Prevalence, antibiotic resistance and RAPD typing of Campylobacter species isolated from ducks, their rearing and processing environments in Penang, Malaysia

International Journal of Food Microbiology

Volumn 154, Issue 3, 2012, Pages 197-205

  Adzitey, Frederick ^a,b   Rusul, Gulam ^a   Huda, Nurul ^a   Cogan, Tristan ^c   Corry, Janet ^c  

^a Universiti Sains Malaysia   (Malaysia)

^b UNIVERSITY FOR DEVELOPMENT STUDIES   (Ghana)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Antibiotics; Campylobacter species; Ducks; Prevalence; RAPD

Indexed keywords

CEFALOTIN; CEFOTAXIME; CEFTRIAXONE; CHLORAMPHENICOL; CIPROFLOXACIN; COTRIMOXAZOLE; ERYTHROMYCIN; GENTAMICIN; NALIDIXIC ACID; NORFLOXACIN; STREPTOMYCIN; TETRACYCLINE;

AGAR DILUTION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM ISOLATION; BROTH DILUTION; CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; CAMPYLOBACTER LARI; CONTROLLED STUDY; DUCK; FOOD PROCESSING; GENETIC VARIABILITY; MALAYSIA; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PREVALENCE; RANDOM AMPLIFIED POLYMORPHIC DNA; REARING;

ANIMALS; ANTI-BACTERIAL AGENTS; CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; DRUG RESISTANCE, MICROBIAL; DUCKS; FOOD HANDLING; MALAYSIA; MEAT; PREVALENCE; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE;

ANAS; CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; CAMPYLOBACTER LARI;

EID: 84857048246     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2012.01.006     Document Type: Article

References (50)

