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Fate of Arcobacter Spp. Upon Exposure to Environmental FATE OF ARCOBACTER SPP. UPON EXPOSURE TO ENVIRONMENTAL STRESSES AND PREDICTIVE MODEL DEVELOPMENT by ELAINE M. D’SA (Under the direction of Dr. Mark A. Harrison) ABSTRACT Growth and survival characteristics of two species of the ‘emerging’ pathogenic genus Arcobacter were determined. The optimal pH growth range of most A. butzleri (4 strains) and A. cryaerophilus (2 strains) was 6.0-7.0 and 7.0-7.5 respectively. The optimal NaCl growth range was 0.09-0.5 % (A. butzleri) and 0.5-1.0% (A. cryaerophilus), while growth limits were 0.09-3.5% and 0.09-3.0% for A. butzleri and A. cryaerophilus, respectively. A. butzleri 3556, 3539 and A. cryaerophilus 1B were able to survive at NaCl concentrations of up to 5% for 48 h at 25°C, but the survival limit dropped to 3.5-4.0% NaCl after 96 h. Thermal tolerance studies on three strains of A. butzleri determined that the D-values at pH 7.3 had a range of 0.07-0.12 min (60°C), 0.38-0.76 min (55°C) and 5.12-5.81 min (50°C). At pH 5.5, thermotolerance decreased under the synergistic effects of heat and acidity. D-values decreased for strains 3556 and 3257 by 26-50% and 21- 66%, respectively, while the reduction for strain 3494 was lower: 0-28%. Actual D- values of the three strains at pH 5.5 had a range of 0.03-0.11 (60°C), 0.30-0.42 (55°C) and 1.97-4.42 (50°C). z-values for the three strains ranged from 5.20-6.11°C and 5.55- 6.28 °C at pHs of 7.3 and 5.5, respectively. D-values for a cocktail of the three strains in raw ground pork were 18.51 min at 50°C and 2.18 min at 55°C. The one strain tested (A. butzleri 3556) was highly sensitive to the combined effects of mild heat (50°C) followed by cold shock, exhibiting a 3.2-4.0 log10 decrease in cell numbers at a cold shock temperature of 4°C, as compared to a 0.33-1.12 log10 decrease at a temperature of 16°C. Predictive mathematical models (quadratic and cubic) were constructed from a dataset of growth curves obtained for a cocktail of three A. butzleri strains. These models described the main and interactive effects of incubation temperature (12-37°C), pH (6.0-7.5), sodium chloride (0.09-3.5%), sodium nitrite (0-180 ppm), and sodium tripolyphosphate (0-0.012%) levels on the growth characteristics of the cells. Predictions for generation time (GT), lag phase duration (LPD) and Gompertz parameters B and M were analyzed from natural logarithm transformed quadratic models. INDEX WORDS: Arcobacter, A. butzleri, A. cryaerophilus, D-values, z-values, pH, sodium chloride, sodium nitrite, sodium tripolyphosphate, predictive growth model FATE OF ARCOBACTER SPP. UPON EXPOSURE TO ENVIRONMENTAL STRESSES AND PREDICTIVE MODEL DEVELOPMENT by ELAINE M. D’SA B.S., The University of Bombay, India, 1984 M.S., The University of Bombay, India, 1986 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2002 © 2002 Elaine M. D’Sa All Rights Reserved FATE OF ARCOBACTER SPP. UPON EXPOSURE TO ENVIRONMENTAL STRESSES AND PREDICTIVE MODEL DEVELOPMENT by ELAINE M. D’SA Approved: Major Professor: Mark A. Harrison Committee: J. Stan Bailey Larry R. Beuchat Joseph F. Frank William L. Kerr Electronic Version Approved: Gordhan L. Patel Dean of the Graduate School The University of Georgia May 2002 iv DEDICATION This work is dedicated to my parents, to my brother, and to my spiritual family here in Athens, Georgia. v ACKNOWLEDGEMENTS First and foremost, I give thanks to my Lord Jesus Christ for many blessings and for His constant presence by my side in all situations. I am deeply grateful to my Major Professor, Dr. Mark A. Harrison, for his unfailing encouragement and support, for believing in me more than I believed in myself, and for being a great teacher, in the truest sense; this work would not have been possible without his patience. Thanks also to Dr. Judy Harrison for her warmth and hospitality. I also wish to thank Dr. Elizabeth Andress for her support and willingness to share of her knowledge and time. Thanks are also due to the members of my committee: Dr. J. Stan Bailey, Dr. Larry R. Beuchat, Dr. Joseph Frank, Dr. William L. Kerr, and Dr. Emmett Shotts; I have learned much from them. To Dr. Irene Wesley (USDA-ARS-NADC, Ames, IA) and Dr. Vijay Juneja (USDA-ERRC, PA) I am grateful for personalized technical assistance. Thanks to my parents, my brother Eustace, and to Tiny, for their love, support, many hours of prayers, for 'being there' for me all these years. Also to my spiritual family: Cindy Boatwright, Dr. Fred and Sherry White, Dr. Virginia and Mary Macagnoni, Punitha and Jonathan Samuel - thanks for praying and walking through many valleys with me. I thank RuthAnn and Michael Morrow for many years of treasured friendship, for sharing your lives, your home, (and your families!) with me. To Marion Rodrigues and Msgr. Richard Mathias I am grateful for wise counsel. vi Thanks are due to many friends for their friendship, help and cheerfulness, for sharing good and bad times with me – especially to Doris D’Souza, Firibu Saalia, Charisse Holmes, Michael Mouat, Meera Ramesh, Shivani