Assessing transmission of Salmonella to bovine peripheral lymph nodes upon horn fly feeding

Authors: Olafson, Pia; Brown, Tyson; Lohmeyer, Kimberly - Kim; Harvey, Roger; Nisbet, David; LONERAGAN, GUY - Texas Tech University; Edrington, Thomas

Submitted to: Journal of Food Protection
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/6/2016
Publication Date: 10/1/2018
Citation: Olafson, P.U., Brown, T.R., Lohmeyer, K.H., Harvey, R.B., Nisbet, D.J., Loneragan, G.H., Edrington, T.S. 2018. Assessing transmission of Salmonella to bovine peripheral lymph nodes upon horn fly feeding. Journal of Food Protection. 54:734-744. https://doi.org/10.7589/2017-09-239.
DOI: https://doi.org/10.7589/2017-09-239

Interpretive Summary: Blood-feeding ectoparasites are an economic burden to cattle production systems. Their role in mechanical dissemination of bacterial pathogens is also of significance. Biting arthropods are implicated in the transdermal transmission of Salmonella to bovine peripheral lymph nodes (PLNs), which may ultimately contribute to Salmonella contamination in beef processing. In a laboratory setting, the horn fly can acquire and subsequently excrete Salmonella in its feces; however, it is unclear if this relationship may result in transmission of the bacteria to bovine PLNs. The current study used an on-animal horn fly infestation approach to assess whether horn flies have a role in this transmission. Results of these experiments indicated that Salmonella persists for at least 5 d in the fly. Flies can successfully acquire Salmonella from the hide, as assessed by recovery from homogenates of surface-sterilized flies. Fly fecal excreta can serve as a bacterial contaminant on the hide and overall mean estimates of the quantity shed on the hide were 7.17 ± 1.47 x 10^5 CFU per caged area. No transmission of the bacteria to bovine PLNs was evident after a 5 d fly feeding period. To evaluate the effect of prolonged horn fly feeding in the presence of Salmonella shed in fly fecal excreta, the bacteria was offered to horn flies in a bloodmeal and animals were infested with these flies for 5 days, after which either the study was terminated (Group 3) or the flies were removed and the cages replenished with unfed flies either once or twice over the course of an 11 d (Group 2) or 19 d (Group 1) fly exposure period, respectively. An animal inoculated with the challenge strain using a microlancet apparatus was included in each group for comparison. The impact of prolonged horn fly feeding was evident, as 11% of lymph nodes cultured were positive from Group 3 compared with 53% and 50% from Groups 2 and 1, respectively. This is the first report documenting the role of biting flies in transmission of Salmonella to bovine PLNs.

Technical Abstract: Blood-feeding ectoparasites are an economic burden to cattle production systems. Their role in mechanical dissemination of bacterial pathogens is also of significance. Biting arthropods are implicated in the transdermal transmission of Salmonella to bovine peripheral lymph nodes (PLNs), which may ultimately contribute to Salmonella contamination in beef processing. In a laboratory setting, the horn fly can acquire and subsequently excrete Salmonella in its feces; however, it is unclear if this relationship may result in transmission of the bacteria to bovine PLNs. The current study used an on-animal horn fly infestation approach to assess whether horn flies have a role in this transmission. Salmonella Montevideo, Anatum, and Senftenberg were used throughout the study. The strains were used either to inoculate dung that was applied to an area of hide under an adhered fly cage (Salm-hair) or to spike a bloodmeal delivered to unfed flies (Salm-fed). Salm-hair animals were infested with unfed horn flies, while Salm-fed animals were infested with flies offered a spiked bloodmeal. Results of these experiments indicated that Salmonella persists for at least 5 d in the fly. Flies can successfully acquire Salmonella from the hide, as assessed by recovery from homogenates of surface-sterilized flies. Fly fecal excreta can serve as a bacterial contaminant on the hide and overall mean estimates of the quantity shed on the hide were 7.17 ± 1.47 x 10^5 CFU per caged area. No transmission of the bacteria to bovine PLNs was evident after a 5 d fly feeding period. To evaluate the effect of prolonged horn fly feeding in the presence of Salmonella shed in fly fecal excreta, Salmonella Senftenberg was offered to horn flies in a bloodmeal and animals were infested with these flies for 5 days, after which either the study was terminated (Group 3) or the flies were removed and the cages replenished with unfed flies either once or twice over the course of an 11 d (Group 2) or 19 d (Group 1) fly exposure period, respectively. An animal inoculated with the challenge strain using a microlancet apparatus was included in each group for comparison. The impact of prolonged horn fly feeding was evident, as 11% of lymph nodes cultured were positive from Group 3 compared with 53% and 50% from Groups 2 and 1, respectively. Higher concentrations of Salmonella were recovered from fly-infested animals versus the microlancet-inoculated control, and this may be a result of repeated inoculations over time by flies versus at a single timepoint. This is the first report documenting the role of biting flies in this transmission.