Materials and Methods

Sample population—Data were extracted for the period from 1998 through 2006 from the Minnesota Board of Animal Health generic database through the assistance of Board of Animal Health staff members. For numbers of participating cattle herds in the program, data were summarized at the end of each year. The MNJDCP herds were categorized on the basis of cattle type (dairy or beef) and category of program participation (Management Program or Test-Negative Program). Herds participating in the Management Program included cattle herds making efforts to control Johne's disease, with or without testing of the herd and without herd classification, and herds participating in the Test-Negative Program included herds at levels 1, 2, 3, or 4 of the Voluntary US Johne's Disease Test-Negative Program.

Data analysis—Herd participation in the program was calculated as the proportion of Minnesota dairy or beef cattle herds participating in the Minnesota Management or Test-Negative Program; the denominators were the estimated number of cattle herds (dairy or beef) in the state by type with at least 1 adult cow, as reported by the USDA National Agricultural Statistics Service.¹² Funding information regarding expenditures for testing, including veterinary fees for collection of biological samples as well as fees for veterinarian completion of risk assessments, was provided by the Minnesota Board of Animal Health.

Data on management practices and herd size were determined annually from Johne's disease risk assessments completed by certified veterinarians.¹³ Herd size was recorded as the number of adult cows in the herd from the Johne's disease risk assessment. When information on herd size changed during the years a herd participated in the program, data from the most recent (up to 2006) Johne's disease risk assessment were used because these data were not maintained in the database from earlier years. Some herds did not have annual risk assessments and therefore were not included in certain analyses when data were unavailable (eg, rates of participation on the basis of herd size). Thus, the numbers of herds for each analysis were reported. A comparison of herd participation on the basis of herd size was performed by use of the χ² test of association.

Management changes were assessed in herds that were initially participating in the Johne's Disease Management Program because these herds were considered infected with the agent that causes Johne's disease and implemented a control program. Risk scores from the Johne's disease risk assessment are considered a measure of risk of transmission of Johne's disease. For dairy herds, scores are assigned on a scale of 0 to 80 for calving area risks (with a higher score indicating a higher risk of transmission), 0 to 50 for preweaned calves, 0 to 30 for weaned calves, 0 to 24 for bred heifers, and 0 to 16 for adult cattle for a total of 200 maximum points for the on-farm score. Beef cattle herds have a maximum score of 180. An additional score from 0 to 60 is given for replacement cattle risks for an overall total of 260 for dairy herds (240 for beef herds). For year-to-year comparison of scores, the on-farm score (a summary of scores for the calving area, preweaned calves, weaned calves, bred heifers, and adult cattle but excluding replacement cattle) was considered the best summary score for evaluating management changes during the program because the on-farm score is a measure of within-herd Johne's disease transmission risk. Total score was modified by the addition of the risk score for replacement cattle starting in 2002, but this change did not affect on-farm scores. For comparisons among years, the median risk score for each year was calculated from available risk assessments. Within-herd reduction in risk scores was calculated as the change in the risk assessment score between the first year the herd participated in the Management Program and a subsequent year. For evaluation of differences from the starting risk scores (reduction in risk scores), 95% confidence intervals of the mean differences were estimated.

Estimates of Johne's disease herd testing results were calculated from available herd test information from the Minnesota Board of Animal Health. Because Johne's disease is a reportable disease to the Minnesota Board of Animal Health, all Johne's disease test results were required to be submitted to the agency. These test results were predominantly from the Minnesota Veterinary Diagnostic Laboratory, which was the official laboratory of the Minnesota Board of Animal Health and therefore performed most of the tests in the state, although other laboratories also reported test data. Annual within-herd apparent seroprevalence for Johne's disease for each herd was estimated by use of data from nonvaccinated cattle herds that tested at least 20 cows (these herds were initially categorized as Johne's Disease Management Program herds). Within-herd apparent seroprevalence estimates were calculated by use of the number of cows with positive results for an ELISA divided by the number of cows tested by use of an ELISA at any point within a calendar year. No adjustments were made for cows tested more than once throughout the year because this information was not available. Data were reported as median withinherd seroprevalences for each year. Within-herd reduction in seroprevalence by year in the program reflected the difference between ELISA-determined within-herd seroprevalence from the first year the herd participated in the Johne's Disease Management Program and any subsequent year. For evaluation of significance of mean differences of seroprevalence by year in the program, 95% confidence intervals of mean differences by year in the program were estimated. Values of P < 0.05 were considered significant.