and Rajesh Nair. I thank my present and past lab mates and friends in the department for many shared hours, especially Melissa Carlos, Warapa Mahakarnchanakul, Radha Reddy and Isabel Blackman. Finally, I would like to thank my 'extended-family' at the Catholic Center, UGA, and at the Fountain of Life Ministries, for their prayer-support, love and concern. Thank you all! vii TABLE OF CONTENTS Page ACKNOWLEDGEMENTS.................................................................................................v CHAPTER 1 INTRODUCTION .............................................................................................1 2 LITERATURE REVIEW ..................................................................................7 3 EFFECT OF pH, NaCl CONTENT AND TEMPERATURE ON GROWTH AND SURVIVAL OF ARCOBACTER SPP.....................................................69 4 PREDICTIVE MODELING OF EFFECTS OF pH, TEMPERATURE, SODIUM CHLORIDE, SODIUM NITRITE AND SODIUM TRIPOLYPHOSPHATE CONTENT ON GROWTH OF ARCOBACTER BUTZLERI .....................................................................................................112 5 SUMMARY AND CONCLUSIONS ............................................................172 APPENDICES A NATURAL LOGARITHM TRANSFORMED PLOTS OF RESPONSE SURFACES ...................................................................................................176 1 CHAPTER 1 INTRODUCTION The history of organisms belonging to the genus Arcobacter (from the Latin word for ‘arc-shaped’ bacterium) began long before they were officially designated as a separate genus in 1991 (Vandamme et al., 1991a). The close relatedness of Arcobacter species (four have been identified to date: A. butzleri, A. cryaerophilus hybridization groups 1A and 1B, A. skirrowii and A. nitrofigilis) to members of the genus Campylobacter, allows them to share a relatively common background of sources, illness manifestations in humans and animals, and history, dating from the early 1900’s, when the vibrio-like campylobacters were first studied. No discussion on arcobacters would therefore be complete without providing a short summary of the epidemiological role of campylobacters as pathogenic species. About 15 species and six subspecies of Campylobacter have been identified (Atabay and Corry, 1997). Thermophilic campylobacters notably C. jejuni and C. coli are thought to be the leading cause of foodborne human diarrheal illness in many developed countries including the U.S. (Atabay and Corry, 1998; CDC-MMWR, 2001). These campylobacters are present as a reservoir in the intestinal tract of food animals and have been identified in up to 100% of carcasses and raw poultry products, sometimes at levels of 106 – 107 CFU/g of poultry caecal contents. Cross-contamination of carcasses may occur during processing, although other studies have demonstrated the ease with which experimental infections with campylobacters can be spread through a poultry house flock. 2 Transmission of infection in cases of human campylobacteriosis is thought to occur from raw products (especially poultry) via unsafe food handling practices including unwashed hands, kitchen utensils and implements, insufficient cooking or direct hand to mouth transfer (Atabay and Corry, 1997). Arcobacter spp. have been known to mainly cause gastritis in humans, and abortions and gastritis in livestock (Wesley, 1994). Estimates of the occurrence of Arcobacter spp. in the environment and in raw or cooked food products, may be possible as the result of an educated guess or an extrapolation from Campylobacter-related data, since limited studies have been conducted globally to date, on the actual prevalence of these organisms. Furthermore, most classical laboratory tests are geared towards the detection of the thermophilic campylobacters (Bolton et al., 1992) and include the use of antibiotic-containing media, incubation at 42°C and microaerobic growth; thus, other campylobacters or arcobacters could go undetected. Additionally, biochemical tests that accurately identify and distinguish Arcobacter genus and species are extremely limited and somewhat unreliable. These tests include catalase activity (A. cryaerophilus exhibits a strong catalase reaction and A. butzleri a weak one), nitrate reduction, fatty acid analysis, sensitivity to cadmium chloride, growth in the presence of glycine or sodium chloride, and growth on MacConkey agar (Wesley, 1994). However, glycine tolerance, which has been noted in 25-78% of Arcobacter isolates is also a major identifying characteristic of Campylobacter fetus subsp. fetus strains that have been associated with animal abortions. A further confounding feature is the ability of C. fetus subsp. fetus strains (Wesley, 1994), and the recently discovered capability of C. jejuni strains (Engvall et al., 2002) to develop aerotolerance (a distinguishing characteristic of 3 Arcobacter spp.) on subculture. Cross-reactivity with C. jejuni and C. fetus antigens in complement fixation tests was also noted in patients suffering from A.
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