A model of animal–human brucellosis transmission in Mongolia

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Abstract

We developed a dynamic model of livestock-to-human brucellosis transmission in Mongolia. The compartmental model considers transmission within sheep and cattle populations and the transmission to humans as additive components. The model was fitted to demographic and seroprevalence data (Rose Bengal test) from livestock and annually reported new human brucellosis cases in Mongolia for 1991–1999 prior to the onset of a mass livestock-vaccination campaign (S19 Brucella abortus for cattle and Rev1 Brucella melitensis for sheep and goat). The vaccination effect was fitted to livestock- and human-brucellosis data from the first 3 years of the vaccination campaign (2000–2002). Parameters were optimized on the basis of the goodness-of-fit (assessed by the deviance). The simultaneously fitted sheep–human and cattle–human contact rates show that 90% of human brucellosis was small-ruminant derived. Average effective reproductive ratios for the year 1999 were 1.2 for sheep and 1.7 for cattle.

Introduction

Brucellosis is one of the world's major zoonoses (Boschiroli et al., 2001). Human brucellosis commonly is caused by exposure to infected livestock and livestock products (mostly raw milk and milk products). The clinically most-important causative bacteria in humans are in decreasing order of severity of illness: Brucella melitensis (small ruminants), Brucella abortus (cattle), Brucella suis (pigs) and Brucella canis (dogs). There is no recorded transmission of the infection between humans (Krauss et al., 1996) but humans can very rarely infect animals (Parnas et al., 1966). In humans, mortality is negligible, but the illness can last for several years (Madkour, 2001). In animals, brucellosis mainly affects reproduction and fertility, reduces survival of newborns (Sewell and Brocklesby, 1990) and reduces milk yield. Mortality of adult animals is insignificant (Sewell and Brocklesby, 1990).

Control strategies available to prevent human infection are pasteurisation of milk, livestock vaccination and the elimination of infected animals. In Mongolia, after numerous surveys in the 1960s, the World Health Organization (WHO) came to the conclusion that livestock vaccination was the only effective way to control brucellosis. The production of livestock vaccines successfully was established in the early 1970s and a country-wide mass-vaccination program of livestock planned for 11 years started in1975 under difficult field conditions. The vaccination of livestock successfully reduced human incidence of brucellosis to less than one case per 10,000 per year (Kolar, 1977). The vaccination program was interrupted in the early 1980s due to the end of WHO assistance and democratic reform followed by the shift away from dependence on the former Soviet Union in 1990; human brucellosis re-emerged. Based on a request of the Mongolian Government to WHO to provide assistance again in brucellosis control and to resurrect the vaccination program and recommendations made to the WHO and the Mongolian government (Garin-Bastuji, 1999), a whole-herd vaccination strategy covering 10 years was developed (Mikolon, 1999) to start in 2000.

Available models of brucellosis transmission consider only transmission between single livestock species and no transmission to humans, although brucellosis is transmitted to humans from both small ruminants (sheep and goat) and cattle (Roe, 1977, Carpenter et al., 1987, Dalrymple, 1993, Gonzalez-Guzman and Naulin, 1994). Our main objective was to develop a dynamic model of livestock-to-human brucellosis transmission to estimate demographic (birth rate, mortality) and transmission parameters (contact rates) between livestock and livestock to humans as an underlying basis for a cost-effectiveness analysis of a nation-wide mass-vaccination programme for livestock, which is reported elsewhere (Roth et al., 2003). Minor objectives were: (1) to fit vaccination parameters to data on the first 3 years of the national brucellosis livestock-vaccination campaign in Mongolia and (2) to simulate the brucellosis epidemic with and without specified interventions.

Section snippets

Data collection

Livestock demographic data were provided by the Mongolian Statistical Office (Mongolian Statistical Yearbook, 1999). Animal brucellosis-seroprevalence survey data (Rose Bengal; RBT) were provided at the provincial level for cattle and sheep for the years 1990–1999 by the Ministry of Agriculture for the model fit without intervention (Appendix A). The RBT is a simple and inexpensive test to detect antibodies against Brucella spp. in serum of many species. For the diagnosis of B. melitensis in

Parameter optimization without interventions

The model fitted the susceptible livestock and human populations very well (in Figs. 2a and 3, the observed and fitted values for cattle and humans overlie). The fits to the seropositive sheep and cattle and annually reported human brucellosis cases are presented in Figs. 2b and 3. In Table 1, the fitted parameters with their 95% confidence limits are presented. For sheep and cattle, the unknown proportions infectious were estimated by variation of their boundaries in a uniform distribution.

Model

To our knowledge, this reported model is the first comprehensive dynamic assessment of livestock-to-human brucellosis transmission fitted to a period of transmission with and without intervention. The model conception was adapted to the available data (only seroprevalence data), the needs of economic assessment (Roth et al., 2003) and the consideration of the Mongolian brucellosis patient registry policy to adapt the analysis to the needs and decision pathways of the Mongolian authorities (

Acknowledgements

We thank the Ministries of Health and Agriculture and Industry of Mongolia. Data were provided by D. Bat-Ochir and D. Idesh, National Centre of Infectious Diseases (Ministry of Health), D. Nyamkhorol, Statistical Information Department, Directorate of Medical Services; P. Dorjsuren and P. Bolortuya, State Veterinary and Animal Breeding Department; A. Yondondorj, Veterinary Research Institute, all in Ulaan Baatar, Mongolia. Tumurkhuu Gantsetseg provided information on clinical aspects of

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