Results

Herd participation—Several states participated in the VBJDCP in 2006, but Minnesota had the highest number of cattle herds participating in the program^11,a (Table 1). Results from analyses of MNJDCP data revealed steady increases in program participation by dairy producers such that 1,663 (30.8%) Minnesota dairy producers participated in the Johne's Disease Management Program or Test-Negative Program in 2006 (Table 2). Much of the program growth has been since 2002. Herd participation in the Johne's Disease Management Program was related to herd size, with larger herds being significantly (P < 0.001) more likely to participate than smaller herds (Table 3). In 2005 through 2006, 52.9% of Minnesota dairy herds with 500 or more cows participated in the Management Program, compared with only 9.9% of herds with < 50 cows. Participation by herds in the Test-Negative Program increased over time, with 513 (9.5%) Minnesota dairy herds participating in 2006. Participation by beef producers also increased over time but at a lower rate, compared with that for dairy herds, with 320 (2.1%) beef producers participating in the program in 2006. In 2006, only 0.8% of Minnesota beef herds participated in the Test-Negative Program.

The MNJDCP started with state funding in 1998, with nearly $158,000 expended by the Minnesota Board of Animal Health for testing of herds (Figure 1). Since that time, state and federal funding for support of laboratory testing, veterinary fees for sample collection, and veterinarian completion of herd risk assessments increased to a peak of $571,000 in 2005, then decreased slightly to $556,000 in 2006. The surge of funding from the federal government for the cooperative State-Federal Control Program began in 2003; since that time, an increasing proportion of MNJDCP funds have been spent on completion of risk assessments and development of herd management plans by veterinarians. Overall, increased herd participation was directly correlated (r = 0.97; P < 0.001) with the increase in funds spent for these program activities. These data do not include funds spent on other aspects of the MNJDCP, such as expenses for time and travel costs of federal and state veterinarians in support of the program, nor funds spent by cattle producers on testing.

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Funding for the MNJDCP for testing and risk assessments by certified herd veterinarians (triangles) and number of cattle herds in the MNJDCP (squares) since its inception in 1998.

Citation: Journal of the American Veterinary Medical Association 233, 12; 10.2460/javma.233.12.1920

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Herd management changes subsequent to participation in the Management Program—Estimates of transmission risks for Johne's disease, which were available from analyses of risk assessments, revealed that many Minnesota cattle herds introduced cattle to their operations from other herds. In 2004, 36.3% of the 510 dairy herds in the Management Program and 43.3% of the 60 beef herds in the Management Program indicated that they had introduced cattle during the preceding year. Little change was evident for 2005, with 42.4% of 663 dairy herds and 45.6% of 68 beef herds, or 2006, with 33.8% of 672 dairy herds and 41.7% of 96 beef herds. Overall, Johne's Disease Management Program on-farm risk assessment scores for dairy herds decreased only marginally over time, although total scores remained relatively constant as a result of the addition of risk score from introduction of replacement cattle starting in late 2002 (Table 4). Although the median replacement cattle risk score for dairy and beef herds since 2003 was zero, which reflected the fact that fewer than half of the herds introduced cattle during any specific year, the mean replacement cattle score for dairy herds was 14.0, 11.1, 11.8, and 11.2 for years 2003, 2004, 2005, and 2006, respectively; the score for beef herds was 2.0, 10.7, 15.2, and 11.6 for the same years, respectively.

However, dairy herds in the Johne's Disease Management Program had reduced on-farm risk assessment scores (mean of 10.5 for the first year of participation in the control program and 18.1 for the first 2 years of participation in the control program; Table 5). These reductions were maintained during subsequent years of program participation. Similarly, beef herds in the Johne's Disease Management Program had substantial reductions in on-farm risk assessment scores.

