×

Assessing the potential impact of Salmonella vaccines in an endemically infected dairy herd. (English) Zbl 1402.92279

Summary: Salmonella spp. in cattle contribute to bacterial foodborne disease for humans. Reduction of Salmonella prevalence in herds is important to prevent human Salmonella infections. Typical control measures are culling of infectious animals, vaccination, and improved hygiene management. Vaccines have been developed for controlling Salmonella transmission in dairy herds; however, these vaccines are imperfect and a variety of vaccine effects on susceptibility, infectiousness, Salmonella shedding level, and duration of infectious period were reported. To assess the potential impact of imperfect Salmonella vaccines on prevalence over time and the eradication criterion, we developed a deterministic compartmental model with both replacement (cohort) and lifetime (continuous) vaccination strategies, and applied it to a Salmonella Cerro infection in a dairy farm. To understand the uncertainty of prevalence and identify key model parameters, global parameter uncertainty and sensitivity analyses were performed. The results show that imperfect Salmonella vaccines reduce the prevalence of Salmonella Cerro. Among three vaccine effects that were being considered, decreasing the length of the infectious period is most effective in reducing the endemic prevalence. Analyses of contour lines of prevalence or the critical reproduction ratio illustrate that, reducing prevalence to a certain level or zero can be achieved by choosing vaccines that have either a single vaccine effect at relatively high effectiveness, or two or more vaccine effects at relatively low effectiveness. Parameter sensitivity analysis suggests that effective control measures through applying Salmonella vaccines should be adjusted at different stages of infection. In addition, lifetime (continuous) vaccination is more effective than replacement (cohort) vaccination. The potential application of the developed vaccination model to other Salmonella serotypes related to foodborne diseases was also discussed. The presented study may be used as a tool for guiding the development of Salmonella vaccines.

MSC:

92C60 Medical epidemiology
92D30 Epidemiology
PDFBibTeX XMLCite
Full Text: DOI

References:

