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Salmonella in Broiler Carcass Bone Marrow and Neck Skin: Potential

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Salmonella in Broiler Carcass Bone Marrow and Neck Skin: Potential SALMONELLA IN BROILER CARCASS BONE MARROW AND NECK SKIN: POTENTIAL SOURCES FOR GROUND CHICKEN CONTAMINATION by DIEZHANG WU (Under the Direction of Walid Q. Alali) ABSTRACT Possible routes for Salmonella contamination of ground chicken are through grinding chicken parts containing contaminated neck skin and bone marrow internalized with Salmonella. The objective of this study was to determine Salmonella prevalence and serotype distribution of broiler bone marrow and neck skin samples. A total of 300 drumstick bone marrow samples, 299 neck skin samples, and bootsock samples from 26 broiler houses were tested according to the USDA-FSIS standard protocols. Salmonella prevalence of bone marrow, neck skin, and broiler houses were 0.8%, 21.4% and 80.1%, respectively. Salmonella prevalence of rinsed skin samples (2.3%) and stomached skin samples (20.7%) were significantly different (p<0.05). Six Salmonella serotypes including S. Kentucky, Typhimurium, Enteritidis, Agona, Ouakam, and Liverpool were identified. Overall, Salmonella Kentucky was the most frequently isolated serotype. To conclude, contaminated neck skin can contribute to ground chicken contamination; whereas the contribution of internalized drumstick bones is expected to be much lower. INDEX WORDS: Salmonella, broiler carcass, bone marrow, neck skin, ground chicken contamination v SALMONELLA IN BROILER CARCASS BONE MARROW AND NECK SKIN: POTENTIAL SOURCES FOR GROUND CHICKEN CONTAMINATION by DIEZHANG WU B.S., Purdue University, West Lafayette, 2011 A Thesis Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree MASTER OF SCIENCE ATHENS, GEORGIA 2013 i © 2013 Diezhang Wu All Rights Reserve ii SALMONELLA IN BROILER CARCASS BONE MARROW AND NECK SKIN: POTENTIAL SOURCES FOR GROUND CHICKEN CONTAMINATION by DIEZHANG WU Major Professor: Walid Q. Alali Committee: Mark A. Harrison Charles L. Hofacre Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia December 2013 iii ACKNOWLEDGEMENTS I would like to express my greatest gratitude to my major professor, Dr. Walid Q. Alali, for his direction, comments, remarks and engagement through out my graduate study at the University of Georgia. I would also like to thank Dr. Mark A. Harrison and Dr. Charles L. Hofacre for being on my committee, and offering suggestions and great support for finishing my study. Thanks to Daniel Lefever, Da’Shundria Davis, Cagatay Celik, who accompanied my visits to the farm and plant, and helped me finish the project. Special thanks to Hao Zhang, for being supportive and patient. In the end, I would like to give the utmost appreciation to my parents, Yuefeng Wu and Xiaoqing Wu for their unconditional love and support. Thank you for teaching me to work hard and never stop learning. I love you! iv TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .........................................................................iv LIST OF TABLES ..................................................................................vii CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW .................................... 1 Salmonellosis and Poultry Products ……………...........................1 Salmonella Prevalence at Farm Level ....................................3 Salmonella Prevalence at Processing Plants ...........................6 Controlling Strategies at Farms ...........................................10 Controlling Strategies at Processing Plants ...........................17 Conclusions .................................................................... 23 References ......................................................................25 2 SALMONELLA IN BROILER CARCASS BONE MARROW AND NECK SKIN: POTENTIAL SOURCES FOR GROUND CHICKEN CONTAMINATION ........ 43 Abstract ..........................................................................44 Introduction ....................................................................45 v Materials and Methods .................................................... 47 Results ......................................................................... 52 Discussion ..................................................................... 53 References ..................................................................... 58 3 CONCLUSIONS ........................................................................ 62 vi LIST OF TABLES Page Table 1 Salmonella prevalence in broiler skin and bone samples ..................................... 63 Table 2 Salmonella serogroup isolated from broiler farm, skin and bone samples ...64 Table 3 Salmonella serotype isolated from broiler farm, skin and bone samples ..