Changes in within-herd seroprevalence subsequent to participation—Among dairy cattle herds in the Johne's Disease Management Program that tested at least 20 cows by use of a serum ELISA in a given year that were included in this assessment, the median number of cows tested per year was 95 cows (25th to 75th percentiles, 49 to 183 cows) in 2001, 78 cows (25th to 75th percentiles, 45 to 135 cows) in 2002, 68 cows (25th to 75th percentiles, 41 to 116 cows) in 2003, 54 cows (25th to 75th percentiles, 30 to 104 cows) in 2004, 30 cows (25th to 75th percentiles, 30 to 57 cows) in 2005, and 30 cows (25th to 75th percentiles, 30 to 70 cows) in 2006. Among this group of dairy herds, the median seroprevalence decreased from 9.9% in 2002 to 3.4% in 2006 (Table 6). The mean reduction in seroprevalence (as determined by results of an ELISA) was 1.1% from year 1 to year 2 in the program, 2.6% from year 1 to year 3 in the program, 4.0% from year 1 to year 4 in the program, and 4.9% from year 1 to year 5 in the program (Table 7). Lower participation rates of beef herds, compared with the participation rates of dairy herds, limited interpretation of study results, but a substantial reduction in within-herd seroprevalence was detected for beef herds that participated in the Johne's Disease Management Program for at least 3 years. In addition, 103 dairy herds and 52 beef herds initially in the Management Program with at least 20 cows tested by use of a serum ELISA within a specific year qualified for and entered the Test-Negative Program by 2006.

Discussion

The evaluation reported here was conducted with data for testing of herds and risk assessments collected longitudinally by the Minnesota Board of Animal Health. This study was designed to describe herd management and Johne's disease in cattle herds participating in the MNJDCP. The retrospective design of this assessment resulted in lack of control for selection of herds and missing information on risk assessments and seroprevalence from some herds during certain years. As such, this study was not designed to evaluate cause and effect of the control program, as could be done in a controlled clinical trial. Instead, the objective of this study was to measure change in specific Johne's disease outcomes and their correlation with duration of participation in the control program. One important result from this study was the steadily increasing number of Minnesota cattle herds that participated in the program, especially after federal funding was initiated in 2003.

Another study limitation was the use of available data on serologic testing for estimation of seroprevalence. Few herds used bacterial culture of fecal samples from individual cows for diagnostic testing because of higher costs, and therefore, results of bacterial culture of fecal samples were not used in this study. For estimation of within-herd seroprevalence, we used data from herds that tested at least 20 samples during each year in the program. Although 20 samples/herd provides only a crude estimation of apparent seroprevalence, most herds had substantially more samples tested each year, and we used all available ELISA results for this estimation. Another limitation was the reliance on risk scoring by veterinarians for the assessment of change in management practices because of the possibility that some veterinarians may have wanted to provide positive feedback to producers in the program through a reduction in scores over time. Although a degree of subjectivity of the risk scoring system is inherent, the veterinarians completing the risk assessments did receive training and certification to complete this task.

One critical aspect of the VBJDCP is the identification of low-risk (test-negative) herds. A major risk factor for infected herd status is introduction of infected cattle,¹⁴ and results from the assessment revealed the continued risks posed for herds whose owners purchased cattle. Testing of randomly selected replacement cattle of unknown infection status is less effective in reducing risk of herd infection than is purchase of cattle from test-negative programs.¹⁵ Therefore, a ready source of identified low-risk cattle from herds participating in a low-risk herd classification program is necessary to meet the needs of the US dairy and beef industries. Results from the MNJDCP indicated a steady increase in the number of these low-risk herds.

Herds with more cows were more likely to participate in the Johne's Disease Management Program, compared with participation of herds with fewer cows, perhaps because of the higher likelihood of infection with M avium subsp paratuberculosis, which was reported in the most recent national study.¹ This association was also reported in an earlier analysis of data from MNJDCP herds that included data up to February 2004.¹⁶ One reason for this increased likelihood of infection is that larger herds are more likely to introduce cattle from other herds than are herds with fewer cows.¹⁷ Some of these larger herds may have recently attempted herd expansions through purchase of cattle, which has the potential to result in high incidence of cows with clinical Johne's disease. Certainly, larger herds have a larger potential financial risk from Johne's disease, which may be reflected in higher participation rates in Johne's disease control programs.