[1] Anderson, R.M.; May, R.M., Infectious diseases of humans: dynamics and control, (1991), Oxford University Press, Inc. New York
[2] Anderson, R.J., Epidemiological and biological characteristics of salmonellosis in three dairy herds, J. am. vet. med. assoc., 219, 310-322, (2001)
[3] Arino, J.; Connell Mccluskey, C.; van den Driessche, P., Global results for an epidemic model with vaccination that exhibits backward bifurcation, SIAM J. appl. math., 64, 260-276, (2003) · Zbl 1034.92025
[4] Baumler, A.J., Foodborne salmonella infections, ()
[5] Becker, N.G.; Starczak, D.N., The effect of random vaccine response on the vaccination coverage required to prevent epidemics, Math. biosci., 154, 117, (1998) · Zbl 0930.92016
[6] Chapagain, P.P.; van Kessel, J.S.; Karns, J.S.; Wolfgang, D.R.; Hovingh, E.; Nelen, K.A.; Schukken, Y.H.; Grohn, Y.T., A mathematical model of the dynamics of salmonella cerro infection in a US dairy herd, Epidemiol. infect., 136, 2, 263-272, (2007)
[7] Cody, S.H., Two outbreaks of multidrug-resistant salmonella serotype typhimurium DT104 infectious linked to raw-milk cheese in northern California, J. am. med. assoc., 281, 1805-1810, (1999)
[8] Dechet, A.M., Outbreak of multidrug-resistant salmonella enterica serotype typhimurium definitive type 104 infection linked to commercial ground beef, northeastern united states, 2003-2004, Clin. infect. dis., 42, 747-752, (2006)
[9] Denagamage, T.N.; O’Connor, A.M.; Sargeant, J.M.; Rajic, A.; Mckean, J.D., Efficacy of vaccination to reduce salmonella prevalence in live and slaughtered swine: a systematic review of literature from 1979 to 2007, Foodborne pathog. dis., 4, 539-549, (2007)
[10] Diekmann, O.; Heesterbeek, J.A., Mathematical epidemiology of infectious diseases, model building, analysis and interpretation, (2000), Wiley Chichester, West Sussex, England · Zbl 0997.92505
[11] Elbasha, E.H.; Gumel, A.B., Theoretical assessment of public health impact of imperfect prophylactic HIV-1 vaccines with therapeutic benefits, Bull. math. biol., 68, 577-614, (2006) · Zbl 1334.91060
[12] el-Gazzar, F.E.; Marth, E.H., Salmonellae, salmonellosis, and dairy foods: a review, J. dairy sci., 75, 2327-2343, (1992)
[13] Farrington, C.P., On vaccine efficacy and reproduction numbers, Math. biosci., 185, 89-109, (2003) · Zbl 1021.92034
[14] Gupta, A., Emergence of multi-resistant salmonella enterica serotype newport infections resistant to expanded-spectrum cephalosporins in the united states, J. infect. dis., 188, 1707-1716, (2003)
[15] Halloran, M.E.; Struchiner, C.; Longini, I.M., Study designs for evaluating different efficacy and effectiveness aspects of vaccines, Am. J. epidemiol., 146, 789, (1997)
[16] Halloran, M.E.; Longini, I.M.; Struchiner, C., Design and interpretation of vaccine field studies, Epidemiol. rev., 21, 73-88, (1999)
[17] Heider, L.C.; Meiring, R.W.; Hoet, A.M.; Gebreyes, W.A.; Funk, J.A.; Wittum, T.E., J. am. vet. med. assoc., 233, 466-469, (2008)
[18] Helton, J.C.; Davis, J.D., Illustration of sampling-based methods for uncertainty and sensitivity analysis, Ris anal., 22, 3, 591-622, (2002)
[19] Helton, J.C.; Davis, J.D., Latin hypercube sampling and the propagation of uncertainty in analyses of complex systems, Reliab. eng. syst. saf., 81, 1, 23-69, (2003)
[20] Helton, J.C.; Johnson, J.D.; Sallaberry, C.J.; Storlie, C.B., Survey of sampling-based methods for uncertainty and sensitivity analysis, Reliab. eng. syst. saf., 91, 10-11, 1175-1209, (2006)
[21] Helton, J.C.; Johnson, J.D.; Encamped, W.L.; Storlie, C.B., A sampling-based computational strategy for the representation of epistemic uncertainty in model predictions with evidence theory, Comput. meth. appl. mech. eng., 196, 37-40, 3980-3998, (2007) · Zbl 1173.62301
[22] House, J.K.; Ontiveros, M.M.; Blackmer, N.M.; Dueger, E.L.; Fitchhorn, J.B.; McArthur, G.R.; Smith, B.P., Evaluation of an autogenous salmonella bacterin and a modified live salmonella serotype choleraesuis vaccine on a commercial dairy farm, Am. J. vet. res., 62, 1897-1902, (2001)
[23] House, J.K., Smith, B.P., 2004. Profitable strategies to control salmonellosis in dairy cattle. In: Proceedings of the WBC Congress, Quebec, Canada.; House, J.K., Smith, B.P., 2004. Profitable strategies to control salmonellosis in dairy cattle. In: Proceedings of the WBC Congress, Quebec, Canada.
[24] Humphrey, T., Science and society—salmonella, stress responses and food safety, Nature reviews microbiology, 2, 504-509, (2004)
[25] Keeling, M.J.; Rohani, P., Modeling infectious diseases in humans and animals, (2008), Princeton University Press NJ · Zbl 1279.92038
[26] Kribs-Zaleta, C.M.; Velasco-Hernandez, J.X., A simple vaccination model with multiple endemic states, Math. biosci., 164, 183-201, (2000) · Zbl 0954.92023
[27] Kunze, D.J.; Loneragan, G.H.; Platt, T.M.; Miller, M.T.; Besser, T.E.; Koohmaraie, M.; Stephens, T.; Brashears, M.M., salmonella enterica burden in harvest-ready cattle populations from the southern high plains of the united states, Appl. environ. microbiol., 74, 345-351, (2008)