…65 vii CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW Salmonellosis and Poultry Products Salmonella is a genus of gram-negative, rod shaped bacteria discovered by American scientist Daniel Salmon. The genus is divided into two species, Salmonella enterica and Salmonella bongoria (CDC, 2011). The Salmonella genus is found to contain over 3,000 serotypes. Pathogenic Salmonella serotypes mostly belong to Salmonella enterica subsp. enterica. Salmonellosis is the infection caused by Salmonella, in which patients usually develop diarrhea, fever, and abdominal cramps 12 to 72 hours post infection (CDC, 2010). In severe cases, Salmonella cells may spread into the blood stream, invade other organs, and lead to chronic arthritis or even death. Young children, elderly, and people with a compromised immune system are more susceptible to severe Salmonella infection (CDC, 2010). Salmonella is estimated to cause about 1.03 million foodborne illnesses including about 19,500 hospitalizations and 378 deaths in the U.S. every year (Scallan et al., 2011). According to the 2011 Foodborne Disease Active Surveillance Network (FoodNet) surveillance report, a total of 7,813 lab-confirmed Salmonella cases were reported, among which S. Enteritidis (1,424 [18.2%]) was the most common serotype identified, followed by S. Typhimurium (981 [12.6%]), S. Newport (959 [12.3%]), S. Javiana (753 [9.6%]), and S. I 4,[5], 12:i:- (314 [4.0%]) (CDC, 2012). 1 Poultry products are the primary sources of human Salmonella infections. In 2011, USDA-FSIS reported that the Salmonella prevalence in post-chill broiler carcasses and ground chicken were 6.5%, and 30.9%, respectively (USDA-FSIS, 2012a). The most common serotype isolated from broiler carcasses and ground chicken was S. Kentucky, and the prevalence of this serotype had an ascending trend from 36.8% in 2008 to 45.4% in 2010 on broilers carcasses, and from 28.6% in 2008 to 35.0% in 2010 in ground chicken (USDA-FSIS, 2011a). Although S. Kentucky is frequently isolated from chicken carcass and ground chicken, it was reported that this serotype was over 100 times less likely to cause human illness compared to S. Typhimurium, Enteritidis, and Newport (Sarwari et al., 2001). The annual number of foodborne illness caused by major pathogens is estimated to be 9.4 million in the U.S. (Scallan et al., 2011). According to the food attribution model using foodborne outbreak data from 1988 to 2008, poultry meat was associated with 900,000 (10%) foodborne illnesses, following leafy vegetables (2.2 million [22%]), dairy (1.3 million [14%]), and fruits-nuts (1.1 million [12%]) (Painter et al., 2013). With regard to Salmonella and poultry meat, Painter et al. (2013) reported that 10-29% (approximately 103,000 to 298,000 illnesses) of all salmonellosis was associated with poultry meat. Furthermore, of the 278 deaths attributed to poultry between 1998-2008, Salmonella caused about 73 cases (26%) (Painter et al., 2013). 2 Salmonella Prevalence at Farm Level The broiler industry in the U.S. is described as vertically integrated production system. The poultry company known as the “integrator”, provides chicks, feed, veterinary and field personnel service, makes decisions about frequency of flock rotation, and usually gives house and equipment specifications (MacDonald, 2008; Vukina, 2001). The farmers who contract with a poultry company are responsible for land and housing facilities, utilities including water and electricity, operating expenses, and for growing the chicks to a required weight (MacDonald, 2008; Vukina, 2001). Since the U.S. broiler industry is entirely vertically integrated from breeding and hatcheries to feed mills, and then to transportation and processing (Vukina, 2001), both vertical and horizontal Salmonella transmission are the routes responsible for the contamination of the final products. Vertical transmission of Salmonella occurs when pathogens disseminate from breeder flocks to broilers. Several studies found that: 1) Salmonella was able to colonize the laying hen reproductive system (Gast et al., 2004; Keller et al., 1995; Okamura et al., 2001), and 2) contaminated eggs could be produced by challenging laying hens with Salmonella orally, intravenously, intracloacally and intravaginally (Gast et al., 2004; Gast et al., 2002, 2003; Gast et al., 2013; Miyamoto et al., 1997; Shivaprasad et al., 1990). Reiber et al. (1995) examined rooster semen and found that the most frequently isolated bacterial genera included Escherichia, Staphylococcus, Micrococcus, Enterococcus, and Salmonella, which indicates that the aforementioned bacteria are endemic to poultry and may contaminate fertilized eggs. In the study conducted by Liljebjelke and colleagues, the 3 authors revealed that the S. Typhimurium and S. Enteritidis strains isolated from one company’s breeder farms and the broiler houses had
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