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Campylobacter Spp. in Conventional and Organic Poultry Operations

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Campylobacter Spp. in Conventional and Organic Poultry Operations CAMPYLOBACTER SPP. IN CONVENTIONAL AND ORGANIC POULTRY OPERATIONS DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctoral of Philosophy in the Graduate School of The Ohio State University By Taradon Luangtongkum, D.V.M. ***** The Ohio State University 2005 Dissertation Committee: Dr. Teresa Y. Morishita, Advisor Approved by Dr. Yehia M. Saif Dr. Charles A. Neer ________________________________ Dr. Qijing Zhang Advisor Graduate Program in Veterinary Preventive Medicine ABSTRACT Campylobacter spp. particularly C. jejuni has been recognized as one of the most important causes of foodborne bacterial diarrhea in humans worldwide. Since poultry are considered the major reservoir of this foodborne pathogen, the prevalence along with the antimicrobial resistance of Campylobacter spp. in conventional and organic poultry operations is a matter of concern. However, relatively little information on the impact of different food animal production practices on the prevalence of antibiotic-resistant Campylobacter is available. Hence, a farm-based study was conducted to determine the prevalence and the antimicrobial resistance rates of Campylobacter isolates from both conventionally-raised and organically-raised poultry. Although Campylobacter was highly prevalent in both organic and conventional production systems, the antibiotic resistance rates were significantly higher in conventional operations than in organic operations. These findings clearly indicate the influence of different production practices on the antibiotic resistance rates of Campylobacter spp. on poultry farms, which is likely due to the result of antimicrobial usage in conventional poultry production. However, antimicrobial usage alone may not solely be responsible for the increased antibiotic resistance in Campylobacter isolates because even in the absence of antibiotic exposure, a high level of tetracycline resistance was also observed in Campylobacter isolates from organic poultry farms. Since antibiotics including tetracycline have never been used on these organic poultry farms, a high ii prevalence of tetracycline resistance observed among Campylobacter isolates from this operation type is interesting. Hence, another part of this study was conducted to investigate the epidemiology of tetracycline resistance of thermophilic Campylobacter on organic poultry farms. The results showed the changes of tetracycline resistance rates in Campylobacter isolates during the production cycle of one organic broiler flock with 0%, 100%, and 33.33% of tetracycline resistance rates detected at week 3, 6, and 10 of the production period, respectively. Although no tetracycline-resistant Campylobacter strains were isolated from unexposed environmental samples collected from these organic poultry farms except for one organic broiler farm, some of these samples were positive for tetracycline resistance gene [tet(O) gene]. In addition, the agreement between the disk diffusion method and the agar dilution method in identification of antimicrobial resistance of thermophilic Campylobacter was also investigated. The results indicated that the disk diffusion method can be used as a reliable alternative method for susceptibility testing of Campylobacter species to fluoroquinolone and aminoglycoside antibiotics; however, until the standard resistance breakpoints specific for Campylobacter is established and validated, the agar dilution method should be used to determine antimicrobial resistance of Campylobacter to other classes of antibiotics. Together, this study reveals the complex nature in the spread of antibiotic resistance and further highlights the need for prudent measures to prevent the occurrence and transmission of antibiotic-resistant Campylobacter in the poultry reservoir. iii Dedicated to my parents, Songkram and Theraphan Luangtongkum Without their love and support this dissertation would not have been possible iv ACKNOWLEDGEMENTS I wish to thank my advisor, Dr. Teresa Y. Morishita, for providing me the opportunity and freedom to conduct this research, and for her intellectual guidance, support, and encouragement, which made this dissertation possible. The experiences that I have gained from working with her for over the last 5 years here at The Ohio State University have been invaluable to my future career. I am also grateful to my dissertation committee members, Dr. Yehia Mo. Saif, Dr. Charles A. Neer, and Dr. Qijing Zhang for their kindness and willingness to serve on the committee, as well as for their contribution on this dissertation. In this regard, I particularly would like to thank Dr. Qijing Zhang for his invaluable advice, for sharing with me his