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Elimination of Mycobacterium avium Subspecies paratuberculosis from Dairy Farms: Fact or Fiction?

Y.H. Schukken, R.M. Mitchell, A.K. Pradhan, Z. Lu, R. Smith, J. Cho, J. Dressler, L.W. Tauer, and Y.T. Gröhn
Dept. of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY.

Introduction
Johne’s disease or paratuberculosis is an infectious disease in cows, caused by Mycobacterium avium subspecies paratuberculosis (MAP). In many countries, the prevalence of MAP in dairy herds has been estimated, and these estimates are usually very close. Most studies show an apparent prevalence of infected cows in MAP infected herds in the 5-10% range (Woodbine et al. 2009, VanSchaik et al. 2003).

Given this low estimated MAP prevalence, it is surprising that no reports have been published about long-term infection-free herds. Most studies that report on the implementation of control programs, report a dramatic decrease in incidence and prevalence, but never a full elimination of the infection. An example of such a control program in a well-monitored dairy herd is shown in Figure 1 (Benedictus et al., 2007).
johnes

Clearly, Johne’s Disease eradication programs based on known MAP transmission routes were not successful in eliminating the disease from these herds. There are at least two lessons to be learned from results in Figure 1. First, there are likely more routes of MAP transmission than we currently recognize. Second, the low incidence and prevalence that were observed after implementation of control programs (after 1995 in Figure 1) are unlikely to be correct, as culling of a few infected cows would lead to elimination of MAP infection in many herds going through such a control program.

Recent studies have provided evidence for other previously not recognized routes of MAP transmission. A study by VanRoermund et al. (2007) showed that infected calves may be infectious to their peers in birth cohorts. These calves would be shedding infectious organisms and because of their close contact with susceptible individuals, transmission of infection would occur. A hallmark of such calf-to-calf transmissions would be the presence of clusters of infected animals when sorted by day of birth as shown by Benedictus et al. (2007) and Pradhan et al. (2009).

A second little recognized transmission route was recently proposed by Pradhan et al. (2009). They argued, based on molecular typing of MAP strains, that adult animal infection is an important route of transmission in dairy herds. Animals shedding very high numbers of bacteria (so called ‘super shedders’) were particularly able to infect other adult animals.

It was observed that in the presence of super-shedders in dairy herds, approximately 50% of animals other than those identified as super-shedders shed the same strain as that of contemporary super-shedders. When these low shedders were followed through to slaughter, about 60% of these suggestive adult infected cows showed a tissue infection with the same strain as the super-shedders. Thus, adult infection may be much more important than previously thought.

Estimates of true prevalence of MAP in dairy herds vary widely, mostly because of uncertainty in the ‘gold standard’ definition of infection status. Often fecal culture results are used as the gold standard, but it is also widely recognized that fecal culture results severely underestimate true infection status. Recent studies by the Regional Dairy Quality Management Alliance (RDQMA) provide strong evidence for a much higher actual prevalence of MAP infection than suggested by fecal culture results.

 In this longitudinal multi-site study, animals in three herds were followed and tested from birth to slaughter. Results are presented in Figure 2 and show that MAP infection prevalence, as estimated by culture of intestinal lymph nodes and the intestinal tract, is at least 10 times as high as the MAP prevalence estimated by fecal culture. Although these results need confirmation from other projects and investigators, the much higher prevalence of infection in dairy herds would explain the inability of current control programs to eliminate MAP from dairy farms.

Recent economic models and economic data obtained from observational studies (Groenendaal and Wolf, 2008) show that control programs for MAP in dairy farms are generally only cost-effective when best management practices, particularly with regard to calf raising, were in place.

Extensive test-and-cull strategies alone were shown to be ineffective and costly for producers (Groenendaal and Wolf, 2008). Milk production loss linked to MAP infection was studied across a number of longitudinally followed populations (Nielsen et al., 2009, Smith et al., 2009).
johnes2

In both of these studies, animals known to be infected with MAP, but shedding low bacterial numbers, did not show an important milk production loss relative to uninfected controls. Only when cows started to shed larger numbers of bacteria or when MAP ELISA values were increased for a prolonged period of time was a discernable effect on milk production present (Smith et al. 2009, Nielsen et al. 2009). These data would also indicate that test-and-cull strategies may be costly when applied across all MAP infected animals.

Models to Study MAP Infections
Mathematical modeling to study MAP infections in dairy herds has been proposed (Lu et al., 2008). With these mathematical infection models, MAP infections in herds can be simulated and studied. These models try to reflect the biology and epidemiology of MAP as realistic as possible, but often relatively simple models are used to study simulated infections. Despite their simplicity, mathematical models have shown to be useful in obtaining a better understanding of MAP transmission on dairy farms.

Some important results include the prediction that calf-to-calf transmission may play an important role in infection maintenance, the quantification of the importance of super-shedders in herds and a full understanding of the value of test-and-cull control programs in dairy herds (Lu et al. 2008). These mathematical models also provide a more generic insight into MAP infection dynamics in dairy herds.

