Transmission of Escherichia coli O157:H7 to cattle by house flies

doi:10.1016/j.prevetmed.2007.01.006

Preventive Veterinary Medicine

Volume 80, Issue 1, 15 June 2007, Pages 74-81

https://doi.org/10.1016/j.prevetmed.2007.01.006 Get rights and content

Abstract

The main reservoir of Escherichia coli O157:H7 is the digestive tract of cattle; however, the ecology of this food-borne pathogen is poorly understood. House flies (Musca domestica L.) might play a role in dissemination of this pathogen in the cattle environment. In our study, eight calves were individually exposed to house flies that were orally inoculated with a mixture of four strains of nalidixic acid-resistant E. coli O157:H7 (Nal^REcO157) for 48 h. Another eight calves were individually exposed to uninoculated flies and served as the control. Fresh cattle feces (rectal sampling) and drinking water were periodically sampled and screened for Nal^REcO157 up to 19 days after the exposure. At the end of the experiment, all calves were euthanized and the lumen contents of rumen, cecum, colon, and rectum as well as swab samples of gall-bladder mucosa and the recto-anal mucosa were screened for Nal^REcO157. On day 1 after the exposure, fecal samples of all eight calves and drinking-water samples of five of eight calves exposed to inoculated flies tested positive for Nal^REcO157. The concentration of Nal^REcO157 in feces ranged over time from detectable only by enrichment (<10²) to up to 1.1 × 10⁶ CFU/g. Feces of all calves remained positive for Nal^REcO157 up to 11 days after the exposure and 62% were positive until the end of experiment. Contamination of drinking water was more variable and all samples were negative on day 19. At necropsy, the highest prevalence of Nal^REcO157 was in the recto-anal mucosa region, followed by rectal and colonic contents.

Introduction

Enterohemorrhagic Escherichia coli O157:H7 is an important causative agent of hemorrhagic colitis and hemorrhagic uremic syndrome in humans (Rangel et al., 2005). Although the number of human infections in the United States has declined over the past several years (402 human infections in the United States in 2004) (FoodNet Surveillance Annual Reports, 1997–2004); the outbreaks in 2006 (CDC, Health and Safety Topics, 2006) have underscored the importance of this human food-borne pathogen. The main reservoir for E. coli O157:H7 is the intestinal tract of healthy cattle; individual cattle are transiently colonized and shed E. coli O157:H7 in their feces (Bach et al., 2002). The sources of E. coli O157:H7 that colonize cattle are not well understood and little is known about the ecology of E. coli O157:H7 in the environment (Bach et al., 2002, Sargeant et al., 2003). Additionally, high variability of prevalence of E. coli O157:H7 among cattle suggests the possibility of a reservoir of E. coli O157:H7 external to the cattle. E. coli O157:H7 has been detected in non-bovine animals including sheep, horses, dogs, and wild birds (Bach et al., 2002); however, the mode of dissemination of this pathogen in the environment is not well understood.

One of the potential means of spread of this pathogen in the environment is by insects that develop in animal feces/manure (primarily house flies, Musca domestica L.). House flies (HF) commonly build up very large populations on cattle farms and other animal facilities. Previously, a laboratory-based study demonstrated that E. coli O157 ingested by HF remain viable in the fly excreta and the flies were able to carry and disseminate E. coli for several days (Kobayashi et al., 1999). In Japan, HF were implicated in transmission of E. coli O157:H7 from reservoir animals to other animals and humans (Moriya et al., 1999). Alam and Zurek (2004) reported the E. coli O157:H7 prevalence of 2.9 and 1.4% in HF collected in a cattle feedlot from feed bunks and cattle-feed storage, respectively. E. coli O157:H7 counts ranged from 3.0 × 10 to 1.5 × 10⁵ CFU/fly. PCR analysis revealed that 90.4, 99.2, and 99.2% of the E. coli O157:H7 isolates (n = 125) possessed the virulence genes stx1, stx2, and eaeA, respectively (Alam and Zurek, 2004). They suggested that HF in cattle farms play a role in the dissemination of E. coli O157:H7 among animals and to the surrounding environment.

Our objectives were: (a) to assess whether HF can transmit E. coli O157:H7 to cattle; (b) to evaluate duration and concentration of E. coli O157:H7 in cattle feces and drinking water after the fly exposure; (c) to assess the spatial prevalence and concentration of E. coli O157:H7 in cattle's digestive tract at the end of the experiment.

Section snippets

Bacteria

We used four strains of E. coli O157:H7 resistant to nalidixic acid (50 μg/ml; Nal^R). The strains were originally isolated from feces collected from feedlots and all were positive for the virulence genes stx1, stx2, and eaeA (Sargeant et al., 2003). Bacterial suspensions from the overnight culture of each Nal^REcO157 strain on blood agar (Remel Laboratories, Lenexa, KS, USA) were prepared and adjusted to 5.0 McFarland turbidity in sterile phosphate-buffered saline (PBS) (pH 7.2; MP Biomedicals,

Results and discussion

None of the fecal samples of the 16 calves or the drinking water sampled from each pen before the exposure to HF was positive for Nal^REcO157. All samples (feces, water, and necropsy) from the eight control calves exposed to uninoculated HF were negative for the pathogen throughout the experiment.

On day 1 after the exposure, fecal samples of all calves exposed to inoculated flies and 62% of their drinking-water samples tested positive for Nal^REcO157 (Table 1). Feces of all exposed calves were

Acknowledgments

We thank Jan Metlevski for technical assistance and Dr. A. Broce for reviewing the manuscript. This study was supported by a U.S. Department of Agriculture Grant (2005-34359-15684). This is contribution 06-349-J of the Kansas Agricultural Experiment Station.

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Preventive Veterinary Medicine

Abstract

Introduction

Section snippets

Bacteria

Results and discussion

Acknowledgments

References (15)

The role of non-biting flies in the epidemiology of human infectious diseases

Microb. Infect.

Escherichia coli O157 in feedlot cattle feces and water in four major feeder-cattle states in the USA

Prev. Vet. Med.

Association of Escherichia coli O157:H7 with house flies on a cattle farm

Appl. Environ. Microbiol.

Transmission and control of Escherichia coli O157:H7—a review

Can. J. Anim. Sci.

Dispersal of house flies and stable flies

Cited by (93)

Understanding the role of insects in the acquisition and transmission of antibiotic resistance

Prevalence of salmonella enterica in flies on a diversified cattle and fresh produce farm across two growing seasons

Risk factors and dynamics of verotoxigenic Escherichia coli O157:H7 on cattle farms: An observational study combining information from questionnaires, spatial data and molecular analyses

Combination of active behaviors and passive structures contributes to the cleanliness of housefly wing surfaces: A new insight for the design of cleaning materials

Environmental dissemination of mcr-1 positive Enterobacteriaceae by Chrysomya spp. (common blowfly): An increasing public health risk

kdr mutations and deltamethrin resistance in house flies in Abu Dhabi, UAE

Short communicationTransmission of Escherichia coli O157:H7 to cattle by house flies

Abstract

Introduction

Section snippets

Bacteria

Results and discussion

Acknowledgments

Microb. Infect.

Prev. Vet. Med.

Association of Escherichia coli O157:H7 with house flies on a cattle farm

Appl. Environ. Microbiol.

Transmission and control of Escherichia coli O157:H7—a review

Can. J. Anim. Sci.

Dispersal of house flies and stable flies

Short communication
Transmission of Escherichia coli O157:H7 to cattle by house flies