knowledge and discussions, and for being so patient in answering all the questions that I have had over the last several years, especially while I was writing the manuscripts for publication. I also wish to thank Dr. Amna B. El-Tayeb, Dr. Meredith F. Davis, Dr. Benjamas Promsopone, Ms. Elisabeth J. Angrick, Mr. Aaron J. Ison, and all of the many fellow graduate, undergraduate, and veterinary students at the Avian Disease Investigation Laboratory, both past and present, whom I have had a chance to know and work with, for creating a pleasant environment in which to work, and for offering me their support, especially friendship inside and outside of the laboratory for over the last several years v that I have been here in the States. The friendship and encouragement that I have received from Dr. William L. Ingalls since the first day that I have been in the Department also deserve a space here. Many thanks also go to the organic and conventional poultry farms and processing plants for participating in this study. Research funding from the United States Department of Agriculture (USDA) and the North Central Region program for Sustainable Agriculture Research and Education (NCR-SARE) are also gratefully acknowledged. I am indebted to The Anandamahidol Foundation for their financial support throughout my entire study. Without this support, I would not have been able to pursue my doctoral degree in the United States. I am also very thankful to Ms. Nuttha Thongchul for everything she has done for me and for being so supportive and understanding. The help of Ms. Supaporn Suwannakham on this dissertation is truly appreciated as well. Finally, my heartfelt gratitude goes to those who are the most important persons in my life, my parents, Songkram and Theraphan Luangtongkum, for their unconditional love and life-long support, for always encouraging me, believing in me, being my inspiration, and helping me get through the tough, difficult, and stressful times during my studies. Without them, this doctoral degree would not have been possible. vi VITA April 19, 1976 ………………… Born – Bangkok, Thailand 1993 – 1999 …………………... Doctor of Veterinary Medicine (Honors) Chulalongkorn University, Bangkok, Thailand 1999 – present ………………… Instructor, Department of Veterinary Public Health Chulalongkorn University, Bangkok, Thailand 2000 – present ………………… Graduate Student, Department of Veterinary Preventive Medicine The Ohio State University, Columbus, OH PUBLICATION 1. Huang, S., T. Luangtongkum, T. Y. Morishita, and Q. Zhang. 2005. Molecular typing of Campylobacter strains using the cmp gene encoding the major outer membrane protein. Foodborne Pathog. Dis. 2: 12-23. FIELDS OF STUDY Major Field: Veterinary Preventive Medicine Studies in Food Safety and Public Health vii TABLE OF CONTENTS Page Abstract…………………………………………………………….………................…. …ii Dedication…………………………………………………………….…………..........…iv Acknowledgments………………………………………………………………..……..….v Vita…………………………………………………………………………………........vii List of Tables…………………………………………………………….................... .….x List of Figures………………………………………………………………………...…. .xii Chapters: 1. Literature review ……………….……………………………………………...…....…..1 1.1 Introduction…………………………………………...………………………..…..1 1.2 Campylobacter: The Organism…………………………………………………......7 1.2.1 Historical background……………………….…………………………... …..7 1.2.2 General characteristics ….………………………………………………. …..9 1.2.3 Isolation and identification………………...…………………………….…..13 1.3 Campylobacter spp. in Humans…………………………………………..………. ..31 1.3.1 Sources and modes of transmission………….……………………………….31 1.3.2 Infection and clinical manifestation……………………………….....…..…..36 1.3.3 Treatment and control and prevention……….…………………………..…..45 1.4 Campylobacter spp. in Poultry…………………………..……………………..…..56 1.4.1 Prevalence in poultry and other animals……………………………………. ..56 1.4.2 Sources of poultry flock colonization….……………………………………..70 1.4.3 Control and prevention at the farm level……………………………..……..81 1.5 Antimicrobial Resistance of Campylobacter species…………………………..…..86 1.5.1 Antimicrobial susceptibility testing methods……………...………………..86 1.5.2 Occurrence and trends of antimicrobial resistance………...…………….…. ..89 1.5.3 Mechanisms of antimicrobial resistance………………………..………..…..95 1.6 References……………………………………………………………………...…101 2. The effect of different poultry production practices on antibiotic resistance rates of Campylobacter in poultry…………………………………………………….....…150 2.1 Abstract…………………………………………………………………………..150 2.2 Introduction…………………………………………………………………….…151 2.3 Materials and methods……………………………………………………………155 viii 2.4 Results…………………………………………………....…………………….…159 2.5 Discussion…………………………………………………………....………...…164 2.6 Acknowledgement…………………………………………………………………172 2.7 References………………………………………………………..…………….…172 3. Antimicrobial susceptibility testing of Campylobacter by the
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