The basic reproduction ratio or R0 of a contagious disease is defined as the number of secondary infections after the introduction of a single infectious individual in a susceptible population (herd). A threshold value of 1 for R0 distinguishes successful control measures (R0 < 1) from non-successful or a lack of control measures (R0>1). In Figure 3, the relationship between the R0 value and the endemic infection prevalence is shown. When the R0 value is below 1, the endemic prevalence is stable at zero. With increasing R0, or a lack of control measures, the endemic infection prevalence increases in a sigmoid fashion (line A). Under normal circumstances, prevalence would decrease again along the same sigmoid curve (line A) when infection control measures are implemented (R0 will become smaller). However, with some endemic infections prevalence will initially not decrease, but remain high despite the reduction in R0 value to values below the threshold value of 1 (Line B).

Under these circumstances there is a situation possible where there is a high prevalence of infection in a management situation where a new introduction of MAP infection would not be successful (Line C). This phenomenon is defined as backward bifurcation (Figure 3). There are a number of reasons to believe that the backward bifurcation phenomenon is present in the case of MAP infections in dairy herds.
johnes3

First, environmental contamination and MAP survival in the environment may lead to a backward bifurcation; second, the presence of dose dependency in the likelihood of calfhood shedding status and the subsequent increased rate of development into a super-shedder also will result in a backward bifurcation.

These findings would imply that in endemically MAP-infected herds, the effort to control the infection will be much more elaborate than what may have been predicted based on introduction of the infection in a dairy herd. This difficulty to fully control MAP appears to be present in many dairy herds in virtually all countries with reported MAP prevalence data.

Summary
Is elimination of MAP from dairy herds fact or fiction? To answer this question we need to consider a number of arguments. The key arguments are that 1) within herd prevalence is much higher than measured using current diagnostic tools; 2) several currently underestimated transmission routes of infection appear to be important for infection maintenance in dairy farms; 3) aggressive test-and-cull based control programs are not economically feasible in modern dairy farms; and, 4) endemically infected dairy herds will need to employ extensive MAP control programs to overcome the impact of backward bifurcation in MAP infection dynamics. Based on these arguments, combined with observed data across all dairy herd populations it appears that MAP elimination from dairy farms is more fiction than fact.

Acknowledgements
The authors are supported in part by the USDA-Agricultural Research Service (Agreements. 58-1265-3-155, 58-1265-3-156, 58-1265-3-158, 58-1265-4-020, and 58-1265-8-064) for the Regional Dairy Quality Management Alliance (RDQMA) and the Johne’s Disease Integrated Program (JDIP, USDA contract 45105).

REFERENCES
Benedictus A., Mitchell RM., Linde-Widmann M., Sweeney R., Fyock T., Schukken YH., Witlock, RH, 2008. Transmission parameters of Mycobacterium avium subspecies paratuberculosis infections in a dairy herd going through a control program. Prev Vet Med 83:215-227.

Groenendaal H, Wolf CA. 2008. Farm-level economic analysis of the US National Johne's Disease Demonstration Herd Project. J Am Vet Med Assoc. 233:1852-1858.

Lu Z, Mitchell RM, Smith RL, Van Kessel JS, Chapagain PP, Schukken YH, Grohn YT. 2008. The importance of culling in Johne's disease control. J Theor Biol. 254:135-146.

Nielsen SS, Krogh MA, Enevoldsen C. 2009. Time to the occurrence of a decline in milk production in cows with various paratuberculosis antibody profiles. J Dairy Sci. 92:149-55.

Pradhan AK, Van Kessel JS, Karns JS, Wolfgang DR, Hovingh E, Nelen KA, Smith JM, Whitlock RH, Fyock T, Ladely S, Fedorka-Cray PJ, Schukken YH. 2009. Dynamics of endemic infectious diseases of animal and human importance on three dairy herds in the northeastern United States. J Dairy Sci. 92:1811-1825.

Smith RL, Grohn YT, Pradhan AK, Whitlock RH, Van Kessel JS, Smith JM, Wolfgang DR, Schukken YH. 2009. A longitudinal study on the impact of Johne's disease status on milk production in individual cows. J Dairy Sci. 92:2653-2661.

van Roermund HJ, Bakker D, Willemsen PT, de Jong MC, 2007. Horizontal transmission of Mycobacterium avium subsp. paratuberculosis in cattle in an experimental setting: calves can transmit the infection to other calves. Vet Microbiol. 122:270-279.

van Schaik G, Schukken YH, Crainiceanu C, Muskens J, VanLeeuwen JA. 2003. Prevalence estimates for paratuberculosis adjusted for test variability using Bayesian analysis. Prev Vet Med. 60:281-295.

Woodbine KA, Schukken YH, Green LE, Ramirez-Villaescusa A, Mason S, Moore SJ, Bilbao C, Swann N, Medley GF. 2009. Seroprevalence and epidemiological characteristics of Mycobacterium avium subsp. paratuberculosis on 114 cattle farms in south west England. Prev Vet Med. 89:102-109.

 

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