Microbial Drug Resistance 16:171-176.
Crossref

 
 

Zhao C, Ge B, De Villena J, Sudler R, Yeh E, Zhao S, Meng J (2001). Prevalence of Campylobacter spp., E. coli, and Salmonella serovars in retail chicken, turkey, pork, and beef from the Greater Washington, DC, area. Applied and Environmental Microbiology 67:5431-5436.
Crossref

 

 




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