[28] Lanzas, C.; Brien, S.; Ivanek, R.; Lo, Y.; Chapagain, P.P.; Ray, K.A.; Ayscue, P.; Warnick, L.D.; Grohn, Y.T., The effect of heterogeneous infectious period and contagiousness on the dynamics of salmonella transmission in dairy cattle, Epidemiol. infect., 136, 1496-1510, (2008)
[29] Leedom, J.M., 2006. Milk of nonhuman origin and infectious diseases in humans. Clin. Infect. Dis. 43, 610-615.; Leedom, J.M., 2006. Milk of nonhuman origin and infectious diseases in humans. Clin. Infect. Dis. 43, 610-615.
[30] Lloyd, A.L., Destabilization of epidemic models with the inclusion of realistic distributions of infectious periods, Proc. R. soc. London ser. B biol. sci., 268, 985-993, (2001)
[31] Lloyd, A.L., Realistic distributions of infectious periods in epidemic models: changing patterns of persistence and dynamics, Theor. popul. biol., 60, 59-71, (2001)
[32] Longini, I.M.; Sagatelian, K.; Rida, W.N.; Halloran, M.E., Optimal vaccine trial design when estimating vaccine efficacy for susceptibility and infectiousness from multiple populations, Statist. med., 17, 1121-1136, (1998)
[33] Marino, S.; Hogue, I.B.; Ray, C.J.; Kirschner, D.E., A methodology for performing global uncertainty and sensitivity analysis in systems biology, J. theor. biol., 254, 178-196, (2008) · Zbl 1400.92013
[34] Mead, P.S.; Slutsker, L.; Dietz, V.; MaCaig, L.F.; Bresee, J.S.; Shapiro, C.; Griffin, P.M.; Tauxe, R.V., Food-related illness and death in the united states, Emerg. infect. dis., 5, 607-625, (1999)
[35] Morrow, J.L.; Mitloehner, F.M.; Johnson, A.K.; Galyean, M.L.; Dailey, J.W.; Edrington, T.S.; Anderson, R.C.; Genovese, K.J.; Poole, T.L.; Duke, S.E.; Callaway, T.R., Effect of water sprinkling on incidence of zoonotic pathogens in feedlot cattle, J. anim. sci., 83, 1959-1966, (2005)
[36] Olsen, S.J., Multidrug-resistant salmonella typhimurium infection from milk contaminated after pasteurization, Emerg. infect. dis., 10, 932-935, (2004)
[37] Pandya, M., Wittum, T., Tadesse, D.A., Gebreves, W., Hoet, A., 2009. Environmental Salmonella Surveillance in The Ohio State University Veterinary Teaching Hospital. Vector Borne Zoonotic Dis. March (Epub ahead of print).; Pandya, M., Wittum, T., Tadesse, D.A., Gebreves, W., Hoet, A., 2009. Environmental Salmonella Surveillance in The Ohio State University Veterinary Teaching Hospital. Vector Borne Zoonotic Dis. March (Epub ahead of print).
[38] Saltelli, A., Chan, K., Scott, E.M., 2000. Sensitivity analysis. In: Wiley Series in Probability and Statistics. Wiley, Chichester, New York.; Saltelli, A., Chan, K., Scott, E.M., 2000. Sensitivity analysis. In: Wiley Series in Probability and Statistics. Wiley, Chichester, New York. · Zbl 0961.62091
[39] Saltelli, A., Making best use of model evaluations to compute sensitivity indices, Comput. phys. commun., 145, 2, 280-297, (2002) · Zbl 0998.65065
[40] Saltelli, A., Sensitivity analysis in practice: A guide to assessing scientific models, (2004), Wiley Hoboken, NJ · Zbl 1049.62112
[41] Sharomi, O.; Podder, C.N.; Gumel, A.B.; Elbasha, E.H.; Watmough, J., Role of incidence function in vaccine-induced backward bifurcation in some HIV models, Math. biosci., 210, 436-463, (2007) · Zbl 1134.92026
[42] Smith, B.P., Immunization of calves against salmonellosis, Am. J. vet. res., 41, 1947-1951, (1980)
[43] Smith, B.P., Aromatic-dependent salmonella Dublin as a parenteral modified live vaccine for calves, Am. J. vet. res., 45, 2231-2235, (1984)
[44] Steinbach, G.; Meyer, H., Efficacy of subcutaneous inoculation of calves with “murivac” inactivated salmonellosis vaccine, Tierarztliche praxis, 22, 529-531, (1994)
[45] Stocker, B.A., Auxotrophic salmonella typhi as live vaccine, Vaccine, 6, 141-145, (1988)
[46] Troutt, H.F.; Osburn, B.I., Meat from dairy cows: possible microbiological hazards and risks, Rev. sci. technol., 16, 405-414, (1997)
[47] van den Driessche, P.; Watmough, J., Reproduction numbers and subthreshold endemic equilibria for compartmental models of disease transmission, Math. biosci., 180, 29-48, (2002) · Zbl 1015.92036
[48] van Kessel, J.S.; Karns, J.S.; Wolfgang, D.R.; Hovingh, E.; Schukken, Y.H., Longitudinal study of a clonal, subclinical outbreak of salmonella enterica subsp. enterica serovar cerro in a US dairy herd, Foodborne pathog. dis., 4, 449-461, (2007)
[49] Weber, A.; Bernt, C.; Bauer, K.; Mayr, A., The control of bovine salmonellosis under field conditions using herd-specific vaccines, Tierarztl praxis, 21, 511-516, (1993)
[50] Wray, C.; Sojka, W.J.; Morris, J.A., The immunization of mice and calves with gal E mutants of salmonella typhimurium, J. hyg., 79, 17-24, (1977)
[51] Wray, C., A three-year study of salmonella Dublin infection in a closed dairy herd, Vet. rec., 124, 532-537, (1989)
[52] Xiao, Y.; Bowers, R.G.; Clancy, D.; French, N.P., Understanding the dynamics of salmonella infections in dairy herds: a modeling approach, J. theor. biol., 233, 159-175, (2005) · Zbl 1442.92185
[53] Xiao, Y.; Clancy, D.; French, N.P.; Bowers, R.G., A semi-stochastic model for salmonella infection in a multi-group herd, Math. biosci., 200, 214-233, (2006) · Zbl 1089.92053
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.