1. Adzitey F., Corry J.E.L. A comparison between hippurate hydrolysis and multiplex PCR for differentiating C. coli and C. jejuni. Tropical Life Sciences Research 2011, 22:57-64.
2. Adzitey F., Nurul H. Campylobacter in poultry: incidences and possible control measures. Research Journal of Microbiology 2011, 6:182-192.
3. Adzitey, F., Rusul, G., Huda, N., in press. Prevalence and antibiotic resistance of Salmonella serovars in ducks, duck rearing and processing environments in Penang, Malaysia. Food Research International. doi: 10.1016/j.foodres.2011.02.051.
4. Ang C.W., De Klerk M.A., Endtz H.P., Jacobs B.C., Laman J.D., Van der Meche F.G., Van Doorn P.A. Guillain-barre syndrome and Miller Fisher syndrome-associated Campylobacter jejuni lipopolysaccharides induce anti-GM1 and anti-GQ1b antibodies in rabbits. Infection and Immunity 2001, 69:2462-2469.
5. Anonymous Asia dominates world waterfowl production Available at:, [accessed 18 February 2010]. http://www.thepoultrysite.com/articles/1633/asia-dominates-world-waterfowl-production.
6. Arun K.B. Foodborne Microbial Pathogens: Mechanisms and Pathogenesis Campylobacter and Arcobacter 2008, 217-226. Springer Publisher, New York.
7. Bauer A.W., Kirby W.M.M., Sherris J.C., Turk M. Antibiotic susceptibility testing by a standardized single disc method. American Journal of Clinical Pathology 1966, 45:493-496.
8. Bereswill S., Kist M. Recent developments in Campylobacter pathogenesis. Current Opinion in Infectious Diseases 2003, 16:487-491.
9. Boonmar S., Yingsakmongkon S., Songserm T., Hanhaboon P., Passadurak W. Detection of Campylobacter in duck using standard culture method and multiplex polymerase chain reaction. The Southeast Asian Journal of Tropical Medicine and Public Health 2007, 38:728-731.
10. Chai L.C., Ghazali F.M., Bakar F.A., Lee H.Y., Suhaimi L.R.A., Talib S.A., Nakaguchi Y., Nishibuchi M., Radu S. Occurrence of thermophilic Campylobacter spp. contamination on vegetable farms in Malaysia. Journal of Microbiology and Biotechnology 2009, 19:1415-1420.
11. Clark M. Treatment for Campylobacter infection Available at, [accessed 23 August 2010]. http://www.about-campylobacter.com/campylobacter_treatment.
12. Clinical and Laboratory Standards Institute (CLSI) Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria; Approved Guideline (M45-A) 2006, Clinical and Laboratory Standards Institute, Wayne, PA.
13. Communicable Disease Surveillance Centre (CDSC) Sentinel surveillance of Campylobacter in England and Wales. Communicable Disease Report Weekly 2003, 13:7-9.
14. Ekkapobyotin C., Padungtod P., Chuanchuen R. Antimicrobial resistance of Campylobacter coli isolates from swine. International Journal of Food Microbiology 2008, 128:325-328.
15. Ertas H.B., Çetinkaya B., Muz A., Öngor H. Genotyping of broiler-originated Campylobacter jejuni and Campylobacter coli isolates using fla typing and random amplified polymorphic DNA method. International Journal of Food Microbiology 2004, 94:203-209.
16. European Food Safety Authority (EFSA) Scientific report of the Scientific Panel on Biological Hazards on the request from the Commission related to Campylobacter in animals and foodstuffs. Annex to the EFSA Journal 2005, 173:1-105.
17. Fisher R.A., Yates F. Statistical Tables for Biological Agricultural and Medical Research 1963, 47. Oliver and Boyd, Edinburgh, Table IV, Available at:, [accessed 7 July 2010]. http://digital.library.adelaide.edu.au/dspace/bitstream/2440/10701/1/stat_tab.pdf, 6th ed.
18. Food and Agriculture Organisation (FAO) FAOSTAT on main producer country of duck meat in 2007 Available at:, [accessed 9 July 2011]. http://faostat.fao.org/site/569/DesktopDefault.aspx?PageID=569#ancor.
19. Gupta A., Nelson J.M., Barrett T.J., Tauxe R.V., Rossiter S.P., Friedman C.R., Joyce K.W., Smith K.E., Jones T.F., Hawkin M.A., Shiferaw B., Beebe J.L., Vugia D.J., Rabatsky-Ehr T., Benson J.A., Root T.P., Angulo F.J. Antimicrobial resistance among Campylobacter strains in the United States, 1997-2001. Emerging Infectious Diseases 2004, 10:1102-1109.
20. Han K., Jang S.S., Choo E., Heu S., Ryu S. Prevalence, genetic diversity, and antibiotic resistance patterns of Campylobacter jejuni from retail raw chickens in Korea. International Journal of Food Microbiology 2007, 114:50-59.
21. Hatch J.J. Threats to public health from gulls (Laridae). International Journal of Environmental Health Research 1996, 6:5-16.
22. Humphrey T., O'Brien S., Madsen M. Campylobacters as zoonotic pathogens: a food production perspective. International Journal of Food Microbiology 2007, 117:237-257.
23. Hunt J.M., Abeyta C., Tran T. Bacteriological Analytical Manual 1998, AOAC International, Gaithersburg. 8th Edn.
24. Inglis G.D., Cohen A.C. Influence of antimicrobial agents on the spoilage of a meat-based entomophage diet. Journal of Economic Entomology 2004, 97:235-250.
25. Jasson V., Sampers I., Botteldoorn N., Lopez-Galvez F., Baert L., Denayer S., Rajkovic A., Habib I., De Zutter L., Debevere J., Uyttendaele M. Characterization of Escherichia coli from raw poultry in Belgium and impact on the detection of Campylobacter jejuni using Bolton broth. International Journal of Food Microbiology 2009, 135:248-253.
26. Jimenez A., Velazquez J.B., Rodriguez J., Tinajas A., Villa T.G. Prevalence of fluoroquinolone resistance in clinical strains of Campylobacter jejuni isolated in Spain. Journal of Antimicrobial Chemotherapy 1994, 33:188-190.