Analysis of the results also revealed a reduction in risk of transmission of Johne's disease and a reduction in seroprevalence of Johne's disease over time for dairy herds in the MNJDCP Management Program, which is consistent with a positive effect of the control program. Because there were fewer beef herds participating in the program, less inference can be drawn for the beef herds. However, the available evidence indicates a similar beneficial effect in beef herds. The earlier analyses of MNJDCP data¹⁶ (which did not include approximately 3 years of program data included in the study reported here) revealed a similar reduction in risk scores from the first score to most recent score in program herds. However, a reduction in seroprevalence in herds participating in the program was not identified at that time.

The data reported here were consistent with results for Minnesota dairy herds in the NJDDHP. Results from the Minnesota demonstration herds,¹⁸ which were summarized as part of the NJDDHP, revealed that implementation of a Johne's disease control program through the use of management practices and test information resulted in a reduction in seroconversion and shedding of infectious organisms in feces. It was suggested in that study¹⁸ that reduction of environmental contamination of heifers < 1 year old had measurable impact on the success of the program and that the NJDDHP appeared more beneficial for herds that achieved a greater reduction of the risk assessment score.

As a state, Minnesota has the highest number of cattle herds participating in the VBJDCP (Table 1). One advantage of the program in Minnesota was the availability of state funding prior to initiation of federal funding, which generated early development and implementation of the program. Several other states also reported high participation rates, and the results reported here for the Minnesota producers were expected to be typical of results in other states with active Johne's disease control programs. The evidence from this study is consistent with the effectiveness of the control program, and continued funding is needed to support progress of the program. Currently, several funding options are available for the national program. These options include continuation of federal funding for the program (federal-funded program), reduction of federal funding for the program without replacement from an off-farm source (producer-funded program), or reduction of federal funding for the program and replacement with funding from another source (other-funded program).

At this time, the federal-funded option appears to be at risk because of other priorities of the USDA. Funding through APHIS has already decreased from a high of $21 million in 2003 to $12 million in 2007. Additional funding cuts are likely, especially without an increased focus and lobbying by producer groups. Without federal funds and without replacement of those funds from another source, the VBJDCP is at risk. Critical components of the program, including policy development and coordination, education, completion of risk assessments, and herd testing are expensive. Participation by herds is expected to decrease without funding support. The third option of replacement of some or all of the federal funds for this program by another funding source may be the best opportunity for long-term success of the program. Potential options available include state or industry funding. Whatever the source of funding, a sustained program is believed to be necessary for national control of this disease in cattle and other livestock species.

Despite the risk of reduction in federal funding for the VBJDCP, positive enhancements can be implemented to maintain critical program components while potentially increasing the efficiency of available funding. One critical component of the VBJDCP is communication between the certified veterinarians for each of the herds, federally employed veterinarians, and cattle producers. This relationship is necessary to ensure completion of risk assessments and herd plans (including review of principles for control of Johne's disease and identification of high-priority mitigations). In the study reported here, completion of risk assessments (with the associated education delivered as part of the process) was associated with reduced risk scores and reduced within-herd seroprevalence of infection over time for herds participating in the Johne's Disease Management Program. In addition, recent advances and understanding of diagnostic tests have identified alternatives that can reduce test costs through the use of less expensive tests and more efficient test strategies. The use of inexpensive testing options (including testing of milk with an ELISA) can reduce the cost of herd monitoring.^19,20 In addition, new herd testing strategies can accurately identify herd infection status at a reasonable cost.²¹ Improved information about the value of specific on-farm management practices is expected in the near future as a result of clinical trials and related studies, such as the NJDDHP. Information generated from these and other studies is expected to help identify ways to reduce the overall cost of Johne's disease control programs.

Analysis of results for the study reported here indicated that in a state with high participation of dairy producers in the VBJDCP, an assessment of herds enrolled in the Johne's Disease Management Program revealed a reduction in risk of transmission of Johne's disease and in seroprevalence of Johne's disease over time. These data from Minnesota cattle herds with active Johne's disease control programs were consistent with confirmation of the effectiveness of the VBJDCP in reducing the incidence of Johne's disease in dairy and beef herds.