27. Jørgensen F., Bailey R., Williams P.S., Henderson P., Wareing D.R., Bolton F.J., Frost J.A., Ward L., Humphrey T.J. Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. International Journal of Food Microbiology 2002, 76:151-164.
28. Kramer J.M., Frost J.A., Bolton F.J., Wareing D.R. Campylobacter contamination of raw meat and poultry at retail sale: identification of multiple types and comparison with isolates from human infection. Journal of Food Protection 2000, 63:1654-1659.
29. Krumperman P.H. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of food. Applied and Environmental Microbiology 1983, 46:165-170.
30. Leotta G.A., Vigo G.B., Giacoboni G. Isolation of Campylobacter lari from seabirds in Hope Bay, Antarctica. Polish Polar Research 2006, 27:303-308.
31. Little C.L., Richardson J.F., Owen R.J., de Pinna E., Threlfall E.J. Prevalence, characterisation and antimicrobial resistance of Campylobacter and Salmonella in raw poultry meat in the UK, 2003-2005. International Journal of Environmental Health Research 2008, 18:403-414.
32. Madden R.H., Moran L., Scates P. Frequency of occurrence of Campylobacter spp. in red meats and poultry in Northern Ireland and their subsequent subtyping using polymerase chain reaction-restriction fragment length polymorphism and the random amplified polymorphic DNA method. Journal of Applied Microbiology 1998, 84:703-708.
33. McCrea B.A., Tonooka K.H., Van Worth C., Boggs C.L., Atwill E.R., Schrader J.S. Prevalence of Campylobacter and Salmonella species on farm, after transport, and at processing in specialty market poultry. Poultry Science 2006, 85:136-143.
34. Mead P.S., Slutsker L., Dietz V., McCaig L.F., Bresee J.S., Shapiro C., Griffin P.M., Tauxe R.V. Food-related illness and death in the United States. Emerging Infectious Diseases 1999, 5:607-625.
35. Miller R.S., Miller W.G., Behringer M., Hariharan H., Matthew V., Oyarzabal O.A. DNA identification and characterization of Campylobacter jejuni and Campylobacter coli isolated from caecal samples of chickens in Grenada. Journal of Applied Microbiology 2010, 108:1041-1049.
36. Moore J.E., Corcoran D., Dooley J.S.G., Fanning S., Lucey B., Matsuda M., McDowell D.A., Mégraud F., Millar B.C., O'Mahony R., O'Riordan L., O'Rourke M., Rao J.R., Rooney P.J., Sails A., Whyte P. Review article, Campylobacter. Veterinary Research 2005, 36:351-382.
37. Nielsen E.M., Engberg J., Fussing V., Petersen L., Brogren C.H., On S.L.W. Evaluation of phenotypic and genotypic methods for subtyping Campylobacter jejuni isolates from humans, poultry, and cattle. Journal of Clinical Microbiology 2000, 38:3800-3810.
38. Nonga H.E., Muhairwa A.P. Prevalence and antibiotic susceptibility of thermophilic Campylobacter isolates from free range domestic duck (Cairina moschata) in Morogoro Municipality, Tanzania. Tropical Animal Health and Production 2010, 42:165-172.
39. Qin S.S., Wu C.M., Wang Y., Jeon B., Shen Z.Q., Wanga Y., Zhang Q., Shen J.Z. Antimicrobial resistance in Campylobacter coli isolated from pigs in two provinces of China. International Journal of Food Microbiology 2011, 146:94-98.
40. Rahimi E., Ameri M. Antimicrobial resistance patterns of Campylobacter spp. isolated from raw chicken, turkey, quail, partridge, and ostrich meat in Iran. Food Control 2011, 22:1165-1170.
41. Ridsdale J.A., Atabay H.I., Corry J.E.L. Prevalence of Campylobacters and Arcobacters in ducks at the abattoir. Journal of Applied Microbiology 1998, 85:567-573.
42. Saleha A.A. Isolation and characterization of Campylobacter jejuni from broiler chickens in Malaysia. International Journal of Poultry Science 2002, 1:94-97.
43. Sallam K.I. Prevalence of Campylobacter in chicken and chicken by-products retailed in Sapporo areas, Hokkaido, Japan. Food Control 2006, 18:1113-1120.
44. Suresh T., Hatha A.A.M., Harsha H.T., Lakshmanaperumalsamy P. Prevalence and distribution of Salmonellaserotypes in marketed broiler chickens and processing environment in Coimbatore city of southern India. Food Research International 2011, 44:823-825.
45. Suzuki H., Yamamoto S. Campylobacter contamination in retail poultry meats and by-products in Japan: a literature survey. Food Control 2009, 20:531-537.
46. Tresierra-Ayala A., Bendayan M.E., Bernuy A., Pereyra G., Fernandez H. Chicken as potential contamination source of Campylobacter lari in Iquitos, Peru. Reviews of Institute Medicine Trop Sao Paulo 1994, 36:497-499.
47. Waldenstrom J., Broman T., Carlsson I., Hasselquist D., Achterberg R.P., Wagenaar J.A., Olsen B. Prevalence of Campylobacter jejuni, Campylobacter lari, and Campylobacter coli in Different Ecological Guilds and Taxa of Migrating Birds. Applied and Environmental Microbiology 2002, 68:5911-5917.
48. Wang G., Clark C.G., Taylor T.M., Pucknell C., Barton C., Price L., Woodward D.L., Rodgers F.G. Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. Journal of Clinical Microbiology 2002, 40:4744-4747.
49. Wassenaar T.M., Newell D.G. Genotyping of Campylobacter spp. - a minireview. Applied and Environmental Microbiology 2000, 66:1-9.
50. Zhao S., Young S.R., Tong E., Abbott J.W., Womack N., Friedman S.L., McDermott P.F. Antimicrobial resistance of Campylobacter isolates from retail meat in the United States between 2002 and 2007. Applied and Environmental Microbiology 2010, 76:7949-7956.